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What are the major evolutionary pressures for Bioluminescence?
In many cases, and in particular in marine invertebrates, the bioluminescence is in fact produced by symbiotic bacteria of the Vibrionaceae family. In most cases the bacteria can sense when they are being hosted by the animal through quorum sensing mechanisms, and start producing light.
The evolutionary pressure for the bacteria to produce light is to be in the protected environment of the animal which often feeds them. On the animal side, there can be several reasons to host the luminescent bacteria. In many cases, the evolutionary pressure is linked to reproduction. In order to successfully reproduce in the immensity of oceans, marine animals need to know that they are among their kind before they release their gametes.
Another example is the one of some deep see fish like the anglerfish which have developed a special "flash light" organ to host bio-luminescent bacteria. Fish can use the bacteria to emit a light to aid in camouflage, hunting, and attracting mates. See http://microbewiki.kenyon.edu/index.php/Deep_sea_fish
Bioluminescence, in particular in marine organisms, has also been linked to way to get rid of reactive oxygen species (ROS). In fact, luciferases catalyse the photogenic oxydation of luciferins. In , the authors propose that this system's function was primarily for antioxydation, while in deep seas, where the water is oxygen-poor, the lower selective pressure toward antioxydation would have given rise to light emitting functions in specialized organs.
THE ORIGINS OF MARINE BIOLUMINESCENCE: TURNING OXYGEN DEFENCE MECHANISMS INTO DEEP-SEA COMMUNICATION TOOLS
Bioluminescence in the Ocean: Origins of Biological, Chemical, and Ecological Diversity
Chapter 25 - Bioluminescence
This chapter discusses living light or bioluminescence in insects. It is most commonly is produced in tissues or organs within and shines out of the emitter's body, but some organisms ooze or squirt luminous secretions, some even smear them on attackers. The light-emitting layer is organized into a sheet of rosettes, each with a central channel (cylinder), through which airsupply tubes and nerve trunks pass. Analysis of adult morphology and DNA suggest that the flashing lantern, that is, one capable of emitting short bursts of light, evolved independently at least twice and possibly three times, indicating that structural similarities in divergent lampyrid groups are due to evolutionary convergence. Self-lighting species appear in all four kingdoms — Monera, Fungi, Plantae, and Animalia –—in 11 of 29 phyla. But the best-known insect bioluminescence is that of beetles of the family Lampyridae, known as fireflies, lightningbugs, blinkies, and many other local and colloquial names. Bioluminescence chemistry varies among organisms. Bacteria use riboflavin phosphate, sea pansies use diphosphoadenosine, and fireflies use adenosine triphosphate (ATP) in the oxidative decarboxylation of substrates generically known as luciferins, with enzymes termed luciferases. A tentative conclusion would be that bioluminescence has evolved from many separate biochemical origins.
Evolutionary Pressures in Reptiles
The reptiles have striking adaptations for terrestrial life.
Adaptations in Chuckwalla (Sauromalus obesus)
It lives in the deserts of Southwestern United States. It has following adaptations:
(i) Adaptation in summer: It can survive in late summer at temperate above 40 degree centigrade. Chukwallas browse on plants. These plants wither. Therefore, chuckwallas aestivate to withstand these hot and dry conditions. Chukwallas disappear below ground during aestivation.
(ii) Adaptation for winter:
Temperature becomes model ate during the winter. But little rain falls. Thus lift in the desert is still not possible. Therefore, summer sleep of chuckwalla enters into winter sleep. Rain fall started in March. Therefore, greenery and appears in the desert. The chukwalla comes out from sleep. The chuckwalla browses and drinks water. It stores large amount of water under its skin.
(iii) Defense from predators: Predators cannot prey chukwallas easily. If threatened, a chukwalla enters into rock crevice. It inflates lungs with air. It increases its forms a wedge entrance or the rock walls. There is friction of its the rocks. Therefore, chukwalla cannot be removed from rock.
EXTERNAL STRUCTURE AND LOCOMOTION
Skin of reptiles has no respiration functions. Reptilian skin is thick, dry or keratinized. Scales are modified for various functions. For example, the snakes have large belly scales. The scales provide contact with the substrate during locomotion. Reptilian skin is less glandular than that of amphibians. Skin glands secrete phermones. These pheromones functions in sex recognition and defense.
The chromatophores of reptiles are dermal in origin. Cryptic coloration, mimicry and aposematic coloration occur in reptiles. Colors also function in sex recongnition and thermoregulation.
The process in which reptiles periodically shed their outer epidermal layers of then is called ecdysis. All reptiles undergo ecdysis. The blood supply to the skin does not move in the epidermis. The outer epidermal cells lose contact with the blood supply and die. The lymph moves between moves the inner and outer epidermal layers. It loosens the epidermis. Ecdysis begins in the head region. The epidermal layers come off in one piece in many lizards and snakes . In other lizards, epidermal layers broken into small pieces. The frequency of ecdysis is different in different species . It occurs more in young than in adults.
Suppport and Movement
The reptailians are inherited skeleton from ancient amphibians. The skeletons of reptiles show many notifications. The skeleton is highly ossified. Thus it provides greater support.
1. Skull: Their skull is longer than that of amphibians. They have secondary palate. Secondary palate partially separates the nasal passages from the mouth cavity. Palate was evolved in archosaurs. It was an adaptation for breathing when the mouth is full of water or blood. It is also present in other reptiles. They also have longer snouts. It increases the sense of olfaction.
2. Vertebrae: Reptiles have more cervical vertebrae than amphibians. The first two cervical vertebrae are atlas and axis. They provide greater freedom of movement to head. An atlas articulates with a single condyle on the skull. It helps in nodding. Axis is modified for rotational mo ements. They have different number of cervical vertebrae. It provides additional neck flexibility.
3. Ribs: The ribs of reptiles may be highly modified. The ribs of snakes have muscular connections to large belly scales. It helps in locomotion. The cervical vertebrae of cobras are attached with some special ribs. Cobra flares these ribs in aggressive displays.
4. Pelvic girdle: The pelvic girdle is attached to the vertebral column by two or more sacral vertebrae.
5. Autotomy: The caudal yertebrae ot man !um ds possess a vertical fracture plane. If a lizard is grasped by the tail, caudal vertebrae are broken. Therefore a portion of the tail is lost. The loss of tail is called autotomy. Autotomy is an adaptation that allows a lizard to escape from a predator. Sometimes, the predator runs away from lizard after seeing its broken moving tail. The lizard later regenerates the lost portion of the tail.
There are three types of locomotion in reptiles:
1. Locomotion in primitive reptiles is similar to salamanders. The body move low between paired appendages. The appendages extend laterally and move in the horizontal plane.
2. The limbs of other reptiles are elongated and slender. They remain closer to the body. The knee and elbow .joints rotate posteriorly. Thus, the body moves higher from the ground. Thus the legs support the both vertically.
3. Many prehistoric reptiles were bipedal. The walking on the hind limbs is called bipedalism. They had a narrow pelvis. Ihey have a heavy outstretched tail for balance. Bipedal locomotion treed the front appendages. Thus these appendages are used capturing of prey or flight in some animals.
NUTRITION AND THE DIGESTIVE SYSTEM
Tongue: Most reptiles are carnivores. But turtles eat almost all the things. The tongues of the turtles and crocodilians are nonprotrusible. It helps in swallowing. Some lizards and the tuatara late sticky tongues. It is used or capturing the prey. The extended tongue of chameleons exceeds their body length.
Modification in snakes for swallowing
The skulls of snakes are greatly modified for feeding. The bones of the skull and jaws are attached loosely. These bones move away from for ingestion of prey. In this way, snakes can ingest larger than a snake’s normal head size. The bones of the upper jaw on the skull. The halves of both of the upper and lower jaws are attached loosely by ligments at anterior side. Therefore, each half of the upper and lower jaws can move independently. Opposite sides of the upper and lower jaws are moved forward and retracted alternately alter the capturing of prey. Their teeth are posteriorly pointed. These teeth prevent the prey from escaping. They also force the food into the esophagus.The glottis is much forward in snake. Thus they can breathe during swallowing of prey.
Biting apparatus and biting mechanism
Vipers possess hollow fangs. These fangs are present on the maxillary bone at the anterior margin of the upper jaw. These fangs are connected to venom glands. The Maxillary Bone of the vipers is hinged. It can moved backwards. Thus when the snake mouth is closed the fangs fold back and it lie along the upper jaw. When the mouth opens, the maxillary bone rotates. It swings down the fangs. Thus the fangs project outward from the mouth. Now vipers may strike at objects.
2. Rear fanged snakes
Rear-fanged snakes have groove in rear teeth. Venom is passed through grooves and injected into the prey during swallowing.These snakes usually do not bite.Therefore, they are harmless to humans. However, the African boomslang (Dispholidus typus) have killed men.
3. Coral snake, sea snake and cobra
The fangs of coral snakes, sea snakes. and cobras are attached to the upper jaw. It remains in an erect position in opened mouth. The fangs lit into a pocket in the outer gum of the lower jaw when the mouth is closed. Fangs have a groove or it is hollow. The muscles of the venom glands contract and inject venom into the fangs. Some cobras can spit venom at its prey. This venom may cause blindness.
Venom glands are modified salivary glands. The venoms of most snakes are mixtures of neurotoxins and hemotoxins.
1. Neurotoxin: Neurotoxin attacks on nerve centers. It causes respiratory paralysis. The venoms of coral snakes, cobras, and sea snakes are neurotoxins.
2. Hemotoxins: Hemotoxins break blood cells. It attacks blood vessel linings. The venoms of vipers are primarily hemotoxins.
GAS EXCHANGE AND TEMPERATURE REGULATION
Th circulatorysystem of reptiles is based on amphibians. The blood of reptiles must travel under high pressures.
1. The reptiles possess two atria. These atria are completely separated in the adult. Veins from the body and lungs open into them. The sinus venosus is absent in reptiles except in turtles. It has become a patch of cells and act as a pacemaker.
2. The ventricle of most reptiles is incompletely divided. The ventricular septum is complete only in crocodilians .
3. The ventral aorta and the conus arteriosus divide during development. They form three major arteries that leave the heart.
(a) A pulmonary artery: It leaves the ventral side of the ventricle. It takes blood to the lungs. •
(b) Two systemic arteries: One systemic artery arises from the ventral side of the heart. Second systemic arterv arises from the dorsal side of the heart. It takes blood to the lower body and the head.
Circulation of blood
The deoxygenated blood enters into the ventricle from the right atrium. It leaves the heart through the pulmonary artery and moves to the lungs. Pulmonary veins bring oxygenated blood from lungs and transfer it into left atrium. Blood then enters into the ventricle from. It leaves the heart through left and right systemic arteries.
Mixing of blood: An adaptation
There is incomplete separation of the ventricle in most reptiles. The pulmonary artery contracts and some blood moves from pulmonary circuit to the systemic circuit. All reptiles do not breathe constantly. Therefore, the movement of blood from pulmonary circuit to systemic circuit has advantage for reptiles. The breathing by lung stops when turtles withdraw into their shells. They also stop breathing during diving. During periods of apnea (“no breathing “ ), blood flow to the lungs is limited. It conserves energy. It allows more efficient use of the pulmonary oxygen supply .
Reptiles exchange respiratory gases through internal respiratory surfaces. Thus they do not lose large quantities of water. Larynx is present in them. However, vocal cords are absent in them. Cartilages support the respiratory passages of reptiles. Their lungs are partitioned into sponge like interconnected chambers. Lung chambers provide the large surface area or gas exchange.
Mechanism of respiration in most reptiles
Negative-pressure mechanism is responsible for lung ventilation. A posterior movement of the ribs and the body wall expands the body cavity. It decreases pressure in the lungs. Thus lung draws air into the lungs. Elastic recoil of the lungs and forward movements of the ribs and body wall compress the lungs. Thus air is expelled out of it.
Mechanism of respiration in turtles
The ribs of turtles are a part of their shell. Thus movments of the body wall and ribs arc impossible. Therefore, turtles exhale by contracting muscles. These contractions force the viscera (Internal organs) upward and compress the lungs. They inhale bv contracting muscles that increase the volume of the visceral cavity. It creates negative pressure lung. This pressure draws air into the lungs.
The terrestrial animals face high temperature (65 to 70°C). This temperature is not suitable for life. Thus temperature regulation is important in terrestrial animals. Reptiles inn be:
1. Ectotherms: The animals which use external heat sources for thermoregulation arc called ectotherms. Most reptiles are ectotherms.
2. Endotherms: The animals which generate internal heat during metabolism are called endotherms. Some reptiles like monitor lizards and brooding Indian pythons arc endotherms. Female pythons coil around their eggs. It raises its body temperature by 7.3oC above the air temperature. It uses metabolic heat to raise this temperature.
Reptiles regulate their body temperature by following methods.
1. Heat regulation by hibernation and aestivation: Some reptiles can survive in wide temperature fluctuations (2 to 41 o C or some turtles). However, body temperatures are regulated within a narrow range between 25 and 37 o C. If they are unable to maintain this range, they remain within the range in this retreat.
2. Behavioral methods of heat regulation: Most thermoregulatory activities of reptiles are behavioral. A lizard orients itself at right angles to the sun’s rays to warm itself. It presses its body tightly on a warm surface to absorb heat by conduction. A lizard orients its body parallel to the sun’s rays to cool itsels. It seeks shade or burrows. It take its body erect prostrate (legs extended and tail arched) to reduce conduction from warm surfaces. Many reptiles are nocturnal in hot climates.
3. Physiological methods of heat regulation: Various physiological mechanisms also regulate body temperature. Some reptiles use panting for releasing neat. Panting releases heat through evaporative cooling. Marine iguanas absorb heat by basking in the sun. It divert blood to the skin and arm up quickly. Marine iguanas reduce heart rate and blood flow to the skin during ing into the ocean. It slows down heat loss. Chromatophores also help in emperature regulation. Dispersed chromatophores increase the rate of heat bsorption.
4. Heat regulation by torpor: Many temperate reptiles withstand cold winter temperatures by entering into torpor. Torpor is an inactive stage. The body temperatures and metabolic rates decrease during torpor. The body temperatures of reptiles in torpor are not regulated. It is a difference from the true hibernators.
5. Heat regulation by hibernacula: The solitary reptiles migrate to a common site and spend winter there. These animals clumped together. Heat loss from these groups is called hibernacula. Exposed surface area reduces hibernacula. Sometimes, the animals can freeze and die in cooler winter. Death from freezing is an important cause of mortality for temperate reptiles.
NERVOUS AND SENSORY FUNCTIONS
The brain of reptiles is similar to the brains of other vertebrates. The cerebral hemspheres are larger than amphibians. This increase of size of brains has improved the smell. The optic lobes and the cerebellum are also enlarged. It shows that reptiles much depend on vision. They have better coordination of muscle functions.
The reptiles have complex sensory systems. It is evidenced by a chameleon’s method of feeding. It has protruding eyes. Its eyes move independently. Each eye has different field of view. Initially, the brain keeps both images separate. But when they an insect, both eyes converge on the prey. As a result binocular vision is formed. It helps chameleon to determine whether the insect is within range of the chameleon s tongue.
(a) Focusing mechanism: Vision is the dominant sense in most reptiles. Their eves are similar to amphibians. Snakes moves the lens forward for focusing the nearby objects. Iris contract and places pressure on itrcous body. Vitreous both is gel-like in the posterior region of the eye. The displacement of this gel pushes the lens forward. All other reptiles have different method to locus on nearby objects. Their ciliary muscles press the ciliary body against the lens. It changes the shape of lens from elliptical to more spherical. The spherical lens is used for focusing on nearby object. Reptiles have a greater number of cones than amphibians. Thus they have well-developed color vision.
(b) Protection: The eyes of reptiles have upper and lower eyelids, a nictitating membrane and a blood sinus. These structures protect and cleanse the surface of are eye. In snakes and some lizards, the upper and lower eyelids fuse in the embryo. It forms a protective window of clear skin called the spectacle. The blood sinus is present at the base of the nictitating membrane. It swells with blood and force debris to the corner of the eye. It is rubbed out from this corner. Horned lizards rupture this sinus and blood come out from it. It is a defensive act to confuse the predators.
(c) Median eye: Some reptiles possess a median (parietal) eye. This eye is developed from outgrowths of the roof of the forebrain. In the tuatara, this eye has a lens, nerve and a retina. The parietal eye is less developed in other reptiles. Parietal eyes are covered by skin. Thus it cannot form images. However, parietaleye can differentiate light and dark periods. Thus it is used to locate the position of the sun.
The structure of reptilian ears varies. The ears of snakes detect substrate vibrations.They lack a middle ear cavity, an auditory tube and a tvmpanic membrane. A bone of the jaw articulates with the stapes. The jaws and stapes receive substrate vibrations. Snakes can also detect airborne vibrations. In other reptiles, a tympanic membrane is present on the surface. Or it may be in a small depression in the head. The inner ear of reptiles is similar to amphibians.
3. Olfactory senses
Olfactory senses are better developed in reptiles than amphibians. They have partial secondary palate. It provides more surfaces for olfactory epithelium. Many reptiles possess blind- ending pouches. This pouch opens into the mouth cavity through the secondary palate. These pouches are called Jacobson’s (vomeronasal) organs. These organs are present in diapsid reptiles. However, they are best developed in the squamates. Jacobson’s organs develop in embnonie crocodilians. But it degenerate in adults. Anapsids (turtles) lack these olfactory organs. The protrusible, forked tongues of snakes and lizards are accessory olfactory organs. It detects chemicals present in air. A snake’s tongue come out and then moves to the Jacobson’s organ. Jacobson detect odor molecules. Tuataras use Jacobson’s organs to taste objects present in its mouth.
4. Pit organs
Rattlesnakes and other pit vipers have pit organs. Pit organs are present on each side of the face between the eye and nostril. It is a heat-sensitive organ. Pit organs form depressions. These depressions are lined with sensory epithellium. These are used to protect objects with temperatures different from the snake’s surroundings. Pit vipers are nocturnal. Their pit organs help them to locate small, warm-blooded prey.
EXCRETION AND OSMOREGULATION
Excretory organs: The kidneys of embryonic reptiles are similar fishes and amphibians. Terrestrial animals have larger body size. They have higher metabolic rates. However, kidneys are capable of processing wastes with little water loss. Their kidneys have in many nephrons . The functional unit reptiles are called metanephric kidneys. Their function depends on a circulatory system. It delivers more blood to kidney at greater pressures. Thus kidney filters large quantities of blood.
Mechanism of excretion: Most reptiles excrete uric acid. It is nontoxic and insoluble in w tier. It precipitates in the excretory system. The urinary bladder or the cloacal absorb water. The uric acid is stored in them in a paste like form. Nontoxic uric acid be stored in egg membranes. Thus it has made possible the development of embryos in terrestrial environments.
There are many adaptations in reptiles to reduce water loss by evaporation. These are:
1. Their excretory system reabsorbs water.
2. They have internal respiratory surfaces.
3. They have impermeable exposed surfaces.
4. The behaviors that help regulate temperature also help conserve water.
5. Most reptiles are nocturnal. They do not come out hot day time. The burrowing at du% time reduces water loss.
6. When water is available, many reptiles store large quantities of water in lymphatic spaces. Lymphatic spaces are present under the skin or in the urinary bladder.
7. Many lizards possess salt glands below the eyes. These glands remove excess salt from the body.
REPRODUCTION AND DEVELOPMENT
Vertebrates have internal fertilization and the amniotic egg. It has adapted them completely on land. The amniotic egg is not completely independent of water. Pores are present in the eggshell. They allow the gas exchange. But it allows water to evaporate. Amniotic eggs require a large amount of energy expenditures. This energy is provided by parents in the form of stored food. Parental care occurs in present in some reptiles. They maintain high humidity around the eggs.
Reptiles have internal fertilization. Fertilization occurs in the reproductive tract of the female. Then protective egg membranes are formed around the eggs. All male reptiles possess an intermittent organ. It transfers sperm into the female reproductive tract. Intermittent organs are absent in tuataras. Lizards and snakes possess paired hemipenes at the base of the tail. Hemipenes are erected by turning inside out, like a linger of a glove.
Gonads lie in the abdominal cavity. A pair of ducts transfers sperms into the cloaca in males. The female may store sperms in seminal receptacle after copulation. Secretions of the seminal receptacle nourish the sperm. Sperm may be stored for up to four years in some turtles, and up to six years in some snakes. Sperm can be stored for winter in temperate latitudes. The individuals grouped in hibemacula in the fall and copulation take place. Female stores sperms. Fertilization and development occur in thu spring. Fertilization occurs in the upper regions of the oviduct. Oviduct opens into cloaca. Glandular regions of the oviduct secrete albumen and the eggshell. The shell is tough and flexible. The egg shell is calcareous and rigid in some crocodilians.
Parthenogenesis occurs in six families of lizards and one species of snakes. In these species, no males are present. Populations of parthenogenetic females have higher reproductive rate than bisexual populations. A large population of reptiles died in the cold winter. The surviving reptiles can repopulate rapidly in winter.
Reptiles have complex reproductive behaviour. Males actively seek females. Courtship behaviour helps in sexual recognition. It is involved in physiological preparation for it production.
(a) Some males display head bobbing. These males have bright patches of color on the throat and enlarged folds of skin.
(b) Courtship in snakes is based on tactile stimulation. The male displays tail-waving activity. It brings it chin along the female. Then it entwines his body around her. Then male produces wavelike contractions that pass from posterior to verior side of the body.
(c) Recent research indicates that lizards and snakes also use sex pheromones.
(d) Voclizations are important only in crocodilians. During the breeding season, males bark or cough. It is a territorial warning to other males. Roaring vocalizations also tract females and mating occurs in the water.
Most reptiles freely lay eggs. They do not care about them. Turtles bury their eggs on the ground or in plant debris. Other reptiles lay their eggs under rocks, in debris, or in burrows. About one hundred species of reptiles show parental care of eggs.
One example is the American alligator, Alligator mississippiensis. The female builds a nest or mud and vegetation. It is about 1 m high and 2 m in diameter. She hollows out the cell of the mound. She partially fills it with mud and debris. She deposits her eggs in the cavity and then covers the eggs. Temperature within the nest influences the sex of the hatchlings. Temperature at or below 31.50 C produce females offspring. Temperatures between 32.5 and 33° C produce male offspring. Temperatures around 32°C result in both male and female offspring. Similar temperature effects on sex determination are found in some lizards and many turtles. The female remains near the nest throughout the development and protect the eggs from predation. She frees young from the egg shell. Then she picks them up in her mouth, and transfers them into water. She forms shallow pools for the young and remain with them for up to two years. The female feeds on small vertebrates and invertebrates and drops the food for young. The young scraps this food.
Assemblies and Annotations of Five Mycena Species.
We sequenced the genomes of the bioluminescent fungi M. chlorophos, M. kentingensis, M. sanguinolenta, and M. venus, as well as the nonbioluminescent M. indigotica (Fig. 1A). These species were chosen for their phylogenetic positions (SI Appendix, Fig. S1) and because they displayed different bioluminescence intensities. An initial assembly of each species was produced from Oxford Nanopore reads of each species (SI Appendix, Table S1) using the Canu (13) assembler. Only M. indigotica was successfully isolated from a basidiospore, and the four species that were isolated from heterokaryotic mycelium yielded assemblies 1.3 to 1.8 times larger than haploid genome sizes estimated from Illumina reads using GenomeScope (14) (SI Appendix, Table S2). Mitochondrial genomes in these species were separately assembled into single circular contigs of 88.3 to 133 kb long (SI Appendix, Fig. S2), and haploid nuclear genomes were constructed. The assemblies were further polished using Illumina reads and had consensus quality values (QVs) of 31.1 to 36.8 (SI Appendix, Table S2), which is similar to the QVs of recently published nanopore assemblies in human (also polished with Illumina reads 23.7 to 43.5) (15). These haploid nuclear genomes were 50.9 to 167.2 Mb long, and two of them were among the largest in Agaricales reported to date. The assemblies consisted of 30 to 155 contigs with N50 2.0 to 5.5 Mb (SI Appendix, Table S2), which were comparable to representative fungal reference assemblies (SI Appendix, Fig. S3) and allowed for synteny comparisons (12). Stretches of TTAGGG hexamers were identified at the end of scaffolds, indicating telomeric repeats commonly found in Agaricales (16, 17). The largest scaffolds in M. indigotica and M. kentingensis were telomere to telomere, indicating gapless chromosomes.
Using a combination of reference fungal protein homology support and mycelium transcriptome sequencing (Dataset S1), 13,940 to 26,334 protein-encoding genes were predicted in the Mycena genomes using MAKER2 (18) pipeline, and were 92.1 to 95.3% complete (SI Appendix, Table S3) based on BUSCO (19) analysis. Orthology inference using Orthofinder (20, 21) placed these gene models and those of 37 other Basidiomycota genomes (SI Appendix, Table S4) into 22,244 orthologous groups (OGs SI Appendix, Table S5). Of these OGs, 44.3% contained at least one ortholog from another basidiomycete, while 15 to 29% of the proteomes in each Mycena species were species specific (Dataset S2). The genome sizes were positively correlated with proteome sizes, with the largest (M. sanguinolenta) and smallest (M. chlorophos) varying two- and threefold, respectively. Interestingly, the mitochondrial genomes were larger in species with smaller genomes, and this was because nine out of 16 genes had gained many introns (SI Appendix, Table S6 and Fig. S2).
Interplay between Transposable Elements and DNA Methylation in Mycena.
Similar to other fungal genomes (22, 23), much of the variation in the Mycena nuclear genome sizes can be explained by repetitive DNA content (SI Appendix, Table S7). Only 11.7% of the smallest genome (M. chlorophos) was repeats, which is in stark contrast to the 39.0% and 35.7% in M. sanguinolenta and M. venus, respectively. The majority of transposable elements (TEs) in Mycena were long terminal repeat (LTR) retrotransposons (60 to 85%), followed by DNA transposable elements (11 to 24%) (Fig. 1E and SI Appendix, Table S7). Interestingly, the larger genomes of M. sanguinolenta and M. venus contained the lowest proportion of LTRs (24.9 and 31.1%, respectively), but the highest proportion of unclassified repeats (55.4 and 50.3%, respectively) (SI Appendix, Table S7). A total of 16.6 to 36.5% of the unclassified repeat families shared 53.8 to 60.5% nucleotide identity with known transposable elements, suggesting they were degenerated copies which we defined as relic TEs (SI Appendix, Table S8). Fig. 2A shows that the largest assembled chromosome of M. indigotica exhibits high protein-coding gene content and low transposable element density at scaffold centers, which is typical of fungal chromosomes (24, 25). Such observations were consistent across large Mycena scaffolds (typically >1 Mb), suggesting that our assemblies were robust enough to capture evolutionary dynamics across chromosomes.
Distribution of Mycena genome features. (A) M. indigotica chromosome one. For every nonoverlapping 10-kb window, the distributions from Top to Bottom are: 1) Gene density (content in percentage). Blue stripes denote positions of single-copy ortholog with M. chlorophos. 2) Density of TEs, including LTRs, LINES, and DNA. 3) Average methylation level called from CpG sites per window. The high methylation window generally clustered in high TE regions with low gene density. (B) Methylation level in genes and different types of repeats. (C) Relationships among genome size, number of repeats, and CG methylation levels in Mycena.
We detected 5-methylcytosine (5mC) DNA methylation levels across the five Mycena assemblies with nanopore long reads using deepsignal (26) which was initially trained with M. kentingensis bisulphite sequences (Methods). CG sites were found either highly (mCG level >60%) or weakly (<15%) methylated in gene body, displaying a bimodal distribution (SI Appendix, Fig. S4). Such a bimodal distribution has also been observed in plants, animals, and other fungi, including Tuber melanosporum and Pseudogymnoascus destructans (27 ⇓ ⇓ ⇓ ⇓ –32). Within Mycena, the CG methylation in genes (5.4 to 10.5%) was much lower than that in repeats—i.e., TEs and unclassified repeats (11.6 to 84.5%) (Fig. 2B and SI Appendix, Table S9). The level of CG methylation in these genomes is comparable with those of a previous survey on DNA methylation in 528 fungal species (32), which revealed that 5mC levels were highest in Basidiomycota, further indicating that DNA methylation has a specific effect on repeats in Mycena genomes. DNA transposons or LTR were enriched in 5mC levels and were higher than flanking regions (SI Appendix, Fig. S5). Except for DNA transposons in M. kentingensis, LTR retrotransposons had the highest CG methylation levels of all types of transposable elements (Fig. 2B). Furthermore, CG methylation in relic TEs was clearly lower than that in classic TEs (SI Appendix, Table S9). Among the Mycena species, we found that M. sanguinolenta and M. venus with larger genomes and higher repeat content had lower levels of methylation in the repeats, and the repeat methylation was much higher in M. indigotica, M. chlorophos, and M. kentingensis, which have smaller genomes (Fig. 2C). The same pattern was also observed in genes, though they had fewer changes in their methylation level than did repeats. Our results indicate that the variant composition of repeats is differentially mediated by DNA methylation among closely related Mycena species. Hence, genome expansion in Mycena was likely a result associated with transposable element proliferation and the accumulation of relic TEs, which yielded reduced methylation in active copies this is also observed in some plants, e.g., Arabis alpina (33) and Manihot esculenta (34).
A Single Origin of Bioluminescent Fungi in the Ancestor of Mycena and the Marasmioid Clade.
Phylogenomic analyses based on single-copy ortholog sets have placed Mycena sister to the marasmioid clade, including Armillaria and Omphalotus, which are the other two lineages in which bioluminescent species have been identified. This species phylogeny was recovered in both maximum likelihood analysis (35) of a concatenated supermatrix of single-copy gene alignments (Fig. 1B) and coalescent-based analysis using 360 gene trees (36) (SI Appendix, Fig. S6). In our four bioluminescent Mycena species, we identified genes involved in luciferin biosynthesis and their orthologs across species (Fig. 1C). Fig. 1D shows phylogenetic reconciliation, which suggests that the orthogroup containing luciferases was present in the last common ancestor of the mycenoid + marasmioid clade and Schizophyllaceae, predating their incorporation into the luciferase cluster. This is in contrast to a previous report (7) suggesting that luciferase originated in the last common ancestor of the Agaricales. Phylogenies of other members of the luciferase cluster were also congruent with the species tree (SI Appendix, Fig. S7 A–D). Using MCMCtree (37) with three fossil calibrations, we estimated the age of mycenoid most recent common ancestor to be 105 to 147 million years ago (Mya) in the Cretaceous (Fig. 1B). This is consistent with recent estimates [78 to 110 (8) and mean 125 (1) Mya] and overlaps with the initial rise and diversification of angiosperms (38), suggesting that Mycena are ecologically associated with plants acting as saprotrophs or mycorrhizal partners (3). Finally, the age of mycenoid and marasmioid which was also the age of the luciferase cluster in fungi was estimated to originate around 160 million years ago during the late Jurassic (Fig. 1B).
Differential Conservation of Synteny Regions across Mycena Genomes.
We attempted to characterize chromosome evolution in the mycenoid clade using the newly available, highly contiguous assemblies for Mycena. We first compared the patterns of 4,452 single-copy ortholog pairs between assemblies of M. indigotica and Armillaria ectypa (SI Appendix, Fig. S8). The majority of scaffolds between the two species could be assigned one-to-one relationships unambiguously, providing strong evidence that macrosynteny has been conserved between the marasmioid and mycenoid clades. Such chromosome-level synteny remained conserved until the last common ancestor of the Agaricales, when M. indigotica was compared against the genome of Pleurotus ostreatus (SI Appendix, Fig. S9). Based on the clustering of single-copy orthologs, we identified 10 linkage groups resembling the number of known karyotypes in Basidiomycota, suggesting possible ancestral chromosome numbers (25).
The M. indigotica scaffolds exhibit high orthologous gene density in the centers of scaffolds (Fig. 2A). Fungal chromosomes can typically be compartmentalized into chromosomal cores and subtelomeres which display differential evolutionary dynamics (24, 39). In some extreme cases, filamentous pathogenic fungi contain entire lineage-specific chromosomes that are gene sparse and enriched in transposable elements (40). In the case of Mycena, a multigenome comparison showed that synteny conservation was typically either lost at the scaffold ends or extended by several megabases across the assemblies (Fig. 3).
Genome synteny in Mycena genomes. Schematic representation of the interscaffold relationship between species. The lines between scaffolds denote single-copy orthologs between a pair of species. Shaded areas in each scaffold denote high-synteny regions defined by DAGchainer (41) and colors denote linkage groups assigned by most abundant pairwise single-copy orthologs. Lines are color coded according to corresponding linkage groups. Black triangles denote locations of luciferase clusters.
Defining precise boundaries between regions with and without synteny is challenging. Based on the clustering of orthologous genes using DAGchainer (41), we partitioned the scaffolds into low and high synteny regions. As expected, highly syntenic regions in Mycena were typically found at the scaffold centers. In contrast, synteny was not identified in part of scaffolds or, in some cases, throughout the entire scaffolds, as was the case for the largest (12.0 Mb) assembled scaffold of M. venus (Fig. 3). These regions are highly enriched in repeats they have 1.5 to 2.6-fold higher methylation levels and are overrepresented in expanded and contracted OGs compared to high synteny regions (SI Appendix, Fig. S10 and Table S10 two-proportion z test, P < 2.1E-9). Expansions and contractions of gene families were 1.8- to 4.2- and 1.4- to 2.9-fold higher in the low than high synteny regions, respectively differential gain and loss of genes in these regions may have important implications for Mycena.
Evolutionary Dynamics of Luciferase Clusters.
One of the outstanding questions surrounding the evolution of fungal bioluminescence is why bioluminescent species are scattered across the mycenoid and marasmioid clades. The mechanism of fungal bioluminescence is homologous across species (6), and this implies that nonbioluminescent mycenoid and marasmioid species must have lost the functional luciferase gene cluster. To investigate the evolutionary dynamics of the luciferase cluster, we examined all highly contiguous assemblies across the bioluminescent lineages available and inspected adjacent synteny (Fig. 4). The majority of the Mycena luciferase clusters included luciferase (luz), hispidin-3-hydroxylase (h3h), cytochrome P450 (cyp450), and hispidin synthase (hisps). We found that physical linkage was only maintained within the luciferase cluster, and synteny was lacking in genes surrounding the luciferase cluster (Fig. 4) of species in the mycenoid and Omphalotus lineages. Coupled with the aforementioned synteny analysis, we hypothesized that the luciferase cluster residing in a fast-evolving genomic region may result in it frequently being lost. The nearest TE sequence adjacent to luciferase cluster in Mycena species were 2 to 8.9 kb away and separated by 0 to 5 genes, suggesting possible roles of transposons mediating rearrangements (Fig. 4). Additionally, the luciferase cluster of different Mycena species was identified in low synteny regions of different linkage groups (Fig. 3), providing evidence that the location of the cluster had been extensively rearranged. In contrast, the genes surrounding the luciferase cluster among the eight Armillaria species were generally in the same order, with collinearity partially lost only in Guyanagaster necrorhiza (a very close relative of Armillaria, Fig. 4). We found that the synteny surrounding the Armillaria luciferase cluster was maintained since the common ancestor of Agaricales (SI Appendix, Fig. S11). The up- and downstream regions of the luciferase cluster belonged to two separate regions of the same ancestral chromosome linkage group, suggesting that these regions were previously rearranged—including the luciferase cluster—and were subsequently retained (SI Appendix, Fig. S11).
Synteny around the luciferase cluster among bioluminescent fungi. The OGs shared by at least two species are labeled with the same color, regardless of their orientation. Arrows and rectangles denote protein-encoding genes and transposable element, respectively. Different colors of rectangles denote TE types (pink: LINE and LINE relic light green: LTR and LTR relic yellow: DNA and DNA relic). The cph gene in some species was located in other scaffolds (SI Appendix, Fig. S12).
These observations led us to propose a most plausible evolutionary scenario in which the luciferase cluster evolved across all available bioluminescent fungi (Fig. 5). We inferred that the ancestral luciferase cluster consisted of luz, h3h, cyp450, and hisps, with caffeylpyruvate hydrolase cph—involved in oxyluciferin recycling (6, 7)—also present on the same chromosome. This combination was found in 14 of the 15 bioluminescent species used in this study. Our data outline two contrasting scenarios by which the luciferase cluster was retained. First, the luciferase clusters in family Physalacriaceae are located in slow-evolving chromosomal regions, resulting in all members of the Armillaria synteny retaining both many of the genes adjacent to the luciferase cluster and the uniform luciferase cluster in their genomes. By residing in slow-evolving regions, the luciferase cluster in Armillaria might not be prone to losses by frequent chromosomal events (rearrangements, TE activity, etc.), explaining why it is conserved in the genus. On the other hand, the luciferase cluster in the mycenoid lineage is located in a highly dynamic genomic partition with low synteny (Fig. 3), which could explain why Mycena fungi had a higher tendency to lose the luciferase cluster compared to Armillaria species.
Evolutionary scenario for luciferase cluster evolution. The formation of the luciferase cluster originated at the dispensable region of the last common ancestor and was susceptible to translocate to different genomic locations through rearrangement. In the ancestor of marasmioid, cph was duplicated and translocated into the luciferase cluster. Before the ancestor of the Physalacriaceae family emerged, the luciferase cluster was translocated into the core region and have since kept its synteny in the Armillaria lineage. In the most recent common ancestor of Mycena species, the luciferase cluster was located in the dispensable region and have since been susceptible to further rearrangement. Arrow box indicates gene. The dashed arrow box denotes the loss of gene. Fishhook arrow denotes translocation event. a Percentage of bioluminescent fungi found in the mycenoid lineage (5). b Percentage of bioluminescent fungi found in Armillaria lineage (47).
Variations were common in the luciferase cluster. cph was located in different scaffolds in four of the five Mycena species (SI Appendix, Fig. S12). In M. sanguinolenta, luz and cyp450 were duplicated adjacent to the luciferase cluster (Fig. 4). Losses were observed at different positions in the phylogeny. The nonbioluminescent M. indigotica lost the entire luciferase cluster, but h3h homologs were found in other regions of the genome, while G. necrorhiza has a partial luciferase (7) and three other enzymes (Fig. 4), suggesting that an independent loss of luciferase function alone was enough for it to lose its bioluminescence. Interestingly, we found that the cph gene was independently translocated adjacent to the luciferase cluster in both M. kentingensis and the ancestor of the marasmioid clade (SI Appendix, Fig. S13) it was presumably favored and maintained here by natural selection (42). A selection analysis of genes in the luciferase cluster revealed that 23.1 to 45.2% of conserved sites exhibit purifying selection, with only 7 to 28 sites under episodic selection (SI Appendix, Fig. S14).
Expression Profile of Luciferase Cluster and Identification of Conserved Genes Involved in Fungal Bioluminescence.
Fungal bioluminescence is believed to have ecological roles, such as attracting insects, and is regulated by circadian rhythms (43) however, the complete repertoire of genes involved in bioluminescence is still unknown. We carried out transcriptome profiling between mycelia with different bioluminescent intensities in four Mycena species, and identified genes that were either differentially expressed or positively correlated with bioluminescent intensities (Methods). There were 29 OGs found to contain up-regulated gene members in all four Mycena species (Fig. 6A), including luz, h3h, and hisps, consistent with bioluminescence intensity dependent on the expression of these three genes in the luciferase cluster. In particular, luz expression was significantly different between two tissues with relative high and low bioluminescence in M. kentingensis (log fold change [logFC] 3.0 adjusted P < 0.001) and M. chlorophos (logFC 4.7 adjusted P < 0.001) there was also a significant correlation between bioluminescent intensity and expression level in M. sanguinolenta (Pearson’s correlation coefficient [PCC] 0.82 P < 0.005) and M. venus (PCC 0.86, P < 0.005 Dataset S3). In M. chlorophos, however, its cyp450 and h3h were not differentially expressed, and four distant homologs of h3h were found to be up-regulated (SI Appendix, Fig. S7A). Although a second copy of luz and cyp450 were found in M. sanguinolenta, they showed much lower expression (2 and 3 transcripts per million [TPM], respectively) than those in the cluster (282 and 138 TPM, respectively). The remaining OGs up-regulated in mycelia showing higher bioluminescence included ABC transporters and acetyl-CoA synthetases which also showed a predicted function in metabolic adaptations to bioluminescence in firefly and glowworm (44, 45) (Fig. 6A and SI Appendix, Table S11). In particular, four OGs were annotated as FAD or NAD(P)-binding domain-containing proteins. As these genes do not bear sequence similarity to h3h which is also a NAD(P)H-dependent enzyme, they are likely involved in other biochemical processes that are required during bioluminescence.
Expression analysis to identify genes involved in bioluminescence. (A) Conserved up-regulated OGs. DEGs between mycelia with different bioluminescent intensities were identified in four bioluminescent Mycena species, and all 29 OGs—except OG0009249 and OG0000706—contain at least one up-regulated gene. A detailed annotation of the genes in the OGs is listed in SI Appendix, Table S11. (B) Tissues used for transcriptomic data analysis in M. kentingensis. The Left and Right sides are the tissues under light and dark conditions, respectively (captured by a Nikon D7000). The camera setting for each tissue: mycelium, Sigma 17- to 50-mm ISO100 f2.8 with 16-min exposure time primordia, AF-S Micro Nikkor 60-mm ISO800 f/11 with 122.4-s exposure time YFB, AF-S Micro Nikkor 60-mm ISO800 f/11 with 60.6-s exposure time FB, AF-S Micro Nikkor 60-mm ISO800, f/11 with 9.3-s exposure time. YFB, young fruiting body (0.5 to 1 cm). FB, mature fruiting body (>1 cm). FB-cap, cap from FB. FB-stipe, stipe from FB. (C) Expression profile of luciferase cluster across developmental stages of M. kentingensis. Bold lines indicate four genes in the luciferase cluster. These four genes and the other 53 genes (yellow) were assigned into the same module (Module50) with similar expression patterns. The genes located up- or downstream (gray) of the luciferin biosynthesis cluster had lower expression levels than the four genes in the cluster.
Differences in bioluminescent intensity have been recorded in tissues of fungi both in nature (4, 5, 46 ⇓ –48) and—for M. kentingensis—in a laboratory environment, in which the life cycle can be completed (Fig. 6B). To investigate putative roles of bioluminescence across developmental stages, additional transcriptome profiling was carried out in the primordia, young fruiting body, and cap (pileus) and stipe of the mature fruiting body of M. kentingensis. Bioluminescence was stronger in the cap than in the stipe, so we expected the luciferase cluster genes to have higher expression in the cap tissue. However, luz and h3h showed opposite expression patterns (Fig. 6C and Dataset S4), suggesting that there may be other regulators involved in bioluminescence in M. kentingensis.
The regulation of bioluminescence in M. kentingensis during development was determined by performing a weighted correlation network analysis (WGCNA) (49, 50), which identified 67 modules of coexpressed genes in these stages (SI Appendix, Fig. S15). All members of the luciferase cluster luz, h3h, cyp450, and hisps belonged to the same module (Module50 Fig. 6C) of 57 genes, suggesting that the expression of the luciferase cluster members are coregulated during developmental stages. Only two genes belonging to OG0001818 (acid protease) and OG0000000 (short-chain dehydrogenase) which were part of the 29 aforementioned OGs associated with bioluminescence in the mycelium samples across Mycena. Six genes in this module were annotated as carbohydrate-active enzymes (Dataset S5): one GH75 (chitosanase), one AA1_2 (laccase ferroxidases), two GH16, and two genes with two CBM52 domains. GH16 (glucanases) and AA1 (laccases) are known to be differentially expressed during fruiting body development (51), implying a possible link between cell wall remodelling during development and bioluminescence. In addition, we reanalyzed the transcriptomes of Armillaria ostoyae across different developmental stages from Sipos et al. (9). Consistent with the observation that bioluminescence was only observed in mycelia and rhizomorphs in A. ostoyae (52, 53), the expressions of luz, h3h, cyp450, and cph were highest in these tissues (SI Appendix, Fig. S16). Together, these results imply that the luciferase cluster was differentially regulated during development and that the extent of the expressions was also different among bioluminescent species of different lineages.
Gene Families Associated with the Evolution of Mycenoid Species.
We assessed orthologous group evolution by analyzing OG distribution dynamics along a time-calibrated phylogeny using CAFE (54). The rate gene family changes in mycenoid were comparable to those of other branches of Agaricales (likelihood ratio test P = 0.25). A total of 703 orthologous groups were expanded at the origin of the mycenoid lineage (SI Appendix, Fig. S17). Analysis of gene ontology terms showed that these genes were enriched in NADH dehydrogenase activity, monooxygenase activity, iron ion binding, and transferase activity (Dataset S6). Additionally, we sought to identify proteins specific to mycenoid species by annotating protein family (Pfam) domains and comparing them with those of species outside this lineage (Dataset S7). A total of 537 Pfam domains were enriched in the mycenoid lineage (onefold by Wilcoxon rank sum test with P < 0.01 Dataset S8) of which 3 to 17 were species specific. Acyl_transf_3 (acyltransferase family PF01757), contained in a range of acyltransferase enzymes, was the only domain found in all six mycenoid species. The closest homologs were found in ascomycetous Cadophora, Pseudogymnoascus, or Phialocephala (31 to 35% identity with 73 to 100% coverage). Four of the enriched domains are known pathogenesis-related domains expanded in pathogenic Agaricales Moniliophthora (55) and Armillaria species (9): COesterase (PF00135 carboxylesterase family), thaumatin (PF00314), NPP1 (PF05630 necrosis-inducing protein), and RTA1 (PF04479 RTA1-like protein) (SI Appendix, Fig. S18). Moreover, M. sanguinolenta and M. venus contained over 100 and 17 copies of COesterase and thaumatin (median 37 and 4 copies in other fungal species of this study), respectively.
We have isolated nine novel copepod luciferases using the homology-based PCR cloning strategy. A BLAST search using the amino acid sequences of copepod luciferases as the query revealed no highly similar proteins in the database, except for other calanoid luciferases (GLuc, MLuc, and MpLuc). This may be due to the limited number of deposited sequences of copepod proteins. So far, all of copepod luciferase genes, including GLuc and MLuc reported elsewhere, have been isolated from species in the Augaptiloidea superfamily in Calanoida. We have tried to isolate luciferase or luciferase-like genes from other superfamilies of Calanoida, such as Pseudocyclopoidea or Centropagoidea using degenerate PCR primers. The result was no amplification or no luciferase-like sequences in the amplified DNA product (data not shown). However, we assume that luciferases or luciferase-like genes may exist, not only in Augaptiloidea but also in other superfamilies, because the luminous assay of zooplankton lysate from these superfamilies all had a measurable, though very weak, level of activity compared with that of negative control samples ( fig. 2). Further screening of the calanoid luciferase or luciferase-like genes by different cloning strategies may reveal the structure and evolution of a direct ancestral copepod luciferase gene.
Consensus amino acid residues and domain structure were revealed by an alignment of 13 copepod luciferases obtained in this study ( fig. 4A). Highly conserved amino acid residues, C-x(3)-C-L-x(2)-L-x(4)-C-x(8)-P-x-R-C, which are present in both domains, would be one of the criteria for the copepod luciferase, although the reason for this cysteine-rich area in the conserved sequence remains obscure. Because the similarity in the structure of the two domains was found in all of the copepod luciferases isolated in this study ( fig. 4B), we assume this similarity in the structure of the two domains is very characteristic of the luciferases isolated from Augaptiloidea species.
Cladistic Analysis of rRNAs and Luciferases
The current ML analyses using 18S rRNA sequences essentially support previous morphology- ( Bradford-Grieve et al. 2010) and sequence-based phylogeny ( Blanco-Bercial et al. 2011). The Augaptiloidea family contained numbers of bioluminescence-positive species ( fig. 3, red shadow) and was recovered as monophyletic with a moderate bootstrap value (84%) and closely related with the Pseudocyclopoidea ( fig. 3). In NJ analysis of 18S, the notable difference is in the family Centropagoidea, which forms a monophyletic assemblage and is a sister to other calanoid superfamilies ( supplementary fig. S1 , Supplementary Material online). The topology is supported with a high bootstrap value (100%) and is consistent with the results from several sequence-based analyses of Calanoida ( Braga et al. 1999 Figueroa 2011). Inconsistent results between our ML and NJ trees might indicate that the use of a single gene (18S) in the phylogenetic analysis is likely to produce unstable results. Nevertheless, ML analysis of 18S genes produced a tree with more similar topology to a multigene molecular phylogeny of the Calanoida ( Blanco-Bercial et al. 2011), in comparison with NJ analysis. We also sequenced the D1–D2 regions of 28S rRNA and analyzed phylogenetic relationships among calanoid species by ML and NJ analyses. The results were similar to the 18S analysis, but many clades were very poorly supported, which is probably due to relatively high interspecific divergence of D1–D2 sequences within each superfamily (data not shown).
The ML phylogenetic analysis based upon 18S also clearly showed the intrafamilial relationships of the Augaptiloidea. One of the Augaptiloidean families, Metridinidae, in which many species are capable of strong bioluminescence, consists of three genera Metridia, Pleuromamma, and Gaussia. The genus Metridia contains sibling species in the North Atlantic (M. lucens) and North Pacific (M. pacifica). In the same way, their large body relatives (e.g., M. longa in the North Atlantic and M. okhotensis in the North Pacific) also have similar ecological characteristics in each ocean ( Mauchline 1998). In the monophyletic clade of the Metridinidae family, morphologically similar species of M. pacifica and M. lucens are paired with a high bootstrap value (99% in ML and 100% in NJ trees), which is consistent with a previous report ( Bucklin et al. 1995). Furthermore, phylogenetic relationships among additional luminous species of the genus Metridia (M. okhotensis, M. curticauda, and M. asymmetrica) also was revealed in our analyses. Metridia okhotensis, which is a mesopelagic inhabitant and dominant in the same region of the subarctic Pacific as M. pacifica ( Yamaguchi et al. 2004), is a sister to the clade containing M. pacifica and M. lucens ( fig. 3), which indicates the close relationships between M. okhotensis and these two species. Metridia curticauda and M. asymmetrica are potentially luminous ( fig. 2 and Takenaka Y, unpublished data) and are strongly associated with a high bootstrap value (100%). On the other hand, M. longa is unexpectedly set apart from its North Atlantic counterpart, M. okhotensis. Gaussia princeps is also a calanoid of the family Metridinidae, and it has distinct characteristics if compared with other genera in Metridinidae, such as the large body size, tropic and temperate distribution, and detailed morphology ( Soh et al. 1998). Both ML and NJ analyses showed that Gaussia and Pleuromamma form a monophyletic clade that is sister to Metridia ( fig. 3 and supplementary fig. S1 , Supplementary Material online). Although bootstrap support for the Gaussia–Pleuromamma clade is weak (64% in ML, not shown in fig. 3), our results are similar to the morphology-based phylogeny of Gaussia ( Soh 1998). Further investigation with additional sequences from other Gaussia species will clarify relationships among genera in the family Metridinidae.
The phylogeny of 13 calanoid luciferases suggests a different evolution of the Metridinidae and Heterorhabdidae families' luciferases ( fig. 5A). In the clade containing Metridinidae luciferases (clade 1), two proteins in a single species are likely to have evolved independently. The similarity of primary structures among MpLuc1, MoLuc1, and PaLuc1 (type-I) luciferases were greater than those of their counterparts (MpLuc2, MoLuc2, and PaLuc2) (type-II) luciferases ( fig. 4A). The mRNA coding for MoLuc1 or MoLuc2 would be transcribed from two different loci or alleles since studies of genomic sequences revealed the presence of different lengths and positions of the introns in MoLuc genes ( fig. 5B), as seen in MpLuc genes ( Takenaka et al. 2008). Gene duplication events of luciferase probably happened in the ancestral species of the Metridia and Pleuromamma families, thereafter, paralogous luciferases might have diverged independently. Conversely, it would be expected that specialization of Heterorhabdidae species preceded the duplication and diversification of luciferase genes since pairs of luciferases (HtLuc1 and HtLuc2 HmLuc1 and HmLuc2) are monophyletic (clades 6 and 7) within species. Nucleotide identity between coding sequences of HmLuc1 and HmLuc2 is 91.8%, whereas it is 62.6% between HmLuc1 and HtLuc1, which were isolated from species of the same Heterorhabdidae family. Extensive genome survey of two lineages of Metridinidae and Heterorhabdidae families may shed light on the multigene structure of luciferase genes and how copepod luciferases have evolved. From the present study, we could not interpret any evolutionary novelty derived from gene duplication of luciferases in calanoid copepods. Because phenotypic observation on live copepod bioluminescence is difficult without special video equipment and relevant technical skills, we are trying to evaluate any possible evolutionary novelty of the gene duplication by revealing different biochemical characteristics between type-I and type-II luciferases identified in this study.
Forming a monophyletic clade containing both MLuc (M. longa) and MoLuc1 (M. okhotensis) ( fig. 5A) is consistent with the fact that both species are closely related. However, M. longa is basal to other Metridia species in the 18S rRNA tree, and M. okhotensis is nested within that tree ( fig. 3). The discordance is probably due to the different number of analyzed species and different evolutionary mechanisms between luciferase and the 18S rRNA gene. The inclusion of additional luciferases from Metridia species, such as M. curticauda and M. asymmetrica, might change the topology of the clades 1–4 in figure 5A. The relationships among luciferases from Metridia and Pleuromamma are basically the same between type-I and type-II groups. GLuc, Gaussia luciferase, is weakly associated with Metridinidae type-II luciferases (clade 3). A low bootstrap support value for clade 3 (<50%) indicates the branching position of GLuc could not be determined with high confidence. In fact, GLuc clustered with Metridinidae type-I luciferases as the sister to a monophyletic clade containing all type-I luciferases and MLuc in NJ analysis ( supplementary fig. S2 , Supplementary Material online). The result was inconsistent depending on the method of the phylogeny analysis, substitution model, and parameters used in the analysis. This is probably explained by the neutral characteristic of the GLuc sequence, which possesses an equal ratio of amino acid residues specifically found on type-I or type-II luciferases at different sites (data not shown).
Factors Affecting the Intensity of Copepod Bioluminescence
Zooplankton lysates ( fig. 2) and luciferases ( fig. 6B) from Metridia spp. and Pleuromamma spp. (both in the Metridinidae family) (MpLuc, MoLuc, and PaLuc) showed significantly higher specific activity than those from Heterorhabdus spp. and Heterostylites spp. (family Heterorhabdidae) (HtLuc and HmLuc), although both families belong to the same Augaptiloidea superfamily. As the factors that may affect the intensity of bioluminescence, diel vertical migration (DVM), feeding patterns, and selection pressure from predators are considered.
DVM is a copepod behavior to stay in darker deeper layers during daytime and migrate upward to food-rich surface layers at night for feeding. A most important function of copepod DVM is considered to be avoidance from predation by visual-feeding fishes ( Gliwicz 1986 Neill 1992). Species characterized with strong bioluminescence (Metridinidae) are all medium-sized suspension feeders known to perform strong nocturnal ascent DVM ( Haury 1988 Hays 1995). The dominance of Metridinidae in oceans world-wide can be explained by the fast swimming speed and strong DVM intensity ( Mauchline 1998). Because of its numerical dominance, Metridinidae is selectively captured by various mesopelagic lantern fishes ( Merrett and Roe 1974 Hopkins and Sutton 1998). The bioluminescent behavior of copepods is considered to have a function of avoidance from vision-dependent predators ( Herring 1988 Widder 1992). To distract or blind a predator of mesopelagic lantern fish predator, Metridinidae with reinforced luciferases would have a selective advantage for their stronger bioluminescent system (MpLuc, MoLuc, and PaLuc). We suggest that MpLuc from M. pacifica ( fig. 1) shows the highest bioluminescence ( fig. 6B) because the habitat depth of M. pacifica is the epipelagic layer (0–200 m) ( table 1) where a large number of predators exist.
The species that are characterized with weak bioluminescence ( figs. 2 and 6B), such as H. tanneri and H. major (Heterorhabdidae) (HtLuc and HmLuc), inhabit the deeper darker depths and at low density ( table 1) and show a low intensity of DVM due to their slower swimming behavior ( Yamaguchi and Ikeda 2000). They are also known to be carnivores, evolutionarily having switched from suspension feeders to predators with a specialized feeding mechanism that inject venom or anesthetic from the mandibular ventralmost tooth into the prey animal ( Nishida and Ohtsuka 1996 Ohtsuka et al. 1997). This specialized feeding behavior of Heterorhabdus may facilitate easy capturing of their prey and reduce the need for motion during predation. In contrast to the Metridinidae, their low motility might be insusceptible to the motion-dependent predators. Taken together with these characteristics, the Heterorhabdidae may be exposed to low predation pressure by mesopelagic fishes, resulting in less selective evolutionary advantage for any remarkable bioluminescence.
Lucicutia ovaliformis (family Lucicutiidae) (LoLuc) is a small-sized suspension feeders that dominates the mesopelagic layer (200–1,000 m) ( Yamaguchi et al. 2002). All of the Lucicutiidae species are known to be distributed in the meso- to abyssopelagic zones of the ocean ( Brodskii 1967). Although the feeding type and numerical abundance of Lucicutiidae ( table 1) are comparable to those of Metridinidae, the bioluminescent intensity of Lucicutiidae is lower than that of Metridinidae ( fig. 2). One of factors that might explain the intensity difference between two families is their habitat depth. Because the Lucicutiidae occurs much deeper than the shallower habitat Metridinidae does, they could be difficult to perceive and may not attract predators in the meso- to abyssopelagic layer. This is especially the case if the predators are feeding selectively ( Merrett and Roe 1974 Hopkins and Sutton 1998). Therefore, predation pressure on Lucicutiidae has been relatively low, resulting in a lower intensity of bioluminescence than seen in the Metridinidae.
Bioluminescence in Calanoid Superfamilies Except for Augaptiloidea
Copepod luciferases, isolated in this study and previous reports, are all derived from the Augaptiloidea superfamily in Calanoida. There are few to no reports of bioluminescence in other calanoid superfamilies. The reason for the difference in the luminous ability between the Augaptiloidea and other superfamilies could be explained by their ecology (e.g., motility, habitat, and body size). Although precise evolutionary positions of the Pseudocyclopoidea and Epacteriscoidea are not determined yet, these superfamilies are believed to be the most primitive Calanoida ( fig. 7) ( Bradford-Grieve et al. 2010). Comparing with other eight superfamilies illustrated in figure 7, they are highly specialized because of their adaptation to the epibenthic habitats. They are found only at shallow to shelf depth ( Ohtsuka et al. 1999) or in submarine caves ( Ohtsuka et al. 2002), in contrast to the Augaptiloidea, which has a greater diversity of distribution within the pelagic zones ( Yamaguchi et al. 2004). These observations imply little change, if any, of habitat in the evolutionary history of the Pseudocyclopoidea and Epacteriscoidea ( Bradford-Grieve 2004). Living on-bottom– or in-bottom–dwelling habitat would be a very effective means to find nutrients and hide from predators. There is no report, so far, describing the bioluminescence of these primitive copepods, probably because of the very limited research on these minor species in Calanoida so far. However, considering their stable benthic habitat and very small body size (below 1 mm) ( Ohtsuka et al. 1999), evolving bioluminescence as a defense against the predators seems to be unnecessary for them.
Speculative scheme of evolution of calanoid bioluminescence. Phylogeny of the calanoida is based on previous reports ( Park 1986 Bradford-Grieve et al. 2010).
Lights under the sea
This ability can be used for a variety of purposes, said Matthew Davis, an assistant professor of biology at St. Cloud State University.
“Functionally, probably the majority of fishes that have bioluminescence use the light for camouflage,” he said, noting that the glow can actually help hide a fish’s body in the water column when it’s placed in the right way.
But he added that other species use their bioluminescence to attract prey (think of the anglerfish in Finding Nemo), or to communicate with one another and attract mates.
Within these 1,500 species, there are several different classes of fish that have the ability, such as certain types of sharks, which belong to a class of cartilaginous fishes — fish whose skeletons are made of cartilage, rather than bone.
In a new study, published Wednesday in the journal PLOS ONE, Davis — the lead author — and colleagues John Sparks and Leo Smith focused specifically on ray-finned fishes, as they’re the largest class of fish on the planet, comprising at least 25,000 species (and, in fact, one of the largest groups of vertebrates altogether).
One of the more intriguing (at least to me), and beautiful quirks about the evolution of life on this planet is the repeated development of bioluminescence across many different lineages. Bioluminescence is simply the ability of a living organism to produce light. If it’s alive and luminescing, boom, you’ve got an example of a complex chemical cascade that allows sacks of meat not so different from ourselves to light up like a goddamned Christmas tree. Essentially, what is happening with bioluminescence is a highly controlled chemical reaction that releases energy in the form of light emission. This can be done by the beastie itself, or by a symbiotic microorganism that has been acquired by a larger creature. It occurs in multiple kingdoms of life, in terrestrial and marine environments. If I so desired, I could ruminate tearfully on how all of Earth’s life is chemically derived from components forged in a star in a Saganesque exposition of cosmic perspective…and how in some small way, bioluminescence is the means by which stardust can light the darkness of the universe once again. But, heavy-hearted sighs and poetic attribution of consciousness to a mechanically elegant and indifferent universe are for another day, and if done in all seriousness, for another person.
The thing about bioluminescence is that often our understanding of it is limited to a few well-known examples, and without any sort of context, biological or otherwise, other than ‘that is pretty I like it.’ And while yes, indeed, fireflies and deep-sea fish do have a magical and/or alien quality to them, there is a whole world of bioluminescing organisms that go unloved and underappreciated and denied all the badass reasons for and applications of their abilities. Bioluminescence has evolved many times, and therefore, each example tends to have its own unique story.
First, the most conventional and familiar case of bioluminescence for many folks fireflies.
Fireflies aren’t actually flies. They are beetles, specifically of the family Lampyridae. They range all over the world in warmer latitudes, and tend to inhabit wet, soggy, swampy fields and meadows, or damp wooded areas. Their larvae also produce light, and are often referred to as ‘glow worms.’ Fireflies, both as adults and larvae, produce light from the ends of their abdomens in a special organ in which a chemical reaction involving the enzyme luciferase, magnesium, ATP (major molecular carrier of energy in cells), oxygen, and a light-emitting compound known as luciferin occurs. Luciferase can only work on luciferin in the presence of the other listed compounds, and the eventual outcome of the reaction is a relatively bright emission of ‘cold light’. The color of this emitted light ranges between species (and some species don’t even light up at all), and can be between 510 and 670 nanometers, which means green to yellow to almost red. The actual function of this ability differs for larvae and adults. Larvae use their constant glowing to notify predators that their bodies are currently producing chemicals that make them taste bad, toxic, and often both. A hungry bird looking for an evening snack learns quickly that the attractively squooshy beacons in the meadow grass taste less like food and more like sadness. When puberty sets in for these sparkly grubs, the function, of course, becomes sexual. What once was effective for deterring getting eaten, now is co-opted later in life for attracting mates through fanciful courtship displays. It’s a bit like how when you’re four years old, dancing and singing and running around were decent ways to burn off excess energy, but later on, if you do these things effectively, there’s a good chance you’re going to make a lot of money and get laid. So, subtle nuances of natural and sexual selection have driven firefly bioluminescence, and all of it is based on an enigmatic enzymatic reaction contained within the body of a living creature. Consider that the next time you imprison this wonder of nature in an old jam jar.
“I am your master and I demand entertainment. Glow! Glow, damn you!”
While popular imagery of fireflies surrounds lovely meadow nightscapes, dotted with the flickering bright lights of fairy-like insects, all under the silky light of the full moon, there are multiple dimensions to the the firefly. And some of these dimensions are ironically quite ‘dark’, as fireflies, like any other creature, are continually under the relentless force of natural selection, and their angelically-glowing butts serve no refuge from the brutal realities of nature. For example, take a look at the following two fireflies:
They look very much alike, right? And while it would be tempting to say that they are members of the same species, this is not true. However, they are close relatives. The top firefly is of the genus Photinus and the bottom is Photuris. Photinus are among the most commonly seen fireflies in the U.S., and some species use highly synchronized flashing in courtship behavior. Photinus males search for conspecific females in the darkness by making use of their strobe-light asses and flashing signals in a specific pattern. If a female likes what she sees, she responds with her own, typically much more subdued and demure neon laser in what eventually becomes some sort of silent woodland rave. In one species, P. carolinus, this matter-of-fact response of ‘yes, please’ from a female will often result in a mad rush of males to her location (as many as two dozen), in which they aggressively flash, and try to mount and inseminate the female, as well as other eager males that stray too close and look a little too sexy. After the dazzling light show (and, undoubtedly, random eruptions of clouds of firefly ejaculate) dies down and the impromptu orgy subsides, the female flies away impregnated and twenty-some males fly away satisfied. Confused, but satisfied.
Whenever a phenomenon that causes great fun in nature develops, there is always something that turns up with the primary intention to exploit the hell out of it.
That second firefly from above, Photuris, is that day-ruiner. Photuris fireflies are predators…of other firefly species. Instead of using their light-making powers for good and for procuring sexy times, they’ve turned it into a weapon a light of ill-intent. Along the way, Photuris turned to the dark side of the Force. Somewhere in their recent evolutionary history, these fireflies discarded their green power rings for, uh, orange? Red? Whatever.
Photuris females have evolved the crafty, deceptive behavior of mimicking the affirmative response of the aforementioned Photinus female. Photinus males signal, Photuris females flash back in a perfect imitation, and the males converge to get some nookie, and then this happens:
Consequence #32,691 of thinking with your genitals
It is this om nom noming of hapless, horny firefly males that has given this particular genus of firefly the name ‘femme fatale’ fireflies. Photuris also goes after other small insects, but the females of the species have specialized in dining on the males of closely related species. To describe this phenomenon in familiar human terms and scenarios, imagine that an attractive woman at a bar, who has been getting hit on by some half-intoxicated jagaloon, leads him out of the building. But, instead of the two of them leaving together, it turns out she’s a gorilla in a human-suit, and she dines on his organs in the middle of the alleyway. That is essentially what is going on here for these fireflies.
There are multiple examples of bioluminescence occurring in arthropods (like with fireflies), but only one example of it happening in millipedes, those many-legged, peaceful herbivores. Luckily, this example genus, Motyxia, can be found right here in the U.S. (err, assuming most of the people reading this are American). And, if you live on the West Coast, you’re in an even larger bit of luck. The eight species of Motyxia, known as Sierra luminous millipedes, are found only in southern California specifically in the southern Sierras, the Tehachapi Mountains, and the Santa Monica Mountains. They can be found in giant sequoia and oak forests, and like most members of the order of millipede to which they belong (Polydesmida), they are completely blind. During the day, they spend much of their time underneath loose soil and leaf litter on the forest floor, and they look like this:
But when night falls, they emerge from their hiding places and crawl around feeding on rotting vegetation in the typical millipede fashion. However, in the darkness, unlike all other millipedes…
…they look like glow sticks with legs.
Not much is known yet about how bioluminescence works in Motyxia. It is only the exoskeleton that emits light, and it increases with intensity when the millipede is handled and/or agitated. Because if I could light up, and folks were bothering me about it, I’d try to crank up the power and blind them with my resplendence too. Scientists aren’t sure of the precise compound or reaction responsible for this, but it is known to be based on an unknown photoprotein, which tend to fluoresce when exposed to an outside factor (like UV light, such as in green fluorescent protein, or GFP). As for the evolutionary function, we aren’t too sure of that yet either. It would seem that such a property would be a bit of hindrance to survival in a forest full of hungry predators. Being a slow, blind, easily seen animal initially makes one think that these millipedes are suicidal, and are glowing on purpose. Some field studies have suggested that the bioluminescence acts as a warning signal to predators, as bioluminescence was shown to negatively impact predation rates. This strategy, similar to the role of bioluminescence in firefly young, would make sense, seeing as how like many species within the order Polydesmida, Motyxia produces cyanide in its body, making it one hell of an ‘impactful’ meal for a nocturnal shrew or fox.
For those of us living in the Pacific Northwest, we are likely already familiar with a close relative of Motyxia. In the same family (Xystodesmidae), is the yellow-spotted millipede, or Harpaphe haydeniana, and it can be found all along the northern Pacific Coast from Alaska down to California.
This yellow-spotted millipede has yellow spots. Imagine that.
These little guys are hard to miss. When I lived on the southern Oregon Coast, I’d see tons of them all over the place on the forest floor during the torrential and long-lasting winter rains. I’d curiously watch them walk over downed doug-fir branches and chunks of bark. At times I was tempted to pick them up and have them walk over my hands and forearms I’m glad I never did this. Like the Sierra luminous millipedes, H. haydeniana can produce cyanide. It does this in the form of hydrogen cyanide (HCN), which is excreted through its exoskeleton when it is threatened. Of course, being picked up by inquisitive primates like ourselves very much counts as threatening behavior. It is because of this ability to squirt cyanide compounds through its exoskeletal joints that it is also called the ‘almond-scented millipede’, as cyanide can often smell like burnt almonds to humans that carry the allele for that particular genetic sensitivity to the odor. As a side note, if you are near a place that is storing or using hazardous chemicals, and the faint scent of almonds drifts along to you on a breeze, it would be wise to get your ass out of the area immediately.
Another lesser known bioluminescent animal is a terrestrial snail, Quantula striata, found in parts of Southeast Asia. It is the only known bioluminescent land gastropod (gastropod referring to Gastropoda, the group of mollusks containing ‘stomach footed’ animals like slugs, snails, nudibranchs, etc.).
There is little else unique about this humble animal other than the fact that its eggs will fluoresce slightly in the dark, and juveniles and adult snails can flash yellow-green light from a bioluminescent organ near the mouth called the ‘organ of Haneda’, named after the biologist who discovered the ability, Dr. Yata Haneda. The world of snail biology is obviously a frenetic and rapidly changing field, but the discovery of tan snails in tropical Asia with glowing faces in 1942 was likely upending enough to even throw the brakes on this endlessly tumultuous sub-discipline. The actual reason for this capacity in Q. striata is not yet known. It was once hypothesized that the flashing functioned as a means for juveniles to more easily find short-lived, perishable sources of food. By seeing their hatch-mates more easily in the dark forest understory surrounding a foodstuff, they could easily track down transient sources of food and have a better chance of survival young snails would act as their own beacons for finding temporary sources of sustenance. However, little evidence exists for this hypothesis as of yet. An alternative function postulated by the world’s 6-year-olds is that flashing mouths make it easier for the snails to kiss in the dark.
While many bioluminescent organisms are of the creepy-crawly, distantly related variety, there are a large number of good ol’ familiar, spine-having vertebrates that have their own lights to turn on. All of these are fish, and most of them live in dark environments like the deep sea or subterranean cave ecosystems. Images of deep-sea fish have been popularized in recent decades, and most folks are well-acquainted with conventional examples like lantern fish, with their out-sized, glossy eyes, black bodies, and rows of pale, button-like light organs along their flanks. Also familiar to most are the anglerfish grotesque, droplet-shaped monsters with loose skin, gaping maws, and a well-positioned shining lure females carrying along a parasitic male, fused to her body and reduced to nothing but reproductive organs, hanging on like a mindless tumor, a withered hunk of scrotal tissue. The alien visages have been recreated in cartoonish and widely-accessible platforms, like Spongebob Squarepants and Finding Nemo, and thus the horrible (and yet, physically quite small) demons of the abyss have bled into our popular culture a minute amount. And while the ‘syndromes’ of traits common to deep-sea bioluminescent fish (large mouths and teeth, reduced bodies and fins, little pigmentation, large or absent eyes, strange body forms, eerie blue light producing organs, etc.) are widespread, there are two unique examples that need addressing.
When most people think of sharks, their minds immediately go to large, dynamic super-predators. Great whites. Hammerheads. Makos. Tiger sharks. Giant, sleek macropredators that rip into surfboards (and surfers) like Ritz crackers, and ravenously turn Captain Quint into a scarlet-colored ‘person salad.’ The reality is that while these keystone, charismatic species are certainly more visible and memorable, there are a lot of sharks that don’t fit the stereotype at all. One group are the dogfish, which make up the shark order Squaliformes. They tend to be small (smaller than a human at least), and not quite the pelagic death-torpedoes expected of the shark lineage. One particular kind of squaliform shark that is dramatically different from all other sharks is the genus Isistius, of which there are three species. They are known occasionally as ‘cigar sharks’ based on their chunky, elongated and comparatively un-athletic looking bodies.
While its jock cousins spent their time chasing and killing everything, little Isistius was more interested in schoolwork, pictured here with its beloved pencil.
Isistius really is somewhat of the stereotypical ‘nerd’ of the shark realm. Small, goggle eyed, with a receding chin and bulbous snout, and an ever-present collar. But, it is how Isistius earns its other, more widely-known common name, that gives this big-eyed, somehow adorable little shark a uniquely horrific place in the deep ocean. It is also known as the ‘cookiecutter shark.’
This name comes from how this shark goes about feeding itself. Cookiecutter sharks are the only parasitic sharks, and they target large fish and sea mammals. After intercepting prey, they fasten their highly-specialized mouths (equipped with a pair of suction-creating ‘lips’) onto the flanks of something like a marlin, a whale, or a larger shark. With the help of spiracles (or as non-biologists call them, ‘holes’) on the back of their head, it creates a tight seal on the surface. It closes the spiracles, and retracts its tongue, and the negative pressure makes it nearly immovable. After becoming a living Garfield suction-cup car window decoration, it bites down and digs into its victim with these babies…
The cookiecutter shark gouges into the hide of the unfortunate host with those insanely large lower teeth (which are so derived that they act as a whole unit, and are replaced as a row all at once, instead of individually like in other sharks), wheels in a circle, and then dislodges with a round plug of delicious flesh. It then moves on to another spot on the animal, or to another animal entirely. This feeding habit typically won’t kill the miserable soul subjected to being carved at like a plane of dough for making festive holiday baked goods, but it can weaken the animal to the point of it succumbing to secondary afflictions. Apparently, being covered in crater-like wounds takes a toll on the immune system. The scars associated with these sharks are ubiquitous on large sea mammals, and some dolphins will have entire holes missing from dorsal fins.
“If I could be any animal, I’d be a whale. They look like they have such serene, peaceful lives.”
Humans aren’t immune from these feisty critters, and there have reports of attacks on underwater photographers, as well as capsized ship survivors, based on their descriptions of being bit in small, clean chunks as they floated along the waves at nighttime. The shark also routinely damages oceanographic equipment and underwater telecommunications cables. Even U.S. submarines have had to make changes from neoprene and rubber coverings on external equipment to fiberglass ones after cookiecutter sharks wreaked havoc on them, thinking they were a gastronomic jackpot.
So, observant reader, you are probably asking what the hell does this have to do with bioluminescence? Cookiecutter sharks use photophores (small light producing organs that appear as single, bright dots of light) to lure in a potential host in their dark, mesopelagic zone (the zone just deep enough for light to fail to penetrate) home. Almost the entire body is covered in these photophores:
However, cookiecutter sharks have a dark band of skin forming a collar near the head that does not light up. It is thought that the absence of bioluminescence in this one spot is the source of the lure. The hypothesis is that when the shark is producing light in all areas surrounding that collar, from the point of view of an animal below looking up at the bottom of the cookiecutter, the dark band looks like the silhouette of a small fish against the lighter surface waters way up in the water column. The shark would just slowly hang out and drift, suspended in the water column, its bioluminescence breaking up its figure from a deeper viewpoint by matching the downwelling light in a strategy known as counterillumination. The host would fail to see the outline of the cookiecutter shark looking up at the lighter waters above, and would instead see a vaguely fish-shaped, dark band. All that would be needed would be a close approach, and the cookiecutter shark would dine like a king.
The hellspawn pictured above is known as Malacosteus, or the ‘stoplight loosejaw’, and while that sounds uncomfortably like an antiquated euphemism for a prostitute you’d hear from your grandmother, it’s actually a deep-sea, bioluminescing fish. What makes the stoplight loosejaw unique is the way in which it uses its bioluminescence to catch prey. Most deep-sea animals that are bioluminescent produce green or blue light. Because longer and lower energy wavelengths of light (the reds and oranges and yellows) can’t penetrate into the ocean water that deep, most animals at these extreme depths aren’t sensitive to such wavelengths and subsequent colors. Instead, they can see higher energy wavelengths like green and blue, which is appropriately the wavelengths they use to see and lure prey, as well as find each other for reproduction. The stoplight loosejaw has exploited this selective sensitivity to wavelengths of light through use of a separate, large photophore positioned right underneath the eye (observable below as a pale, banana-shaped patch):
Clearly one of the animal kingdom’s undersold beauties.
This special photophore puts out a red light. Combined with a small, nearby green-glowing photophore, this arrangement inspired the fish’s common name. Stoplight loosejaws, it is thought, use large red light-producing photophores to illuminate the location of prey items without being seen by red-insensitive organisms. You see, the stoplight loosejaw also has the uncanny ability to see the red light it is producing a trait very uncommon to deep-sea fish. This brilliant strategy of ‘I-see-you-but-it’s-physically-impossible-for-you-to-see-me’ is made possible through a certain component of the stoplight loosejaw’s diet. While it has evolved to eat moderately-sized fish as an ambush predator, it snacks between meals on copepods, which are small, plentiful crustaceans. From these copepods, it obtains a derivative of chlorophyll as a photosensitizer, which it then uses in its bizarre visual system. This derivative absorbs red wavelengths of light (at around 700 nanometers), and then stimulates two intrinsic visual pigments already present in the eyes of the fish, which have a maximum absorbances in the green-blue range (typical of most deep-sea fish). So, a molecular tool stolen from the stoplight loosejaw’s diet is used to bypass limitations set-up by millions of years of evolution of the deep-sea visual system, and allow for the recognition of red wavelengths. This system is a bit like eating a hamburger that allowed you to see through people’s clothes.
Bioluminescence is not limited to just mobile animals, and other kingdoms of life have gotten on the glow train. Fungi, denizens of our weird, moisture-loving sister kingdom, also have bioluminescent representatives. One of the most striking is Panellus stipticus, the ‘bitter oyster’ or ‘luminescent panellus’, found in deciduous woodlands over much of the Northern Hemisphere and Australia. It is an important ‘white rot’ (referring to the ability to break down lignin as well as cellulose and hemicellulose in wood, giving the rotting remains a soft, pale, mushy quality) fungus of hardwood trees, and most strains of the fungus produce some sort of greenish light in the majority of tissues in a mystical, Pandora-esque evening show.
“In Soviet Russia, mushroom trips out on you!”
Bioluminescent fungi like this (and there are some 60 known, diverse species) were the inspiration for the notion of ‘foxfire’, which dates back to at least Aristotle’s earliest account of the phenomenon some 2300 years ago. Foxfire, not to be confused with a similarly named internet browser, was simply a whimsical acknowledgement of strange glowing wood in the forest and in outdoor wooden structures. For centuries, foxfire was spun into supernatural yarns and included in the greater, pre-Industrial forest dweller mythos alongside such folklore as the Will-o’-the-wisp. It wasn’t until the 1820s that someone finally figured out the fungal origins and put all the superstitious nonsense to rest by examining a rotting support beam in a mine that housed a glowing fungus. Go Enlightenment!
We now know that bioluminescence in fungi is normally due to the luciferase reaction the same chemical cascade seen in fireflies. As for its function, this is not clear. It appears over a wide diversity of distantly related fungal species, and appears to have evolved separately multiple times. Some have thought that it serves as a mechanism to attract insects or herbivores so that it can deposit its spores on their bodies, and have their genetic material dispersed throughout the forest. However, seeing as how in many species, the fruiting body (the ‘mushroom’ you actually see above ground) that contains the spores will not glow, while the subterranean mycelium network will luminesce…this hypothesis doesn’t seem like an adequate explanation.
If you’re thinking to yourself that eating one of these crazy neon caps will punch you a ticket to the psychedelic land of the Na’vi, please know that you will be sorely disappointed. While bioluminescent fungi give the impression of being saturated with mystical, consciousness-expanding powers, this impression really is only gills deep. Many bioluminescent fungi, while they appear as though they taste of sour apple and can transport you a neverending field of wonder and bliss, are actually quite cruelly toxic. One example is the jack ‘o lantern mushroom (Omphalotus olearius) of the northeastern U.S. It gives off a weak green glow in the dark, and looks like this:
Its similar appearance in the day time to chanterelles, and overall pleasing smell, makes poisoning by jack ‘o lantern mushroom relatively common. The effects are of the typical bad shroom variety vomiting, stomach cramps, and explosive diarrhea until you wish for death. However, since the toxin in this species (illudin) is non-lethal, you’ll have to suffer through it for a few days. Lucky you.
So, remember kids, just because it looks pretty and smells pretty and looks a bit like something that is actually safe to eat…doesn’t mean you have the green light (so to speak) to make a meal out of it. I’m considering beginning a solo (oh and how could it be any other way) campaign to bring warning and skepticism to the realm of bioluminescent mushrooms. Of course, I’d have to combat shameless, irresponsible glorification of these fallaciously friendly fungi by the media and entertainment industry…
Up until now, I’ve only been talking about organisms that generate their own light via chemical processes in their own cells. There exists an entirely different route for bioluminescence to occur stealing it from microorganisms. One such useful microorganism is Vibrio fischeri, which is found in our oceans. V. fischeri uses the familiar luciferin-luciferase pathway to generate light, and in its natural state, is a free-swimming organism. However, multiple multicellular animals have evolved a symbiotic relationship with the bacteria, and inoculate specialized organs with them, and house a regulated colony within themselves in order to cash in on the benefits of bioluminescence, while providing the bacteria with shelter and nutrition. One such relationship exists between V. fischeri and bobtail squid of the cephalopod order Sepiolida. Bobtail squid are closely related to cuttlefish and frequent shallow tropical waters of the Indian and Pacific Oceans. Their generally chunky, rounded mantles, short tentacles, and overall sickening levels of ‘kawaii-ness’ have also given them the names ‘dumpling squid’ and, I shit you not, ‘stubby squid.’ Bobtail squid have a light organ in their mantle which houses the bioluminescent bacteria, which they supply dutifully with hard-earned sugars and amino acids. In return, the bobtail squid can use the bacterial light to break up its silhouette against the downwelling sunlight or moonlight from above (much like with the cookiecutter shark), effectively camouflaging it from both prey and predator. The squid does this by careful articulations of the interior of the light organ, reflecting the light in tightly orchestrated ways between reflective surfaces. This alliance is effective for the survival of both partners, but there are still imperfections.
*snork* Nice vintage blue leopard print, bro. You gonna start wearing headbands too?
So yes, even tiny microorganisms routinely develop the capacity to engage in the great bioluminescence game. In fact, one of the most spectacular displays of bioluminescence comes from lowly single-celled organisms, once amassed in large numbers. The following example is dear to my heart, so I will undoubtedly come off as incredibly biased (but only because it’s the coolest thing I’ve ever seen).
These little fellows are Noctiluca scintillans, a common marine dinoflagellate protist found worldwide in shallow coastal waters. It is bound to these coastal regions because its chief food are photosynthetic algaes that require access to sunlight in shallow seas and continental shelves. They are capable of producing a blue-green light via small ‘microsource’ organelles that utilize the luciferin-luciferase system literally thousands of these organelles pepper the inside of these lily-pad shaped cells. Individually, the light output from a single Noctiluca is negligible, of course. However, when conditions are perfect for the production of their food source (usually the result of seasonal circulation patterns merging with temporary high-nutrient conditions close to shore, increasingly due to nitrate pollution), a ‘bloom’ or ‘red tide’ occurs, and the density of microorganisms in the waves offshore explodes, including Noctiluca. What results is a ‘phosphorescent tide’, in which the waves literally glow an icy blue-green as they crash onto the shore. As the dinoflagellates are disturbed by mechanical motion of the waves, or by human swimming, they fire their lights, causing an impossibly beautiful seascape to unfold.
It is because of this effect during blooms that N. scintillans is often referred to as sea sparkle. I had the privilege of seeing this once when I lived on the Oregon Coast one warm summer night as a teenager. I was completely ignorant of the cause of this miraculous happening, and was caught up in the surprise and wonder of it all. Everything glowed brilliantly. When one stepped on the soaked sand as the most recent wave pulled away, the pressure from the foot would result in a radiating surge of glittery blue light to spread outwards across the sand, signaling the locations of stranded clumps of sea sparkle. Running through those cold waves that night, bathing in their transient, magical light, is an experience I cannot forget, and I hope to have once again.
So, bioluminescence is a bit of a recurrent ability in many forms of life on Earth. It’s used to get other members of the species in the sack, to serve as a clever trick to nab some grub, and to warn bigger and badder creatures to refrain from giving you a taste. It goes beyond the scope of a few select animals like fireflies and weird, abyssal fish, and fits into a broad range of evolutionary contexts. As seemingly special and otherworldly as bioluminescence is, in reality, it’s no more than another tool available to organisms on this planet to propagate their genetic material. Perceived beauty cannot detract from nature’s inherent indifference, no matter how much art or poetry we attempt to assign to it. Perhaps in knowing this indifference, that these gorgeous lifeforms illuminating the dark have no intent to awe us, to inspire us, makes them all the more beautiful. Their artfulness is accidental, as it should be, and we humans are observers, standing at the center of nothing, and certainly not their universe. Us and them? Just little bits of leftover stardust, glowing and non-glowing, drifting along like we have for billions of years. I’m not sure about you, but I’m pretty much okay with that.
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Evolution is a rich and dynamic process. Species respond to pressures in a variety of ways, most of which reduce to finding food, avoiding becoming someone else’s food and attracting a mate. To solve that last one the animal kingdom is replete with fantastic, bizarre and mesmerizing adaptions. The bioluminescent courtship displays of ostracods may encapsulate all three.
Ostracods are peculiar animals. No larger than a sesame seed, these crustaceans have a clam-like shell and often lack gills. Like many sea creatures, a number of ostracods take advantage of bioluminescence to avoid predation and to attract mates. It is this latter use that attracted the attention of UC Santa Barbara doctoral student Nicholai Hensley in his search to better understand the interplay between biochemistry and evolutionary change.
To create their entrancing light displays, cypridinid ostracods expel a bit of mucus injected with an enzyme and a reactant, and then swim away from the glowing orb to repeat the act again. The result is a trail of fading ellipses, or will-o’-the-wisps hanging in the water column. And the length of each of these pulses is a major component of the courtship display. Some are quick like an old-fashioned flashbulb, said Hensley, while others linger in the water.
In a classic scenario, you’d expect to find a clear correlation between how long the flash lasts and the structure of the enzyme responsible for it, said Hensley. “And that’s true for some of the species, but it’s not true for all of the species.”
Instead, Hensley and his colleagues discovered that two mechanisms influence the duration of the light pulses. An animal using enzymes with a slower reaction rate will create a longer glow, but so too will one that spits out a greater amount of reactant, which takes the enzymes longer to exhaust. Both of these are at play in different combinations across the different species.
“That was one of the surprising results we got out of our paper,” said Hensley. The team’s findings appear in the Royal Society journal Proceedings B.
This discovery was due in part to the group of animals Hensley chose to study. Because ostracods spit out their light, Hensley could study the chemistry separately from the behavior of the animal itself. Contrast this with fireflies, in which the reaction happens inside their bodies. As a result, it’s under the animal’s behavioral control the whole time, explained Todd Oakley, a professor in UC Santa Barbara’s department of ecology, evolution and marine biology, and Hensley’s advisor and coauthor. “We can get at more in terms of the specifics of the chemistry because it’s outside the body,” he said.
The relationship between the two mechanisms may even influence how different species evolve in the future. For instance, if one species tends toward ever longer pulses, they may run up against the maximum of what the enzyme is capable of. Without the ability to make the enzyme more efficient, this species may evolve to use more of the chemical per pulse to achieve a longer flash.
Hensley is currently investigating how certain changes in the enzyme affect its ability to produce light: make it work faster, slower, or not at all. He also hopes to reconstruct the group’s ancestral enzyme and test its functions to see how it may have differed from the ones the animals use today.
At the same time, the team is turning an eye toward behavioral aspects of the ostracods’ mating display. For instance, they’d like to determine how much pulse length matters to female ostracods, compared to aspects like spacing or direction. Males of certain species synchronize their displays when surrounded by other males, creating a mesmerizing underwater light show. Hensley plans to take a closer look at this behavior in collaboration with colleagues at University of Kansas.
“Just describing how such diversity arises is our goal,” said Hensley, “and this may give us insight into how it actually occurs.”
From Fins to Limbs and Water to Land: Evolution of Terrestrial Movement in Early Tetrapods
The aerial scene depicts two Late Devonian early tetrapods — Ichthyostega and Acanthostega — coming out of the water to move on land. Footprints trail behind the animals to show a sense of movement. Credit: Davide Bonadonna
The water-to-land transition is one of the most important and inspiring major transitions in vertebrate evolution. And the question of how and when tetrapods transitioned from water to land has long been a source of wonder and scientific debate.
Early ideas posited that drying-up-pools of water stranded fish on land and that being out of water provided the selective pressure to evolve more limb-like appendages to walk back to water. In the 1990s newly discovered specimens suggested that the first tetrapods retained many aquatic features, like gills and a tail fin, and that limbs may have evolved in the water before tetrapods adapted to life on land. There is, however, still uncertainty about when the water-to-land transition took place and how terrestrial early tetrapods really were.
A paper published today (November 25, 2020) in Nature addresses these questions using high-resolution fossil data and shows that although these early tetrapods were still tied to water and had aquatic features, they also had adaptations that indicate some ability to move on land. Although, they may not have been very good at doing it, at least by today’s standards.
Lead author Blake Dickson, PhD in the Department of Organismic and Evolutionary Biology at Harvard University, and senior author Stephanie Pierce, Thomas D. Cabot Associate Professor in the Department of Organismic and Evolutionary Biology and curator of vertebrate paleontology in the Museum of Comparative Zoology at Harvard University, examined 40 three-dimensional models of fossil humeri (upper arm bone) from extinct animals that bridge the water-to-land transition.
Three major stages of humerus shape evolution: from the blocky humerus of aquatic fish, to the L-shape humerus of transitional tetrapods, and the twisted humerus of terrestrial tetrapods. Columns (left to right) = aquatic fish, transitional tetrapod, and terrestrial tetrapod. Rows = Top: extinct animal silhouettes Middle: 3D humerus fossils Bottom: landmarks used to quantified shape. Credit: Courtesy of Blake Dickson
“Because the fossil record of the transition to land in tetrapods is so poor we went to a source of fossils that could better represent the entirety of the transition all the way from being a completely aquatic fish to a fully terrestrial tetrapod,” said Dickson.
Two thirds of the fossils came from the historical collections housed at Harvard’s Museum of Comparative Zoology, which are sourced from all over the world. To fill in the missing gaps, Pierce reached out to colleagues with key specimens from Canada, Scotland, and Australia. Of importance to the study were new fossils recently discovered by co-authors Dr. Tim Smithson and Professor Jennifer Clack, University of Cambridge, UK, as part of the TW:eed project, an initiative designed to understand the early evolution of land-going tetrapods.
The researchers chose the humerus bone because it is not only abundant and well preserved in the fossil record, but it is also present in all sarcopterygians — a group of animals which includes coelacanth fish, lungfish, and all tetrapods, including all of their fossil representatives. “We expected the humerus would carry a strong functional signal as the animals transitioned from being a fully functional fish to being fully terrestrial tetrapods, and that we could use that to predict when tetrapods started to move on land,” said Pierce. “We found that terrestrial ability appears to coincide with the origin of limbs, which is really exciting.”
The evolutionary pathway and shape change from an aquatic fish humerus to a terrestrial tetrapod humerus. Credit: Courtesy of Blake Dickson
The humerus anchors the front leg onto the body, hosts many muscles, and must resist a lot of stress during limb-based motion. Because of this, it holds a great deal of critical functional information related to an animal’s movement and ecology. Researchers have suggested that evolutionary changes in the shape of the humerus bone, from short and squat in fish to more elongate and featured in tetrapods, had important functional implications related to the transition to land locomotion. This idea has rarely been investigated from a quantitative perspective — that is, until now.
When Dickson was a second-year graduate student, he became fascinated with applying the theory of quantitative trait modeling to understanding functional evolution, a technique pioneered in a 2016 study led by a team of paleontologists and co-authored by Pierce. Central to quantitative trait modeling is paleontologist George Gaylord Simpson’s 1944 concept of the adaptive landscape, a rugged three-dimensional surface with peaks and valleys, like a mountain range. On this landscape, increasing height represents better functional performance and adaptive fitness, and over time it is expected that natural selection will drive populations uphill towards an adaptive peak.
Dickson and Pierce thought they could use this approach to model the tetrapod transition from water to land. They hypothesized that as the humerus changed shape, the adaptive landscape would change too. For instance, fish would have an adaptive peak where functional performance was maximized for swimming and terrestrial tetrapods would have an adaptive peak where functional performance was maximized for walking on land. “We could then use these landscapes to see if the humerus shape of earlier tetrapods was better adapted for performing in water or on land” said Pierce.
“We started to think about what functional traits would be important to glean from the humerus,” said Dickson. “Which wasn’t an easy task as fish fins are very different from tetrapod limbs.” In the end, they narrowed their focus on six traits that could be reliably measured on all of the fossils including simple measurements like the relative length of the bone as a proxy for stride length and more sophisticated analyses that simulated mechanical stress under different weight bearing scenarios to estimate humerus strength.
“If you have an equal representation of all the functional traits you can map out how the performance changes as you go from one adaptive peak to another,” Dickson explained. Using computational optimization the team was able to reveal the exact combination of functional traits that maximized performance for aquatic fish, terrestrial tetrapods, and the earliest tetrapods. Their results showed that the earliest tetrapods had a unique combination of functional traits, but did not conform to their own adaptive peak.
“What we found was that the humeri of the earliest tetrapods clustered at the base of the terrestrial landscape,” said Pierce. “indicating increasing performance for moving on land. But these animals had only evolved a limited set of functional traits for effective terrestrial walking.”
The researchers suggest that the ability to move on land may have been limited due to selection on other traits, like feeding in water, that tied early tetrapods to their ancestral aquatic habitat. Once tetrapods broke free of this constraint, the humerus was free to evolve morphologies and functions that enhanced limb-based locomotion and the eventual invasion of terrestrial ecosystems
“Our study provides the first quantitative, high-resolution insight into the evolution of terrestrial locomotion across the water-land transition,” said Dickson. “It also provides a prediction of when and how [the transition] happened and what functions were important in the transition, at least in the humerus.”
“Moving forward, we are interested in extending our research to other parts of the tetrapod skeleton,” Pierce said. “For instance, it has been suggested that the forelimbs became terrestrially capable before the hindlimbs and our novel methodology can be used to help test that hypothesis.”
Dickson recently started as a Postdoctoral Researcher in the Animal Locomotion lab at Duke University, but continues to collaborate with Pierce and her lab members on further studies involving the use of these methods on other parts of the skeleton and fossil record.
Reference: “Functional Adaptive Landscapes Predict Terrestrial Capacity at the Origin of Limbs” by Blake V. Dickson, Jennifer A. Clack, Timothy R. Smithson and Stephanie E. Pierce, 25 November 2020. Nature.
Making light of bioluminescence
I used to think there was a small molecule called luciferin that emitted the light of bioluminescence. I was not exactly wrong, but there is not just one luciferin. There are many, and to look at their molecular structures you’d be justified in concluding they have nothing in common with one another.
The best known is firefly luciferin, a dimer of two thiazol derivatives: that is, of two five-membered heterocyclic rings containing sulfur and nitrogen. Then there’s bacterial luciferin, which is a derivative of vitamin B2 (riboflavin). Some fungi glow because they contain a derivative of hispidin, a conjugated molecule based on pyrone. Some single-celled marine organisms called dinoflagellates harbour an impressive luciferin related to chlorophyll, in which the porphyrin ring has been opened up at one point.
As this diversity of luciferins testifies, bioluminescence is not a trick learnt long ago in evolutionary history and then passed on throughout the tree of life. It arose independently many times (perhaps more than 50), a fact evident also in the enzymes that react with luciferins to cause light emission. Called luciferases, these proteins are very different in their structures: the genes encoding them are not closely related analogues of one another, but seem to have independent origins. Some bioluminescent systems also involve accessory proteins that modify the emission wavelength of the luciferin.
And yet all of these systems use the same basic mechanism: the enzymes use molecular oxygen to oxidise the luciferin into an electronically excited product that sheds its excess energy by releasing a photon. In this respect, bioluminescence is a classic example of convergent evolution: natural selection ‘discovered’ this process for making light many times over, in each case finding its way to the same underlying chemistry.
The cookie-cutter shark uses a fiendishly clever hunting strategy
What’s even more striking is that bioluminescence plays quite different roles in different organisms. 1 Some crustaceans and fish, for example, use the light to signal to prospective mates. Others use it to lure prey, such as the deep-sea anglerfish (where the light from the bulb atop the pole that protrudes from the fish’s head is actually generated by symbiotic bioluminescent bacteria). The cookie-cutter shark uses a fiendishly clever hunting strategy: green bioluminescence on its underside hides its silhouette from potential prey below it while leaving a tapered dark band across its throat that is thought to attract prey (such as dolphins, whales and seals) by mimicking the shape of a much smaller fish.
Many marine species use bioluminescence for warning or evasion, confusing or frightening potential predators with their bursts of light. This seems too to be the function of light emission in dinoflagellates, who might use it as a kind of ‘burglar alarm’: if a predator sets it off, it alerts even bigger predators to tackle the intruder. When pressure deforms the cell walls of these single-celled protists, mechanically sensitive ion channels open. This produces a flux of calcium ions that changes the transmembrane electrical potential and triggers the opening of proton channels. The resulting change in pH stimulates the luciferase proteins into action, transforming the organism’s luciferin within vesicles that surround the cell nucleus and producing blue-green emission. Raymond Goldstein of the University of Cambridge, UK, and his coworkers have recently measured how the intensity of light emission from individual Pyrocystis lunula dinoflagellates is related to the degree of deformation of their cell walls, using glass micropipettes both to squeeze the cells directly and to fire jets of water at them. 2
This is the main source of the ghostly glow that can be seen in tropical and subtropical oceans at night: the shear forces caused by water flow in breaking waves or in the wake of a boat are enough to trigger emission from the microscopic organisms. Charles Darwin wrote of “two billows of liquid phosphorus” that he saw at the prow of the Beagle.
Independent evolution in very different species implies that the trick of chemiluminescence can’t be so hard to learn
Bioluminescence is one of those natural processes that seems so exquisitely designed that it’s baffling how natural selection could have hit upon it. All the same, its independent evolution in very different species implies that the trick of chemiluminescence can’t really be so hard to learn after all. A potential resolution of this apparent paradox is that the oxidative chemical reaction they share in common arose initially for a quite different but ubiquitously important purpose: to soak up reactive oxygen species that might otherwise damage delicate biomolecules. 1,3
In this view, the luciferase enzyme began as a protein that would dump these oxygen species onto some convenient sink molecule: some luciferases and luciferins do indeed have anti-oxidant properties. If this idea is correct, it would make bioluminescence an example of the evolutionary process of exaptation, where a trait evolved for one purpose comes to serve another. It’s a reminder that nature is an opportunist, and develops its strategies wherever it can find them.
1 E A Widder, Science, 2010, 328, 704 (DOI: 10.1126/science.1174269)
2 M. Jalaal et al, Phys. Rev. Lett., 2020, 125, 028102 (DOI: 10.1103/PhysRevLett.125.028102)
3 J F Rees et al, J. Exp. Biol., 1998, 201, 1211