Tuatara: reintroduction of a living fossil

There’s a reptile in New Zealand whose lineage arose in the time of the dinosaurs. Even if its external appearance is similar to that of a lizard, the tuatara (whose name means “spiny back” in the Maori language) is an animal with many unique characteristics that classify it in an order different from the other reptiles. In this entry we’ll explain the main characteristics of this relic from the past, as interesting as endangered.

ORIGIN AND EVOLUTION

The tuataras are unusual reptiles whose lineage goes back to 240 million years ago, at the middle Triassic. Tuataras are lepidosaurs, yet they form a different lineage from the squamates, and that’s why they are found in their own order, the rhynchocephalians (order Rhynchocephalia). Lots of species flourished during the Mesozoic, even if almost all of them were replaced by squamates. At the end of the Mesozoic only one family survived, the Sphenodontidae.

Homoeosaurus fossil, an extinct relative of the tuataras. Photo by Haplochromis.

Of all the existing sphenodontids, only tuataras have survived to the present day. Traditionally it was considered that tuataras included two species: the common tuatara (Sphenodon punctatus) and the Brother’s Island tuatara (Sphenodon guntheri), although recent analyses have popularized the idea that the tuatara is only one species, S. punctatus.

TUATARA ANATOMY

As we have already stated, tuataras look externally like a lizard, having a certain resemblance to iguanas. Male tuataras are larger than females, measuring up to 61 cm in length and one kilogramme of weight, while females only measure 45 cm and weigh half a kilo. Tuataras present a spiny crest on their backs which give them their common name. This crest is bigger in males, and can be erected as display.

Photo by KeresH of a young male tuatara.

What really distinguishes the tuataras is their internal anatomy. All the other reptiles have modified greatly their skull structure, but tuataras have maintained the original diapsid configuration without most changes. While crocodiles and turtles have developed a sturdy skull, tuataras conserve wide temporal openings, and while squamates have developed flexible skulls and jaws, tuataras keep a rigid cranium. Also, unlike most reptiles, tuataras present no external ears.

Modified image from the drawing by Nobu Tamura of the tuatara skull. In it we can see the main characteristics that distinguish it: 1. Beak-shaped premaxilla, 2. Acrodont teeth, fused to the jaws, 3. Diapsid-like wide temporal openings and 4. Parietal or pineal opening.

The name Rhynchocephalia means “beak head” and it refers to the beak-like structure of their premaxilla. Tuataras are also one of the few reptiles with acrodont teeth, which are fused to the maxilla and the jaw, and are not renewed. Also, they present a unique saw-like jaw movement, moving it forwards and backwards.

Video by YouOriginal, of some captive tuataras feeding. In this video we can appreciate the singular jaw movement.

Finally, one of the more incredible anatomic characteristics of tuataras is that they conserve their parietal or pineal eye. This is a structure reminiscent from the first tetrapods, which connects with the pineal gland and which is involved in the thermoregulation and circadian rhythms. Even if some other animals also keep it, the tuataras present a real third eye, with complete lens, cornea and retina, even if it gets covered with scales as they age.

HABITAT AND BIOLOGY

Tuataras live in some thirty islets in the Cook Strait, between the two main islands of New Zealand. Also, the previously considered species S. guntheri is found on Brother’s Island, in the northwest of South Island. All populations live in coastal forests or scrublands, with loose soils easy to dig. Also, in most of their distribution area there are colonies of sea birds, whose nests are also used by tuataras.

Photo by Satoru Kikuchi of a typical humid forest of New Zealand.

Compared with most reptiles, tuataras live in relatively cold habitats, with annual temperatures oscillating between 5 to 28°C. Tuataras are mainly nocturnal, usually coming out of their burrows at night, even if sometimes they can be found basking in the sun during the day (especially in winter).

Tuataras have few natural predators. Apart from some introduced animals, only gulls and some birds of prey represent a danger for these reptiles. In contrast, their diet is fairly varied. Being sit-and-wait predators, tuataras feed mainly on invertebrates like beetles, crickets and spiders, even if they are able to predate on lizards, eggs and bird chicks, and even younger tuataras. As their acrodont teeth don’t renew, these get worn down in time, so older individuals usually feed on softer prey like snails and worms.

Tuataras mate between January and March (summer), when the territorial males compete for the females, which will lay around 18-19 eggs between October and December (spring). The sex of the offspring depends on the incubation temperature (males at higher temperatures and females at lower ones). The eggs will hatch after 11-16 months (one of the longest incubation periods of all reptiles), from which young tuataras will be born, who will avoid the cannibalistic adults being active mainly during the day.

Unique video of the birth of a tuatara at the Victoria University of Wellington. The translucent mark on the little tuatara’s head corresponds to the parietal eye.

As we can see based on their long incubation period, tuataras develop slowly. These reptiles do not reach sexual maturity until the age of 12, and they keep growing. Also, tuataras are extremely long-lived animals, living up to more than 60 years in the wild. In captivity they can live more than 100 years.

CONSERVATION AND THREATS

Before the arrival of man, the tuataras were present in both main islands of New Zealand and many more islets. When the first European settlers arrived, tuataras were already only found in about 32 little islands. It’s believed that the extinction of tuataras from the main islands was due to habitat destruction and to the introduction of foreign mammals like rats. Other threats include the low genetic diversity caused by isolation of the different populations and climate change, which can affect the sex of the offspring.

Current distribution map of the tuataras. The squares correspond to the old species Sphenodon guntheri, now considered a population of S. punctatus.

When the first human settlers arrived in the isles, it is thought that 80% of New Zealand was covered in forests. When the first Polynesian tribes came around the year 1250, they caused the deforestation of more than half the archipelago. Centuries later, with the arrival of Europeans, deforestation intensified even more, up to the current situation, with only 23% of the original forest still preserved.

Photo by Cliff of a Pacific rat (Rattus exulans), one of the main threats for the tuataras.

The introduction of foreign mammals has been one of the main factors of the recent decline of tuataras, especially the introduction of the Pacific rat (Rattus exulans). This rodent has affected the populations of both tuataras and many of New Zealand’s endemic bird species. In studies on coexisting populations of tuataras and rats, it has been observed that rats, apart from preying on eggs and hatchlings, also compete with adult tuataras for resources. With an extremely slow life cycle, tuataras can’t recover from this impact.

Photo by Br3nda of a reintroduced and tagged tuatara.

Yet, tuataras are currently classified as “least concern” in the IUCN red list. This is thanks to the great efforts of conservation groups that have contributed to the recovery of this species. One of the main tasks has been the eradication of the Pacific rat from the main island where tuataras live. In order to do that, a titanic effort was made in many islets where entire populations of tuataras were captured to participate in captive breeding programs, while the rats were eliminated from these islands. After their main threat was eradicated, all the captured individuals and their captive-born offspring were released in their natural habitat so they could live without such a fierce competitor.

Video by Carla Braun-Elwert, about the breeding success of an old tuatara couple.

Currently, the wild tuatara population is estimated to be between 60.000 and 100.000 individuals. It can be said that this living fossil, which was on the brink of extinction after millions of years of existence, received a second opportunity to keep inhabiting the incredible islands of New Zealand. We hope that in the future, we can keep enjoying the existence of these reptiles, the only survivors of a practically extinct lineage, for many more centuries.

REFERENCES

The following sources have been consulted during the elaboration of this entry:

• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Arkive. Tuatara (Sphenodon punctatus).
• The Reptile Database. Sphenodon punctatus.
• Department of Conservation, Te Papa Atawhai. Tuatara.
• Imagen de portada de Michal Klajban.

Desert reptiles

Deserts are some of the most extreme habitats on the planet. The Sahara, the Gobi and the Sonora are some examples of warm deserts where the high temperatures and the lack of water pose a great challenge to animals that live in them. Reptiles are one of the animal groups that present the most incredible adaptations for life in deserts. In this entry we’ll explain the difficulties that desert reptiles must face in order to survive, and we’ll introduce you to different species of snakes and lizards that in the deserts have found their home.

REPTILES IN THE DESERT

The characteristic which unites all deserts is the scarce precipitation as, unlike most people think, not all deserts present high temperatures (there are also cold deserts, like the Arctic and the Antarctic, both in danger because of the climate change). Reptiles thrive better in warm deserts than in cold deserts, because the low temperatures would not allow them to develop their life activity.

Map by Vzb83 of the warm deserts, both arid and semiarid, of the world.

Warm deserts not always have extremely high temperatures. While during the day temperatures may rise up to 45°C, when the sun goes down temperatures fall below freezing point, creating daily oscillations of up to 22°C. The different desert reptiles, being poikilotherms and ectotherms, use different behavioural strategies in order to avoid overheating during the day and to keep their body heat during the night (for example, climbing to elevated areas or sleeping in burrows).

The Namaqua chameleon (Chamaleo namaquensis) regulates its body heat changing its colouration. During sunrise it is black in colour in order to absorb as much radiation of the sun and activate its metabolism. When temperatures become higher, it turns white to reflect solar radiation. Video from BBC.

As we have already stated, the main characteristic of any desert is the lack of water. Generally, in a desert, it rains less than 250 mm of water a year. The scaly and impervious skin of reptiles prevents the loss of water, and their faeces contain uric acid which, compared to urea, is much less soluble in water, allowing them to retain more liquids. Most desert reptiles extract the water they need from their food and some drink water from the dew.

Both the extreme temperatures and the shortage of precipitations make the desert a place with very few living beings. Vegetation is scarce and animals are usually small and secretive. This lack of resources causes desert reptiles to be usually smaller than their cousins from more benevolent environments. Also, these saurians usually exploit any available food resource, although they think twice before wasting their precious energy to get their next meal.

SAND SNAKES

In many sandy deserts we can find various species of snakes (and legless lizards) that have adapted to a life among the dunes. Many of these ophidians share a locomotion method called “sidewinding”, in which they raise their head and neck from the ground and move them laterally while the rest of the body stays on the ground. When they place their head on the ground again they raise their body, making these snakes move laterally in a 45° angle. This method of locomotion makes these snakes move more efficiently in an unstable terrain. It also reduces the contact of their body with an extremely hot substrate, as the body of these ophidians only touches the ground in two points at a time.

As we can see in this video from RoyalPanthera, sidewinding allows desert snakes to move minimizing the contact with the hot terrain.

Many desert ophidians bury themselves in the sand both to avoid sun exposure and to blend in and catch their prey unaware. This has made many desert-dwelling snakes very sensitive to vibrations generated by their prey as it moves through the sand. In addition some species present an overly developed rostral scale (the scale at the tip of their snout), being much thicker in order to aid during excavation in sandy soils.

An example of this are the North American snakes of the Heterodon genus, also known as hog-nosed snakes, as they present an elevated rostral scale giving their snout a characteristic shape. Photo of Heterodon nasicus by Dawson.

The horned vipers of the Cerastes genus also present various characteristics that facilitate life in the deserts. These vipers evade high temperatures becoming active at night and they spend the day buried in the sand. Their hunting method consists in burying themselves waiting for a prey to pass by, this way saving most of their energy. It is believed that their horn-shaped supraocular scales cover their eyes when they are buried in order to protect them from the sand.

Photo by Tambako The Jaguar of a Sahara sand viper (Cerastes vipera), a species from North Africa and the Sinai Peninsula.

SPINY CRITTERS

In different deserts of the world we find reptiles with their bodies covered in spines. This not only provides them with certain protection against predators, but is also helps them blend in in a habitat with plenty of thorny plants. Two of these animals are members of the Iguania suborder: the thorny devil and the horned lizards.

Photo of a thorny devil (Moloch horridus) by Christopher Watson.

The thorny devil (Moloch horridus) is an agamid that lives in the Australian sandy deserts. This lizard presents spines all over its body, making it difficult for its predators to swallow. It also has a protuberance behind its head that acts as a fat storage.  When it feels threatened, it hides its real head between its legs and it exposes its neck protuberance as a decoy head. Probably, the most interesting adaptation of this animal is the system of small grooves among its scales, which collect any water that contacts its skin and conducts it directly to its mouth.

Horned lizards (Phrynosoma genus, affectionately called “horny toads”) are iguanids which are found in different arid habitats of North America. Similarly to the thorny devil, their body is covered in spines making them hard to eat for their predators. Also, when they are caught, they inflate their bodies to make the task even more difficult. Finally, some species like the Texas horned lizard (Phrynosoma cornutum) are known for their autohaemorrhagic abilities: when they feel cornered they squirt a stream of stinky blood from their eyes which scares away most predators.

Photo from the U.S. Fish & Wildlife Service of a Texan horned lizard (Phrynosoma cornutum).

As you have seen, in the deserts we can find reptiles with some of the most inventive (and disturbing) adaptations of the world. These are only a few examples of the astonishing diversity of squamates that are found in the deserts of the world, which only seek to survive the harsh conditions of these extreme environments. Sometimes, it’s just a matter to avoid burning your feet with the hot sand.

Video from BBCWorldwide of a shovel snouted lizard (Zeros anchietae) making the “thermal dance” in order to diminish the contact with the hot sand.

REFERENCES

The following sources have been consulted during the elaboration of this entry:

• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Digital-Desert. Desert Reptiles.
• Arizona-Sonora Desert Museum. Adaptations of Desert Amphibians & Reptiles.
• In the desert. A comprehensive list of the venomous snakes found in the desert.
• H.E.R.P. Herpetological Education & Research Project.
• Christopher J. Bell, Jim I. Mead & Sandra L. Swift (2009). Cranial osteology of Moloch horridus (Reptilia: Squamata: Agamidae). Records of the Western Australian Museum. Vol 25. Pp: 201-237.
• Horned Lizard Conservation Society.
• Cover image by Yathin S. Krishnappa.

Reptiles and mammals: same origin, different stories

Did mammals evolve from reptiles? The truth is they didn’t. Reptiles and mammals both have independent evolutionary histories that separated soon after the apparition of the so-called amniotic egg, which allowed the babies of these animals to be born outside of water. Previously, we talked about the origin of vertebrates and about how they managed to get out of the sea to start walking on land for the first time. In this entry we’ll explain how the ancestors of reptiles and mammals, the AMNIOTES, became independent of the aquatic medium and became the dominant land animals.

THE AMNIOTIC EGG

The characteristic that unites reptiles and mammals in the same group is the amniotic egg. While amphibian eggs are relatively small and only have one inner membrane, the eggs of amniotes are much bigger and present various membranes protecting the embryo and keeping it in an aqueous medium. The outer layer is the eggshell which, apart from offering physical protection to the embryo, prevents water loss and its porosity allows gas interchange. Beneath the eggshell we can find the next membranes:

Diagram of a crocodile egg: 1. eggshell 2. yolk sac 3. yolk (nutrients) 4. vessels 5. amnion 6. chorion 7. air 8. alantois 9. albumin (white of the egg) 10. amniotic sac 11. embryo 12. amniotic fluid. Image by Amelia P.

• Chorion: The first inner membrane, which offers protection and, together with the amnion, forms the amniotic sac. Also, being in contact with the eggshell, it participates in gas interchange, bringing oxygen from the outside to the embryo and carbon dioxide from the embryo to the outside.
• Amnion: Membrane that surrounds the embryo and constitutes a part of the amniotic sac. It offers an aqueous medium for the embryo and connects it with the yolk sac (a structure that brings food and that is also found in fish and amphibians).
• Allantois: The third layer, it is used as a storage for nitrogen waste products, and together with the chorion, helps in gas interchange.

Diagram of an amphibian egg: 1. jelly capsule 2. vitelline membrane 3. perivitelline fluid 4. yolk 5. embryo. Image by Separe3g.

All these different kinds of membranes eliminate the need amphibians had of laying their eggs in water. Also, unlike amphibians, amniotes don’t go through a gilled larval stage, but are instead born as miniature adults, with lungs and legs (at least those that have them). All these made the first amniotes completely independent of the aquatic medium.

AMNIOTE ORIGINS

The first amniotes evolved around 312 million years ago from reptiliomorph tetrapods. At the end of the Carboniferous period lots of tropical forests where the great primitive amphibians lived disappeared, leaving a colder and drier climate. This ended with many of the big amphibians of that time, allowing the amniotes to occupy new habitats.

Reconstruction of Solenodonsaurus janenschi, one of the candidates in being the first amniote, which lived around 320-305 million years ago in what is now the Czech Republic. Reconstruction by Dmitry Bogdanov.

CHARACTERISTICS

These early amniotes had a series of characteristics that set them apart from their semiaquatic ancestors:

• Horny claws (amphibians don’t have claws) and keratinized skin that prevents water loss.
• Bigger large intestine and higher density of renal tubules to increase water reabsorption.
• Specialized lacrimal glands and a third membrane in the eye (nictitating membrane) which keep the eye wet.
• Larger lungs.
• Loss of the lateral line (sensory organ present in fish and amphibians).

The skeleton and musculature also evolved offering better mobility and agility on a terrestrial medium. The first amniotes presented ribs that encircled their body converging at the sternum, making their inner organs more secure, and a series of muscular receptors offered them better agility and coordination during locomotion.

AMNIOTE SKULLS

Traditionally, the different amniotes were classified based on the structure of their cranium. The characteristic used to classify them was the presence of temporal openings (fenestrae), by which we have three groups:

• Anapsids (“no arches”): No temporal openings (turtles).

Diagram of an anapsid skull, by Preto(m).

• Synapsids (“fused arches”): With only one temporal opening (mammals).

Diagram of a synapsid skull, by Preto(m).

• Diapsids (“two arches”): With two temporal openings (reptiles, including birds).

Diagram of a diapsid skull, by Preto(m).

Previously it was believed that the first amniotes presented an anapsid skull (without openings, like turtles) and that subsequently they separated into synapsids and diapsids (the temporal openings formed “arches” that offered new anchor points for the jaw’s musculature). Yet, it has been discovered that this three-group classification is not valid.

Even though we still believe that the first amniotes were anapsid, it is currently known that these, soon after their apparition, separated into two different lineages: the synapsids (clade Synapsida) and the sauropsids (clade Sauropsida).

SYNAPSIDA

This lineage includes mammals and their amniote ancestors. Even though the first synapsids like Archaeothyris looked externally like lizards, they were more closely related to mammals, as they shared one temporal fenestrae where the jaw muscles passed through.

Drawing of the skull of Archaeothyris, which is thougth to be one of the first synapsids that lived around 306 million years ago in Nova Scotia. Drawing by Gretarsson.

The ancestors of mammals were previously known as “mammal-like reptiles”, as it was thought that mammals had evolved from primitive reptiles. Currently it’s accepted that synapsids form a different lineage independent of reptiles, and that they share a series of evolutionary trends that makes them closer to modern mammals: the apparition of different kinds of teeth, a mandible made of one single bone, the vertical posture of their limbs, etc…

Reconstruction of Dimetrodon grandis, one of the better known synapsids, from about 280 million years ago. Reconstruction by Dmitry Bogdanov.

Even though most modern mammals don’t lay eggs and give birth to live offspring, all groups maintain the amniote’s three characteristic membranes (amnion, chorion and allantois) during embryonic development.

SAUROPSIDA

Sauropsids include current reptiles and their amniote ancestors. Currently, in many scientific papers the word “sauropsid” is used instead of “reptile” when discussing phylogenies, as the sauropsids also includes birds. The first sauropsids were probably anapsids, and soon after their appearance they separated into two groups: the Parareptilia which conserved anapsid skull, and the Eureptilia which include the diapsids (current reptiles and birds).

Evolutionary tree of current vertebrates, in which green color marks the groups previously included inside reptiles. As you can see, the traditional conception of "reptile" includes the ancestors of mammals and excludes birds. Image by Petter Bøckman.

Diapsids are currently the most diversified group of land vertebrates. They diversified greatly in the late Permian period (about 254 million years ago), just before the Mesozoic (the Age of Reptiles). These can be divided into two main groups: the Lepidsaurs and the Archosaurs, both with representatives in our days.

LEPIDOSAURIA: SMALL AND PLENTIFUL

Lepidosaurs (literally “reptiles with scales”) appeared in the early Triassic (around 247 million years ago) and, even if most of them didn’t grow to big sizes, they are currently the largest group of non-avian reptiles. These are characterized by presenting a transversal cloacal slit, by having overlapping scales and shedding their skin whole or in patches and by other skeletal characters.

Shed skin of a rat snake. Photo by Mylittlefinger.

The current lepidosaurs belong to one of two different orders:

• Order Rhynchocephalia: That includes the two species of tuatara. Currently endangered, they are considered living fossils because they present skulls and characteristics similar to the Mesozoic diapsids.

Photo of a tuatara (Sphenodon punctatus), by Tim Vickers.

• Order Squamata: Current squamates include iguanas, chameleons, geckoes, skinks, snakes and other legless lizards. With more than 9000 living species, squamates are a large group with a wide array of adaptations and survival strategies.

Photos of some squamates, from left to right and from top to bottom: Green iguana (Iguana iguana, by Cary Bass), king cobra (Ophiophaga Hannah, by Michael Allen Smith), Mexican mole lizard (Bipes biporus, by Marlin Harms) and Indian chameleon (Chamaeleo zeylanicus, by Shantanu Kuveskar).

ARCHOSAURIA: ANCIENT KINGS

Archosaurs (literally “ruling reptiles”) were the dominant group of land animals during the Mesozoic. These conquered all possible habitats until the extinction of most groups at the end of the Cretaceous period. Some of the extinct groups were the pseudosuchians (relatives of modern crocodiles, order Crocodylia), the pterosaurs (large flying reptiles) and the dinosaurs (excepting birds, clade Aves).

Drawing of the skull of the dinosaur Massospondylus in which we can see the different characteristic openings of diapsid archosaurs. Image by Steveoc 86.

As you see, both groups of modern archosaurs couldn’t be more different. Yet, crocodiles and birds share a common ancestor, and they are both more closely related with each other than with the rest of reptiles.

Photo of two species of modern arcosaurs: a Nile crocodile (Crocodylus niloticus) and a yellow-billed stork (Mycteria ibis). Photo by Tom Tarrant.

AND WHAT ABOUT TURTLES?

Turtles (order Testudines) have always been a group difficult to classify. Turtles are the only living amniotes with an anapsid skull, without any post-ocular opening. That’s why previously they had been classified as descendants of primitive amniotes (clade Anapsida, currently disused) or as primitive anapsid sauropsids (inside the Parareptilia clade)

Skeleton of the extinct tortoise Meiolania platyceps which lived in New Caledonia until 3000 years ago. In this photo it can be seen the compact cranium without openings. Photo by Fanny Schertzer.

Recent molecular studies have revealed that turtles are actually diapsids that lost their temporal openings secondarily. What still divides the scientific community is if testudines are more closely related to Lepidosauromorphs (lepidosaurs and their ancestors) or to Archosauromorphs (archosaurs and their ancestors).

Individual leopard tortoise (Stigmochelys pardalis) from Tanzania. Photo by Charles J. Sharp.

As you have seen, the evolution of amniotes is an extremely complex matter. We hope that with this entry some concepts have been clarified:

1. Mammals (synapsids) come from an evolutionary lineage different from that of reptiles (sauropsids).
2. Sauropsids include traditional reptiles (lepidosaurs, archosaurs and turtes) and birds (inside archosaurs).
3. There’s still so much to investigate about the placement of turtles (testudines) in the evolutionary tree of sauropsids.

Modified diagram about the evolutionary relationships of the different amniote groups.

REFERENCES

During the elaboration of this entry the following sources have been consulted:

• Cover image by Henri Pidoux.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Hickman, Roberts, Keen, Larson, l’Anson & Eisenhour (2009). Principios integrales de Zoología (decimocuarta edición). Mc Graw Hill.
• http://www.biologyreference.com/A-Ar/Amniote-Egg.html
• http://www.ucmp.berkeley.edu/vertebrates/tetrapods/amniota.html
• http://tolweb.org/Amniota
• http://onlinelibrary.wiley.com/doi/10.1111/j.1095-8312.1979.tb00027.x/abstract
• https://courses.candelalearning.com/osbiosec/chapter/29-4-reptiles/

How do temperature and global warming affect the sex of reptiles?

In most animals the sex of an individual is determined at the moment of fertilization; when the egg and the sperm fuse together it is fixed if that animal will be male or female. Yet in many reptilian groups sex determination is established later during incubation, and the determinant external factor is the incubation temperature of the eggs. In reptiles, this means that the environment plays a crucial role in determining the sex ratio emerging from an egg clutch, and that these animals are very susceptible to alterations in temperature caused, for example, by climate change.

SEXUAL DETERMINATION: GSD VS TSD

In the majority of animal species, sexual differentiation (the development of ovaries or testes) is determined genetically (GSD). In these cases, the sex of an individual is determined by a specific chromosome, gene or allele which will cause the differentiation to one sex or the other. In vertebrates there exists two main types of GSD, the XX/XY system in mammals (in which XX is a female and XY is a male) and the ZW/ZZ system in birds and some fishes (ZW corresponds to a female and ZZ to a male).

Examples of different types of genetic sexual determination systems found in vertebrates and invertebrates, by CFCF.

In the case of reptiles, there is a great variety of sexual determination mechanisms. Some present GSD models; many snakes follow the ZW/ZZ system and some lizards the XX/XY. Still, in many groups the sex of the offspring is determined mainly by the egg incubation temperature (TSD), and therefore the environment plays an important role in the proportion of males and females found in a population.

The eastern bearded dragon (Pogona barbata) is an example of a reptile with GSD, but which is also affected by incubation temperature. Photo by Trent Townsend.

Nevertheless, the genetic and temperature sexual determination are not mutually exclusive. Reptiles with TSD have a genetic base for the ovarian and testicular differentiation which is regulated by temperature. Similarly, it’s been observed that in reptiles with DSG, such as the eastern bearded dragon (Pogona barbata), high temperatures during incubation causes genetically male individuals (ZZ chromosomes) to develop functionally as females. This proves that in reptiles, there is no strict division between GSD and TSD.

TEMPERATURE AND SEX

The incubation period during which the sex of an individual is determined is called thermosensitive period and usually corresponds to the second third of the incubation period, during which temperature must be maintained constant. This critical incubation period usually lasts between 7 and 15 days, depending on the species. After this period the sex of an individual usually cannot be reversed (all or nothing mechanism).

Komodo dragon baby (Varanus komodoensis) hatching. Photo by Frank Peters.

Temperature during the critical incubation period affects the functioning of the aromatase, a hormone which converts androgens (masculinizing hormones) to estrogens (feminizing hormones). At male-producing temperatures, the activity of the aromatase is inhibited, while at female-producing temperatures the activity of the aromatase is maintained.

Graphics of the aromatase’s activity related to gonadal hormones on European pond turtle’s embryos (Emys orbicularis) at 25oC (males) and at 30oC (females), during the critical incubation period, from Pieau et al. 1999.

The TSD is found in all reptile groups except snakes (which have the ZW/ZZ system). In lizards and turtles we can find both genetic-based and temperature-based sexual determination, while in tuataras and crocodilians sex is determined exclusively by temperature. Currently, different patterns of temperature sex determination are known.

PATTERN I

This pattern is the simplest one, in which higher incubation temperatures produce one sex and lower incubation temperatures produce the other sex. Intermediate temperatures usually produce individuals of both sexes and very rarely, intersex individuals. This pattern can be further divided in:

• Pattern Ia TSD, in which eggs incubated at warmer temperatures produce high female percentages and eggs incubated at cooler temperatures produce high male percentages. This pattern is found in many species of turtles.

Photo of a European pond turtle (Emys orbicularis), species that follows the pattern Ia TSD; at 25oC or less during incubation only males are born, while at 30oC or more only females are born. Photo by Francesco Canu.

• Pattern Ib TSD, in which the contrary occurs; high temperatures produce males and low temperatures produce females. We find this pattern in some lizards with TSD and in the tuataras.

The tuatara (Sphenodon punctatus) is one of the reptiles that follows the pattern Ib TSD; the pivotal temperature is between 21-22oC, above which males will be born and below which females will be born.

PATTERN II

This pattern is a bit more complex than the previous one. In this one, embryos incubated at extreme temperatures (very high or very low) will differentiate to one sex, while the ones incubated at intermediate temperatures will differentiate to the other sex.

Photo of different aged American alligators (Alligator mississippiensis). These reptiles follow the pattern II TSD; at about 34oC males are born, and at higher and lower temperatures, females are born.

This pattern appears in crocodilians, some turtles and in many lizards. Recent phylogenetic studies indicate that this is the ancestral TSD model in reptiles. Some people even argue that all the TSD cases belong to the pattern II, but that in nature temperatures never reach both extremes, although this is yet to be proved.

TEMPERATURE DETERMINED SEX: PROS AND CONS

Even today the evolutionary advantages of the sex determination by temperature are not fully understood. The case of the reptiles is pretty curious because birds, mammals and amphibians determine their sex genetically in most cases, while in reptiles there is a bit of everything.

Currently, there are studies which are being conducted to see if certain temperatures improve the health of males and if other temperatures the health of females. In one of these studies, it was observed that snapping turtles incubated at intermediate temperatures (which produced both males and females) were more active than the ones incubated at temperatures producing only one sex, making them more vulnerable to be attacked by sight-based predators. Currently, there isn’t enough evidence that indicates to what extent these discoveries could be applied. It is possible that reptiles with TSD are able to manipulate the sex of its offspring, altering the proportion of sexual hormones based on the temperature of their nesting site.

Common snapping turtle (Chelydra serpentina) an American fresh-water chelonian, laying its eggs. Photo by Moondigger.

The disadvantages of the TSD are much easier to predict.  Any change in the environmental temperature of the nesting areas may affect negatively the populations of a determined species. If a previously shadowy forest is cut down or buildings are constructed in a previously sunny place, the microclimates of the egg clutches of any reptile nesting there will be changed.

Global change, or climate change, represents an additional threat to reptilians with TSD. The rise of the average temperature on the planet and the temperature fluctuation from one year to another, affect the number of males and females that are born in some species of reptiles. This phenomenon has been observed, for example, in painted turtles (Chrysemys picta), in which it has been predicted that a rise of 4^oC in their habitat’s temperature could cause the extinction of the species, because only females would be born.

Baby of a painted turtle (Chrysemys picta), species in which incubation temperatures between 23-27oC produce males, and temperatures above and below it produce females (pattern II). Foto de Cava Zachary.

REFERENCES

During the elaboration of this entry the following sources have been used:

• Cover photo: Animalspot.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://www.scientificamerican.com/article/experts-temperature-sex-determination-reptiles/
• http://www.ncbi.nlm.nih.gov/books/NBK9989/
• http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2603247/
• https://embryo.asu.edu/pages/temperature-dependent-sex-determination-reptiles
• http://onlinelibrary.wiley.com/doi/10.1002/jez.465/abstract
• http://link.springer.com/article/10.1007/s000180050342#page-2
• http://www.nbcnews.com/science/weird-science/hotter-temperatures-trigger-sex-change-australian-lizards-n385241
• http://www.herpconbio.org/Volume_5/Issue_2/Nelson_etal_2010.pdf