Arxiu d'etiquetes: tortoise

Shell evolution with just four fossil turtles

Turtles are charming animals yet, while they look cute to most people, they’ve been racking the brains of palaeontologists for decades. The combination of apparently primitive features and an extremely specialized anatomy, has made the reconstruction of the origin and evolution of these reptiles a nearly impossible task. In this entry we’ll try to get a general idea about the evolution of one of the most striking characteristics of turtles (the shell) with only four examples of primitive “turtles”.

CURRENT AND EXTINCT RELATIVES

As we explained in an earlier entry, the origin of turtles is still debated among the scientific community. Turtles show some anatomic characteristics not found among any current vertebrate, which makes their phylogenetic origin confusing. One of the characteristics that has puzzled palaeontologist more is their skull.

caretta_carettazz-min
Skull of a loggerhead sea turtle (Caretta caretta) in which we can see the lack of temporal openings. Photo by David Stang.

While the rest of reptiles are diapsid (they present a pair of temporal openings at each side of the skull), turtles present a typically anapsid cranium (without any temporal openings). Yet, recent genomic studies have proved that it’s more likely that testudines (order Testudines, current turtles) descend from a diapsid ancestor and that through their evolution they reverted back to the primitive anapsid form. What is not so clear is if turtles are more closely related to lepidosaurs (lizards, snakes and tuataras) or to archosaurs (crocodiles and birds). The most accepted hypothesis is the second one.

Even if the origins of the testudines are still somewhat mysterious, most palaeontologists coincide in that they belong to the clade Pantestudines, which groups all those species more closely related to turtles than to any other animal. A group of reptiles that are also found inside the pantestudines are the sauropterygians like plesiosaurs and placodonts.

plesiosaurus_3db-min
Reconstruction by Dmitry Bogdanov of the sauropterygian Plesiosaurus, a distant relative of turtles.

EVOLUTION OF TESTUDINES

The rest of pantestudines help us to form an image of how turtles acquired such a specialized anatomy. But first, take a look at some of the characteristics of turtles:

  • A shell made up of two parts: the upper shell (carapace) which comes from the fusion of the vertebrae and the dorsal ribs and the lower shell (plastron) that originates from ventral ribs called “gastralia” (still present in some current reptiles).
  • While the rest of vertebrates present the scapula over their ribs, the turtle’s ribs (their carapace) cover the scapula.
  • The ability to hide their heads and limbs in their shells.
  • The absence of teeth; having instead horny ridges in their jaws.

As we’ll see, these characteristics were acquired very gradually.

8374089715_ed63b95c7d_o-min
The carapace of a dead turtle, in which we can see how the ribs fuse with the vertebrae to form the shell. Photo by Fritz Flohr Reynolds.

Even if their relationship with turtles isn’t still very clear, Eunotosaurus africanus is the most ancient candidate to being a turtle’s relative. Eunotosaurus was a fossorial animal that lived 260 million years ago in South Africa. This animal had very wide dorsal ribs which contacted each other, which is thought to have served as an anchoring point for powerful leg muscles, used while digging. Also, similarly to current turtles, Eunotosaurus had lost the intercostal muscles and presented a reorganization of the respiratory musculature.

eunotosaurus-min
Fossil of Eunotosaurus, in which the characteristically wide ribs can be seen. Photo by Flowcomm.

The oldest indisputable relative of turtles is Pappochelys rosiane from Germany (240 million years ago). The name “Pappochelys” literally means “grandfather turtle” as, before the discovery of Eunotosaurus it was the oldest turtle relative. Just like Eunotosaurus, it presented wide dorsal ribs in contact with each other. Also, its ventral ribs were already wider and thicker and its scapular girdle was placed below the dorsal ribs.

pappo_skelett
Drawing by Rainer Schoch of the skeleton of Pappochelys in which we can see some of its characteristics. It is believed that Pappochelys was a semiaquatic animal that swam with the aid of its long tail.

The next step in the evolution of turtles is found 220 million years ago, during the late Triassic in China. Its name is Odontochely semitestacea, which means “toothed turtle with half a shell”. This name is due to the fact that, unlike true turtles, Odontochelys still had a mouth full of teeth and it only presented the lower half of the shell, the plastron. Even if it also had thick dorsal ribs, only paleontological proofs of the plastron have been found. Odontochelys was discovered in freshwater deposits, leads us to believe that at first it only developed the plastron to protect itself from predators attacking from below.

odontochelys_bw-min
Reconstruction by Nobu Tamura of Odontochelys semitestacea. It’s not considered to be a true turtle due to the fact that it only had half a shell.

The first testudine known to possess a complete shell is Proganochelys quenstedti from the Triassic period, 210 million years ago. It already presented many characteristics found in current turtles: the shell was completely formed, with carapace and plastron, its skull was anapsid looking and it had no teeth. However, Proganochelys wasn’t able to retract its head and legs inside its shell (even if this may be because of the horns it had). It also presented two extra shell pieces at both sides, which probably served to protect its legs.

proganochelys_model-min
Reconstruction of Proganochelys from the Museum am Lowentor of Stuttgart. Photo by Ghedoghedo.

PRESENT DAY TURTLES

The order Testudines as we know it, appeared around 190 million years ago, during the Jurassic period. These current turtles are classified into two different suborders, which both separated quickly at the beginning of the evolution of testudines:

Suborder Pleurodira: This suborder is the smallest one as it only contains three current families, all native from the southern hemisphere. The main characteristic is the form in which they retract their neck laterally inside their shell, which leaves the neck exposed and makes the cervical vertebrae present a characteristic shape (Pleurodira roughly means “side neck”). Also, pleurodirans present 13 scutes in their plastrons.

chelodina_longicollis_1-min
Photo by Ian Sutton of an eastern long-necked turtle (Chelodina longicollis), a typical pleurodiran.

Suborder Cryptodira: Cryptodirans comprise most turtles. While pleurodirans only include freshwater species (as the testudines common ancestor is thought to be), criptodirans include freshwater terrapins, terrestrial tortoises and sea turtles. Apart from only presenting between 11 and 12 scutes in their plastrons, their principal characteristic is the ability to retract their neck and to hide their heads completely in their shell (Cryptodira roughly means “hidden neck”). Cryptodirans are found in practically all the continents and oceans (except in the coldest habitats).

alabama_red-bellied_turtle_us_fws_cropped-min
Photo of an Alabama red-bellied turtle (Pseudemys alabamensis) by the U.S. Fish and Wildlife Service. In this photo we can see how cryptodirans hide their heads.

Even if there still are some questions to be answered about the evolution of turtles, we hope that with this little introduction to some of the most characteristic fossil “turtles”, you have had an overall view about how turtles got their shells. Whatever their origins are, we hope that the apparition of men isn’t what puts an end to the history of this group of slow but steady creatures.

REFERENCES

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

difusio-angles

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:

512px-Crocodile_Egg_Diagram.svgDiagram 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.
512px-Amphibian_Egg_Diagram.svgDiagram 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.

Solenodonsaurus1DBReconstruction 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).
Skull_anapsida_1Diagram of an anapsid skull, by Preto(m).
  • Synapsids (“fused arches”): With only one temporal opening (mammals).
Skull_synapsida_1Diagram of a synapsid skull, by Preto(m).
  • Diapsids (“two arches”): With two temporal openings (reptiles, including birds).
Skull_diapsida_1Diagram 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.

Archaeothyris.svgDrawing 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…

Dimetrodon_grandisReconstruction 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).

Traditional_ReptiliaEvolutionary 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.

Rat_Snake_moulted_skinShed 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.
Sphenodon_punctatus_(5)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.
Sin títuloPhotos 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).

Massospondylus_Skull_Steveoc_86Drawing 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.

Yellow-billed_stork_kazingaPhoto 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)

KONICA MINOLTA DIGITAL CAMERASkeleton 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).

Leopard_tortoiseIndividual 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.
Figure_29_04_03Modified diagram about the evolutionary relationships of the different amniote groups.

REFERENCES

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

Difusió-anglès