Synapsids: Before dinosaurs ruled the Earth

Before dinosaurs ruled the Earth, at the end of the Palaeozoic Era, the land was dominated by the synapsids. The synapsids (the amniote line that includes mammals) were a highly successful group which occupied most niches during the late Carboniferous and the Permian periods, but at the end of the Palaeozoic Era most families were extinguished by the Permian-Triassic mass extinction (around 252 million years ago) with only the mammalian line surviving to the present day. In this entry we’ll look at some of the more peculiar synapsid groups, which have led to the evolution of mammals like us.

CHARACTERISTICS AND EVOLUTIONARY TRENDS

The clade Synapsida includes mammals and all other amniotes more closely related to them than to reptiles. The synapsids were the first amniotes to diversify and appeared about 320 million years ago, at the middle of the Carboniferous period. These first synapsids were characterized by the presence of only one temporal fenestra behind each orbit through which the jaw muscles pass. Synapsida literally means “fused arches” referencing to the zygomatic arches (because in the past scientist believed that synapsids had evolved from diapsid reptiles and so their arches were thought to be “fused”).

Drawing of Archaeothyris’s skull, in which we can see some of the characteristics of the synapsids, like the temporal fenestrae and caniniform teeth. Drawing by Gretarsson.

Other characteristics that appeared through their evolution were:

• Differentiation of differently-shaped (heterodont) teeth.
• Lower jaw formed by fewer bones.
• Acquisition of a more erect posture and an endothermic metabolism.

The first groups of more primitive or “reptile-like” synapsids are informally called pelycosaurs, while the latter more advanced forms are called therapsids (clade Therapsida, which in fact derived from pelycosaurs). As we will see, the evolution of synapsids is of the kind of “one group, which includes the next group, which includes the next group”.

Modified evolutionary tree of the amniotes by Kenneth D. Angielczyk (2009).

THE ORIGIN OF SYNAPSIDS, THE PELYCOSAURS

Reconstruction of Cotylorhynchus, a caseasaurian that grew up to 3 metres long. Drawing by Dmitry Bogdanov.

The first synapsids had a sprawling limb posture, low slung bodies and were probably ectothermic. If we look at the skull morphology, the earliest groups of synapsids were the caseasaurians (clade Caseasauria) characterized by their small heads, an overdeveloped snout and their huge bodies (they were probably ectothermic and slow-moving creatures). Yet, if we look at the postcranial skeleton, the earliest synapsids were two groups called the varanopids and the ophiacodontids (Varanopidae and Ophiacodontidae families) which were similar to varanids (through convergent evolution), and while the former were quite small and agile creatures, the latter developed bigger forms with huge heads.

Drawings of the varanopid Varanodon (top) and the ophiacodontid Ophiacodon (bottom). Both drawings by Dmitry Bogdanov.

Just before the appearance of the more advanced therapsids, the last two groups of “pelycosaurs” evolved and occupied most land ecosystems. Both groups shared a tall sail along their backs (similarly to Spinosaurus) formed by tall neural spines. In life, this sail probably was covered in skin and had plenty of blood vessels. Although it’s believed that these two groups were still ectothermic, this sail was probably used to gain or lose heat more easily.

Reconstruction of different species of edaphosaurids of the genus Ianthasaurus, showing their characteristic sail. Drawing by Dmitry Bogdanov.

The first of these groups is the Edaphosauridae family. Unlike most basal synapsids, the edaphosaurids were herbivorous and, along with the caseasaurians, they were among the first large amniotes to adopt a vegetarian lifestyle. The sails of edaphosaurids were covered with spiny tubercles, of which their function is still debated.

Skeleton of Edaphosaurus from the Field Museum of Chicago, where the tubercles on its spines are shown. Image by Andrew Y. Huang (2011).

The other group, the Sphenacodontidae family, were the sister group of the therapsids, inside the clade Sphenacodontia. While all other pelycosaur clades had their teeth loosely set in the jaw, the sphenacodontians had their teeth set in deep sockets. Most sphenacodontids were carnivorous, with strong jaws and well-developed caniniform teeth. Some species became the top predators on land before the apparition of the therapsids.

Reconstruction of the sphenacodontid Dimetrodon, by Dmitry Bogdanov.

THE FIRST THERAPSIDS

Skeleton of Biarmosuchus, a basal therapsid in which we can see its more erect posture. Image by Ghedoghedo.

The therapsids (clade Therapsida, “beast arches”) appeared around 275 million years ago and replaced the pelycosaurs as the dominant land animals in the middle Permian. Early therapsids already had a more erect posture, unlike the sprawling limbs of the pelycosaurs. Also, their temporal fenestrae were larger, which made their jaws more powerful.

Reconstruction of Estemmenosuchus, a dinocephalian from which fossil skin imprints have been found and so it’s known that it was covered in smooth, glandular skin without scales. Drawing by Mojcaj.

The therapsids diversified greatly and developed some extraordinary adaptations. The dinocephalians (clade Dinocephalia, “terrible head”) developed bony head knobs which are believed to be involved in some kind of head-butting behaviour. Another group, the anomodonts (clade Anomodontia, “abnormal teeth”) were characterized by having no teeth except for a pair of upper canines (which were probably covered by a beak). The anomodonts were the sister group of theriodontians.

Reconstruction of Placerias, an anomodont which could weigh up to one tonne. Drawing by Dmitry Bogdanov.

THERIODONTIA AND THE FIRST SABER-TEETH

Theriodontians (clade Theriodontia “beast teeth”) became the most successful group of synapsids. The three main groups probably looked pretty mammal-like, with fully-erect posture, a secondary bony palate which allowed them to breathe while swallowing or holding a prey and heterodont teeth (incisiviform, caniniform and molariform teeth). The most primitive theriodontian group were the gorgonopsians (clade Gorgonopsia, Gorgonopsidae family). All members of this group were carnivorous and active predators, as revealed by their sabre-toothed teeth. Although most of them were of a modest size, the larger ones reached up to 3 metres long and had canines of up to 15 cm long.

Reconstruction of Inostrancevia, the largest gorgonopsid genus, preying upon Scutosaurus, a parareptilian. Drawing by Dmitry Bogdanov.

A second group, the therocephalians (clade Therocephalia, “beast head”), were pretty more advanced than the gorgonopsians, although they didn’t reach their cousins’ size. Their feet resembled those of early mammals, they presented small pits on their bones which probably supported whiskers on fleshy lips, and most evidence suggests that they were already endotherms.

Reconstruction of a pair of Pristerognathus, a therocephalian genus in which we can see some more mammalian characteristics. Drawing by Dmitry Bogdanov.

Both gorgonopsians and therocephalians disappeared at the end of the Permian. The only therapsid group that survived through the Mesozoic period and that coexisted with the dinosaurs were the cynodonts

SMALL CYNODONTS

The cynodonts (clade Cynodontia “dog teeth”) appeared at the late Permian and diversified greatly along with the archosaurs. Although it is not really proven, most paleoartists represent cynodonts covered in fur, as evidence suggests an endothermic metabolism. Some characteristics of the cynodonts were:

• Lower jaw formed only by the dentary bone, while the other jaw bones became the ossicles of the middle ear (the articular, the quadrate and the angular bones evolved into the malleus, the incus and the stapes).
• Complex teeth: incisors to hold, canines to pierce, and premolars and molars to chew.
• Only two sets of teeth (diphyodonts), instead of constantly-renewing teeth (polyphyodonts like most reptiles).
• Large brain cavities. Some fossil burrows of different cynodonts have been found, revealing complex social behaviours.

Reconstruction of Thrinaxodon, a burrowing cynodont with whiskers and hair. Image by Nobu Tamura.

Even if they competed with archosaurs, some early forms became quite large. For example, some carnivores, like Cynognathus, had a large head and measured 1 metre long, while Trucidocynodon was about the size of a leopard. Yet, the evolutionary trend would make the cynodonts smaller, like the Brasiliodontidae family which, like most cynodonts, lived in the shadow of dinosaurs and other bigger reptiles. Brasiliodontids are thought to be the sister group of the Mammaliaformes (mammals and their most recent relatives).

Reconstruction of Brasilitherium, one of the most advanced non-mammalian cynodonts, which was only 12 cm in length. Drawing by Smokeybjb.

Finally, mammals appeared at the end of the Triassic period around 225 million years ago. The first mammaliaforms were probably, insectivorous, nocturnal shrew-like animals. It is thought that this nocturnal lifestyle is what actually propelled the development of fur coats, because in therapsids endothermy appeared before fur did. These mammaliaforms probably had mammary glands to feed their young when they had no teeth, but they probably had no nipples like current monotremes.

Live reconstruction of Megazostrodon, a small mammaliaform which represents very well the transition from cynodonts to modern mammals. Image by Udo Schröter.

After the extinction of most archosaurs at the end of the Cretaceous period, the surviving synapsids took over the empty ecological niches. Mammals have ruled the world since then, conquering the land, the sea and even the air, but it wouldn’t have been possible without all the different adaptations acquired by early synapsids throughout their evolution. Thanks to them, humans and all other mammals are currently the dominant animals on the planet.

REFERENCES

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

• http://tolweb.org/accessory/Synapsid_Classification_&_Apomorphies?acc_id=466
• http://www.tandfonline.com/doi/full/10.1080/14772019.2011.631042
• http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0094518
• http://www.eurekalert.org/pub_releases/2015-10/sovp-ans102915.php
• http://www.tandfonline.com/doi/abs/10.1080/02724634.2011.627074
• http://dibgd.deviantart.com/gallery/
• Cover image by Mauricio Antón.

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/