Synapsida

Synapsida is a diverse group of tetrapod vertebrates that includes all mammals and their extinct relatives. It is one of the two major clades of the group Amniota, the other being the more diverse group Sauropsida (which includes all extant reptiles and birds). Synapsids have a single lower temporal fenestra, an opening low in the skull roof behind each eye socket. These openings create a bony arch that allows for the attachment of larger jaw muscles and a more efficient bite. While previously argued to be distinctive to synapsids, single temporal fenestrae are also found in many primitive sauropsids. It has recently been argued that the last common ancestor of synapsids and sauropsids shared a single lower temporal fenestra.

The basal amniotes (reptiliomorphs) from which synapsids evolved were historically simply called "reptiles". Therefore, stem group synapsids were then described as mammal-like reptiles in classical systematics, and non-therapsid synapsids were also referred to as pelycosaurs or pelycosaur-grade synapsids. These paraphyletic terms have fallen out of favor and are only used informally (if at all) in modern literature, as it is now known that all extant reptiles are more closely related to each other and birds than to synapsids, so the word "reptile" has been re-defined to mean only members of Sauropsida or even just an under-clade thereof. In a cladistic sense, synapsids are in fact a monophyletic sister taxon of sauropsids, rather than a part of the sauropsid lineage. Therefore, calling synapsids "mammal-like reptiles" is incorrect under the new definition of "reptile", so they are now referred to as stem mammals, proto-mammals, paramammals or pan-mammals. but declined again after the Smithian–Spathian boundary event with their dominant niches largely taken over by the rise of archosaurian sauropsids, first by the pseudosuchians and then by the pterosaurs and dinosaurs. The cynodont group Probainognathia, which includes the group Mammaliaformes, were the only synapsids to survive beyond the Triassic, During the Jurassic, cynodonts lived mostly nocturnally to avoid competition with dinosaurs. After the Cretaceous–Paleogene extinction event wiped out all non-avian dinosaurs and pterosaurs, synapsids (as mammals) rose to dominance once again during the Cenozoic, with roughly 6,800 species living currently.

Linnaean and cladistic classifications

At the turn of the 20th century, synapsids were thought to be one of the four main subclasses of reptiles. However, this notion was disproved upon closer inspection of skeletal remains, as synapsids are differentiated from reptiles by their distinctive temporal openings. These openings in the skull bones allowed the attachment of larger jaw muscles, hence a more efficient bite.

Synapsids were subsequently considered to be a later reptilian lineage that became mammals by gradually evolving increasingly mammalian features, hence the name "mammal-like reptiles" (also known as pelycosaurs). These became the traditional terms for all Paleozoic (early) synapsids. More recent studies have debunked this notion as well, and reptiles are now classified within Sauropsida (sauropsids), the sister group to synapsids, thus making synapsids their own taxonomic group. The monophyly of Synapsida is not in doubt, and the expressions such as "Synapsida contains the mammals" and "synapsids gave rise to the mammals" both express the same phylogenetic hypothesis. This terminology reflects the modern cladistic approach to animal relationships, according to which the only valid groups are those that include all of the descendants of a common ancestor: these are known as monophyletic groups, or clades.

Additionally, Reptilia (reptiles) has been revised into a monophyletic group and is considered entirely distinct from Synapsida, falling within Sauropsida, the sister group of Synapsida within Amniota.

Primitive and advanced synapsids

The synapsids are traditionally divided for convenience, into therapsids, an advanced group of synapsids and the branch within which mammals evolved, and stem mammals, (previously known as pelycosaurs), comprising the other six more primitive families of synapsids. Stem mammals were all rather lizard-like, with sprawling gait and possibly horny scutes, while therapsids tended to have a more erect pose and possibly hair, at least in some forms. In traditional taxonomy, the Synapsida encompasses two distinct grades: the low-slung stem mammals have given rise to the more erect therapsids, who in their turn have given rise to the mammals. In traditional vertebrate classification, the stem mammals and therapsids were both considered orders of the subclass Synapsida.

Teeth

thumb|200px|right|[[Eothyris, an early synapsid with multiple canines]]

Synapsids are characterized by having differentiated teeth. These include the canines, molars, and incisors. The trend towards differentiation is found in some labyrinthodonts and early anapsid reptilians in the form of enlargement of the first teeth on the maxilla, forming a sort of protocanines. This trait was subsequently lost in the diapsid line, but developed further in the synapsids. Early synapsids could have two or even three enlarged "canines", but in the therapsids, the pattern had settled to one canine in each upper jaw half. The lower canines developed later.

Jaw

The jaw transition is a good classification tool, as most other fossilized features that make a chronological progression from a reptile-like to a mammalian condition follow the progression of the jaw transition. The mandible, or lower jaw, consists of a single, tooth-bearing bone in mammals (the dentary), whereas the lower jaw of modern and prehistoric reptiles consists of a conglomeration of smaller bones (including the dentary, articular, angular, surangular and others). In the evolutionary line of mammals these jaw bones other than the dentary were reduced in size and either lost or, in the case of the articular, gradually moved into the ear, forming one of the middle ear bones: while modern mammals possess the malleus, incus and stapes, basal synapsids (like all other tetrapods) possess only a stapes. The malleus is derived from the articular (a lower jaw bone), while the incus is derived from the quadrate (a cranial bone).

Mammalian jaw structures are also set apart by the dentary-squamosal jaw joint. In this form of jaw joint, the dentary forms a connection with a depression in the squamosal known as the glenoid cavity. In contrast, all other jawed vertebrates, including reptiles and nonmammalian synapsids, possess a jaw joint in which one of the smaller bones of the lower jaw, the articular, makes a connection with a bone of the cranium called the quadrate bone to form the articular-quadrate jaw joint. In forms transitional to mammals, the jaw joint is composed of a large, lower jaw bone (similar to the dentary found in mammals) that does not connect to the squamosal, but connects to the quadrate with a receding articular bone.

Palate

Synapsids ancestrally possess palatal teeth present on the bones of the roof of the mouth. These were lost in the cynodont ancestors of mammals.

Over time, as synapsids became more mammalian and less 'reptilian', they began to develop a secondary palate, separating the mouth and nasal cavity. In early synapsids, a secondary palate began to form on the sides of the maxilla, still leaving the mouth and nostril connected.

Eventually, the two sides of the palate began to curve together, forming a U shape instead of a C shape. The palate also began to extend back toward the throat, securing the entire mouth and creating a full palatine bone. The maxilla is also closed completely. In fossils of one of the first eutheriodonts, the beginnings of a palate are clearly visible. The later Thrinaxodon has a full and completely closed palate, forming a clear progression.

Skin and fur

thumb|The [[sea otter has the densest fur of modern mammals.]]

In addition to the glandular skin covered in fur found in most modern mammals, modern and extinct synapsids possess a variety of modified skin coverings, including osteoderms (bony armor embedded in the skin), scutes (protective structures of the dermis often with a horny covering), hair or fur, and scale-like structures (often formed from modified hair, as in pangolins and some rodents). While the skin of reptiles is rather thin, that of mammals has a thick dermal layer.

Although the nature of early synapsid skin was previously subject of ambiguity, it has now been conclusively shown that early "pelycosaur" synapsids were covered in epidermal scales similar to those of reptiles (with the bodies of at least some sphenacodontids having rectangular scales on the underside of the body while their limbs were covered in hexagonal scales). It has been suggested that epidermal scales evolved in their common ancestor prior to the split between reptiles and synapsids.

It is currently unknown exactly when mammalian characteristics such as body hair and mammary glands first appeared, as the fossils only rarely provide direct evidence for soft tissues. The only unambiguous skin impressions known from non-cynodont therapsids are those of the dinocephalian Estemmenosuchus from the Middle Permian of Russia and the dicynodont Lystrosaurus from the Early Triassic of South Africa, which both exhibit "bulging ellipsoid tubercules with a tendency to partially protrude one another, producing an overall pustular surface texture". Hair-like structures in Late Permian coprolites from Russia and possibly South Africa may suggest that some therapsids had possibly acquired hair by this time, though the nature of these structures is ambiguous. The oldest known fossil showing unambiguous imprints of hair is the Callovian (late middle Jurassic) Castorocauda and several contemporary haramiyidans, both non-mammalian mammaliaform (see below, however). More primitive members of the Cynodontia are also hypothesized to have had fur or a fur-like covering based on their inferred warm-blooded metabolism. Mutation of the MSX2 gene in mice shows that when the gene is made non-functional, the mice fail to develop a hair coat, and the pineal foramen, which is ancestrally closed in mammals, becomes open. This may suggest that the two developments occurred around the same time in the cynodont ancestors of mammals.

Within true mammals, aerial locomotion first occurs in volaticotherian eutriconodonts. A fossil Volaticotherium has an exquisitely preserved furry patagium with delicate wrinkles and that is very extensive, "sandwiching" the poorly preserved hands and feet and extending to the base of the tail. Argentoconodon, a close relative, shares a similar femur adapted for flight stresses, indicating a similar lifestyle.

Therian mammals would only achieve powered flight and gliding long after these early aeronauts became extinct, with the earliest-known gliding metatherians and bats evolving in the Paleocene.

Reproduction and mammary glands

thumb|Preserved embryo of [[dicynodont therapsid Lystrosaurus from the Early Triassic of South Africa, with life restoration showing embryo curled up in inferred (but unpreserved) egg]]

Most or all non-mammalian synapsids may have laid relatively soft leathery eggs similar to those of monotremes, which lack a relatively thick hard calcified shell like those found in many modern reptile and bird eggs. Egg laying in non-mammalian synapsids has seemingly been confirmed by a tightly coiled embryo of the dicynodont therapsid Lystrosaurus found in the Early Triassic of South Africa which was likely laid in an (unpreserved) soft leathery egg. Because they were vulnerable to desiccation, secretions from apocrine-like glands may have helped keep the eggs moist.), though this would limit the mobility of the parent. The latter may have been the primitive form of egg care in synapsids rather than simply burying the eggs, and the constraint on the parent's mobility would have been solved by having the eggs "parked" in nests during foraging or other activities and periodically be hydrated, allowing higher clutch sizes than could fit inside a pouch (or pouches) at once, and large eggs, which would be cumbersome to carry in a pouch, would be easier to care for. The basis of Oftedal's speculation is the fact that many species of anurans can carry eggs or tadpoles attached to the skin, or embedded within cutaneous "pouches" and how most salamanders curl around their eggs to keep them moist, both groups also having glandular skin.

Metabolism and activity cycle

It has been disputed when endothermy arose in the synapsid lineage. Some propose that it arose in the common ancestor of synapsids, others that endothermy is only present in members of Therapsida (perhaps with separate origins in dicynodonts and cynodonts), and that synapsids are ancestrally ectothermic like reptiles.

Based on the size of the eye sockets and the scleral ring, some non-mammalian synapsids were likely diurnal (active during the day), while others are likely to have been nocturnal.

Evolutionary history

thumb|left|[[Archaeothyris, one of the oldest synapsids found]]

thumb|left|[[Cotylorhynchus (background), Ophiacodon and Varanops were early synapsids that lived until the Early Permian.]]

Over the course of synapsid evolution, progenitor taxa at the start of adaptive radiations have tended to be derived carnivores. Synapsid adaptive radiations have generally occurred after extinction events that depleted the biosphere and left vacant niches open to be filled by newly evolved taxa. In non-mammaliaform synapsids, those taxa that gave rise to rapidly diversifying lineages have been both small and large in body size, although after the Late Triassic, progenitors of new synapsid lineages have generally been small, unspecialised generalists.

The earliest known synapsid Asaphestera coexisted with the earliest known sauropsid Hylonomus which lived during the Bashkirian age of the Late Carboniferous. It was one of many types of primitive synapsids that are now informally grouped together as stem mammals or sometimes as protomammals (previously known as pelycosaurs). The early synapsids spread and diversified, becoming dominant land predators and the largest terrestrial animals in the latest Carboniferous and Early Permian periods, ranging up to in length. They were sprawling, bulky, possibly cold-blooded, and had small brains. Some, such as Dimetrodon, had large sails that might have helped raise their body temperature. A few relict groups lasted into the later Permian but, by the middle of the Late Permian, all had either died off or evolved into their successors, the therapsids.

thumb|right|[[Moschops is a herbivorous dinocephalian therapsid from the Middle Permian of South Africa.]]

The therapsids, a more advanced group of synapsids, appeared during the Middle Permian and included the largest terrestrial animals in the Middle and Late Permian. They included herbivores and carnivores, ranging from small animals the size of a rat (e.g.: Robertia), to large, bulky herbivores a ton or more in weight (e.g.: Moschops). After flourishing for many millions of years, these successful animals were all but wiped out by the Permian–Triassic mass extinction about 250 mya, the largest known extinction in Earth's history, possibly related to the Siberian Traps volcanic event.

thumb|left|[[Nikkasaurus was an enigmatic synapsid from the Middle Permian of Russia.]]

thumb|right|[[Lystrosaurus was the most common synapsid shortly after the Permian–Triassic extinction event.]]

Only a few therapsids went on to be successful in the new early Triassic landscape; they include Lystrosaurus and Cynognathus, the latter of which appeared later in the Early Triassic. However, they were accompanied by the early archosaurs (soon to give rise to the dinosaurs), which took over the dominant niches after the Smithian-Spathian boundary event. Some of these archosaurs, such as Euparkeria, were small and lightly built, while others, such as Erythrosuchus, were as big as or bigger than the largest therapsids.

After the Permian extinction, the synapsids did not count more than three surviving clades. The first comprised the therocephalians, which only lasted the first 20 million years of the Triassic period. The second were specialised, beaked herbivores known as dicynodonts (such as the Kannemeyeriidae), which contained some members that reached large size (up to a tonne or more). And finally there were the increasingly mammal-like carnivorous, herbivorous, and insectivorous cynodonts, including the eucynodonts from the Olenekian age, an early representative of which was Cynognathus.

thumb|[[Cynognathus was the largest predatory cynodont of the Triassic.]]

Unlike the dicynodonts, which were large, the cynodonts became progressively smaller and more mammal-like as the Triassic progressed, though some forms like Trucidocynodon remained large. The first mammaliaforms evolved from the cynodonts during the early Norian age of the Late Triassic, about 225 mya.

During the evolutionary succession from early therapsid to cynodont to eucynodont to mammal, the main lower jaw bone, the dentary, replaced the adjacent bones. Thus, the lower jaw gradually became just one large bone, with several of the smaller jaw bones migrating into the inner ear and allowing sophisticated hearing.

Triassic and Jurassic ancestors of living mammals, along with their close relatives, had high metabolic rates. This meant consuming food (generally thought to be insects) in much greater quantity. To facilitate rapid digestion, these synapsids evolved mastication (chewing) and specialized teeth that aided chewing. Limbs also evolved to move under the body instead of to the side, allowing them to breathe more efficiently during locomotion. This helped make it possible to support their higher metabolic demands.

thumb|right|[[Repenomamus was the largest mammal of the Mesozoic.]]

Whether through climate change, vegetation change, ecological competition, or a combination of factors, most of the remaining large cynodonts (belonging to the Traversodontidae) and dicynodonts (of the family Kannemeyeriidae) had disappeared by the Rhaetian age, even before the Triassic–Jurassic extinction event that killed off most of the large non-dinosaurian archosaurs. The remaining Mesozoic synapsids were small, ranging from the size of a shrew to the badger-like mammal Repenomamus.

thumb|left|[[Tritylodon was a cynodont that lived in the Early Jurassic.]]

During the Jurassic and Cretaceous, the remaining non-mammalian cynodonts were small, such as Tritylodon. No cynodont grew larger than a cat. Most Jurassic and Cretaceous cynodonts were herbivorous, though some were carnivorous. The family Tritheledontidae, which first appeared near the end of the Triassic, was carnivorous and persisted well into the Middle Jurassic. The other, Tritylodontidae, first appeared at the same time as the tritheledonts, but was herbivorous. This group became extinct at the end of the Early Cretaceous epoch. Dicynodonts are generally thought to have become extinct near the end of the Triassic period, but there was evidence this group survived, in the form of six fragments of fossil bone that were found in Cretaceous rocks of Queensland, Australia. If true, it would mean there is a significant ghost lineage of Dicynodonts in Gondwana. However, these fossils were re-described in 2019 as being Pleistocene in age, and possibly belonging to a diprotodontid marsupial.

Today, the 5,500 species of living synapsids, known as the mammals, include both aquatic (cetaceans) and flying (bats) species, and the largest animal ever known to have existed (the blue whale). Humans are synapsids, as well. Most mammals are viviparous and give birth to live young rather than laying eggs with the exception being the monotremes.

Some examples of modern mammals:

<gallery>

File:Duck-billed platypus (Ornithorhynchus anatinus) Scottsdale.jpg|Platypus

File:Red kangaroo - melbourne zoo.jpg|Male red kangaroo

File:Elephas maximus (Bandipur).jpg|Asian elephant

File:Manuring a vegetable garden.jpg|Human

File:A Friesian Bull, Llandeilo Graban - geograph.org.uk - 579885.jpg|Cattle

File:Canis lupus 265b.jpg|Wolf

File:Anim1754 - Flickr - NOAA Photo Library.jpg|Blue whale

File:Pteropus giganteus fg01.JPG|Indian flying fox

File:Armadillo2.jpg|Nine-banded armadillo

File:Hydrochoeris hydrochaeris in Brazil in Petrópolis, Rio de Janeiro, Brazil 09.jpg|Capybara

</gallery>

Relationships

Below is a cladogram of the most commonly accepted phylogeny of synapsids, showing a long stem lineage including Mammalia and successively more basal clades such as Theriodontia, Therapsida and Sphenacodontia:

Most uncertainty in the phylogeny of synapsids lies among the earliest members of the group, including forms traditionally placed within Pelycosauria. As one of the earliest phylogenetic analyses, Brinkman & Eberth (1983) placed the family Varanopidae with Caseasauria as the most basal offshoot of the synapsid lineage. Reisz (1986) removed Varanopidae from Caseasauria, placing it in a more derived position on the stem. While most analyses find Caseasauria to be the most basal synapsid clade, Benson's analysis (2012) placed a clade containing Ophiacodontidae and Varanopidae as the most basal synapsids, with Caseasauria occupying a more derived position. Benson attributed this revised phylogeny to the inclusion of postcranial characteristics, or features of the skeleton other than the skull, in his analysis. When only cranial or skull features were included, Caseasauria remained the most basal synapsid clade. Below is a cladogram modified from Benson's analysis (2012):

However, more recent examination of the phylogeny of basal synapsids, incorporating newly described basal caseids and eothyridids, returned Caseasauria to its position as the sister to all other synapsids. Brocklehurst et al. (2016)