Synapsida[a] is a diverse group oftetrapodvertebrates that includes allmammals and their extinct relatives. It is one of the two majorclades of the groupAmniota, the other being the more diverse groupSauropsida (which includes all extantreptiles andbirds). Unlike other amniotes, synapsids have a singletemporal fenestra, an opening low in theskull roof behind eacheye socket, leaving abony arch beneath each; this accounts for the name "synapsid".[7] The distinctive temporal fenestra developed about 318 million years ago during theLate Carboniferous period,[1] when synapsids and sauropsids diverged, but was subsequently merged with the orbit in early mammals.
Thebasal amniotes (reptiliomorphs) from which synapsids evolved were historically simply called "reptiles". Therefore,stem group synapsids were then described asmammal-like reptiles in classical systematics, and non-therapsid synapsids were also referred to aspelycosaurs orpelycosaur-grade synapsids. Theseparaphyletic terms have now fallen out of favor and are only used informally (if at all) in modern literature, as it is now known that allextant 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 acladistic sense, synapsids are in fact amonophyleticsister taxon of sauropsids, rather than a part of the sauropsid lineage.[8][9][10][11] Therefore, calling synapsids "mammal-like reptiles" is incorrect under thenew definition of "reptile", so they are now referred to asstem mammals,proto-mammals,paramammals orpan-mammals.[12][13][14] Most lineages of pelycosaur-grade synapsids were replaced by the more advanced therapsids, which evolved fromsphenacodontoid pelycosaurs, at the end of the Early Permian during the so-calledOlson's Extinction.
At the turn of the 20th century, synapsids were thought to be one of the four main subclasses ofreptiles. 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 theskull 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 graduallyevolving increasingly mammalian features, hence the name "mammal-like reptiles" (also known aspelycosaurs). These became the traditional terms for allPaleozoic (early) synapsids. More recent studies have debunked this notion as well, and reptiles are now classified withinSauropsida (sauropsids), the sister group to synapsids, thus making synapsids their owntaxonomic group.[8][10]
As a result, theparaphyletic terms "mammal-like reptile" and "pelycosaur" are seen as outdated and disfavored in technical literature, and the termstem mammal (or sometimesprotomammal orparamammal) is used instead.Phylogenetically, it is now understood that synapsids comprise an independent branch of thetree of life.[19] Themonophyly 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 moderncladistic 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 asmonophyletic groups, orclades.
Additionally,Reptilia (reptiles) has been revised into a monophyletic group and is considered entirely distinct from Synapsida, falling withinSauropsida, the sister group of Synapsida within Amniota.[20]
The synapsids are traditionally divided for convenience, intotherapsids, an advanced group of synapsids and the branch within which mammals evolved, and stem mammals, (previously known aspelycosaurs), comprising the other six more primitive families of synapsids.[21] Stem mammals were all rather lizard-like, with sprawling gait and possibly hornyscutes, while therapsids tended to have a more erect pose and possibly hair, at least in some forms. In traditional taxonomy, the Synapsida encompasses two distinctgrades: 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 consideredorders of the subclass Synapsida.[7][8]
Practical versus phylogenetic usage of "synapsid" and "therapsid"
Inphylogenetic nomenclature, the terms are used somewhat differently, as the daughter clades are included. Most papers published during the 21st century have treated "Pelycosaur" as an informal grouping of primitive members. Therapsida has remained in use as a clade containing both the traditional therapsid families and mammals.
Although Synapsida and Therapsida include modern mammals, in practical usage, those two terms are used almost exclusively when referring to the morebasal members that lie outside ofMammaliaformes.
The synapsids are distinguished by a single hole, known as thetemporal fenestra, in the skull behind each eye. This schematic shows the skull viewed from the left side. The middle opening is the orbit of the eye; the opening to the right of it is the temporal fenestra.
Synapsids evolved atemporal fenestra behind each eyeorbit on the lateral surface of the skull. It may have provided new attachment sites for jaw muscles. A similar development took place in thediapsids, which evolved two rather than one opening behind each eye. Originally, the openings in the skull left the inner cranium covered only by the jaw muscles, but in higher therapsids and mammals, thesphenoid bone has expanded to close the opening. This has left the lower margin of the opening as an arch extending from the lower edges of the braincase.
Synapsids are characterized by having differentiated teeth. These include thecanines,molars, andincisors.[22] The trend towards differentiation is found in somelabyrinthodonts and earlyanapsid reptilians in the form of enlargement of the first teeth on themaxilla, forming a sort of protocanines. This trait was subsequently lost in thediapsid 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.
The jaw transition is a goodclassification 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. Themandible, 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, and others). As they evolved in synapsids, these jaw bones 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 themalleus,incus andstapes,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 thequadrate (a cranial bone).[23]
Mammalian jaw structures are also set apart by the dentary-squamosaljaw joint. In this form of jaw joint, the dentary forms a connection with a depression in thesquamosal known as theglenoid 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 thecranium called thequadrate 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.
Over time, as synapsids became more mammalian and less 'reptilian', they began to develop asecondary palate, separating the mouth andnasal cavity. In early synapsids, a secondary palate began to form on the sides of themaxilla, 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 fullpalatine bone. The maxilla is also closed completely. In fossils of one of the firsteutheriodonts, the beginnings of a palate are clearly visible. The laterThrinaxodon has a full and completely closed palate, forming a clear progression.[24]
Thesea 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, includingosteoderms (bony armor embedded in the skin),scutes (protective structures of the dermis often with a horny covering), hair or fur, andscale-like structures (often formed from modified hair, as inpangolins and somerodents). While the skin of reptiles is rather thin, that of mammals has a thickdermal layer.[25]
The ancestral skin type of synapsids has been subject to discussion. The type specimen of the oldest known synapsidAsaphestera preservedscales.[26] Among the early synapsids, only two species of smallvaranopids have been found to possessosteoderms;[27] fossilized rows ofosteoderms indicate bony armour on the neck and back. However, some recent studies have cast doubt on the placement of Varanopidae in Synapsida,[28][29] while others have countered and lean towards this traditional placement.[30][31] Skin impressions indicate some early synapsids basal possessed rectangular scutes on their undersides and tails.[32][33] The pelycosaur scutes probably were nonoverlappingdermal structures with a horny overlay, like those found in moderncrocodiles andturtles. These differed in structure from thescales of lizards and snakes, which are an epidermal feature (like mammalian hair or avian feathers).[34] Recently, skin impressions from the genusAscendonanus suggest that at least varanopsids developed scales similar to those ofsquamates.[35]
It is currently unknown exactly when mammalian characteristics such asbody hair andmammary glands first appeared, as the fossils only rarely provide direct evidence for soft tissues. An exceptionally well-preserved skull ofEstemmenosuchus, a therapsid from the Upper Permian, preserves smooth skin with what appear to be glandular depressions,[36] an animal noted as being semi-aquatic.[37] The oldest known fossil showing unambiguous imprints of hair is theCallovian (late middleJurassic)Castorocauda and several contemporaryharamiyidans, both non-mammalianmammaliaform[38][39] (see below, however). More primitive members of theCynodontia are also hypothesized to have had fur or a fur-like covering based on their inferred warm-blooded metabolism.[40] While more direct evidence of fur in early cynodonts has been proposed in the form of small pits on the snout possibly associated withwhiskers, such pits are also found in some reptiles that lack whiskers.[40] There is evidence that some other non-mammalian cynodonts more basal thanCastorocauda, such asMorganucodon, hadHarderian glands, which are associated with the grooming and maintenance of fur. The apparent absence of these glands in non-mammaliaformes may suggest that fur did not originate until that point in synapsid evolution.[40] It is possible that fur and associated features of true warm-bloodedness did not appear until some synapsids became extremely small and nocturnal, necessitating a higher metabolism.[40] The oldest examples of nocturnality in synapsids is believed to have been in species that lived more than 300 million years ago.[41]
However,Late Permiancoprolites from Russia and possibly South Africa showcase that at least some synapsids did already have pre-mammalian hair in this epoch. These are the oldest impressions of hair-like structures on synapsids.[42][43]
Early synapsids, as far back as their known evolutionary debut in the Late Carboniferous period,[44] may have laid parchment-shelled (leathery) eggs,[45] which lacked a calcified layer, as most modern reptiles andmonotremes do. This may also explain why there is no fossil evidence for synapsid eggs to date.[46] Because they were vulnerable to desiccation, secretions fromapocrine-like glands may have helped keep the eggs moist.[44]
According to Oftedal, early synapsids may have buried the eggs into moisture laden soil, hydrating them with contact with the moist skin, or may have carried them in a moist pouch, similar to that of monotremes (echidnas carry their eggs and offspring via a temporary pouch[47][48]), 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 ofanurans can carry eggs or tadpoles attached to the skin, or embedded within cutaneous "pouches" and how mostsalamanders curl around their eggs to keep them moist, both groups also having glandular skin.[46]
The glands involved in this mechanism would later evolve into true mammary glands with multiple modes of secretion in association with hair follicles. Comparative analyses of the evolutionary origin of milk constituents support a scenario in which the secretions from these glands evolved into a complex, nutrient-rich milk long before true mammals arose (with some of the constituents possibly predating the split between the synapsid andsauropsid lines).Cynodonts were almost certainly able to produce this, which allowed a progressive decline of yolk mass and thus egg size, resulting in increasinglyaltricial hatchlings as milk became the primary source of nutrition, which is all evidenced by the small body size, the presence ofepipubic bones, and limited tooth replacement in advanced cynodonts, as well as inmammaliaforms.[44][45]
Aerial locomotion first began in non-mammalianharamiyidan cynodonts, withArboroharamiya,Xianshou,Maiopatagium andVilevolodon bearing exquisitely preserved, fur-covered wing membranes that stretch across the limbs and tail. Their fingers are elongated, similar to those of bats andcolugos and likely sharing similar roles both as wing supports and to hang on tree branches.[49]
Within true mammals, aerial locomotion first occurs involaticotherianeutriconodonts. A fossilVolaticotherium has an exquisitely preserved furrypatagium with delicate wrinkles and that is very extensive, "sandwiching" the poorly preserved hands and feet and extending to the base of the tail.[50]Argentoconodon, a close relative, shares a similar femur adapted for flight stresses, indicating a similar lifestyle.[51]
Therian mammals would only achieve powered flight and gliding long after these early aeronauts became extinct, with the earliest-known glidingmetatherians andbats evolving in thePaleocene.[52]
Recently, it has been found thatendothermy was developed as early asOphiacodon in the late Carboniferous. The presence of fibrolamellar, a specialised type of bone that can grow quickly while maintaining a stable structure, shows that Ophiacodon would have used its high internal body temperature to fuel a fast growth comparable to modern endotherms.[53]
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.[54]
The earliest known synapsidAsaphestera coexisted with the earliest known sauropsidHylonomus which lived during theBashkirian age of theLate Carboniferous.[26][14] It was one of many types of primitive synapsids that are now informally grouped together as stem mammals or sometimes as protomammals (previously known aspelycosaurs). The early synapsids spread and diversified, becoming the largest terrestrial animals in the latest Carboniferous andEarly Permian periods, ranging up to 6 metres (20 ft) in length. They were sprawling, bulky, possibly cold-blooded, and had small brains. Some, such asDimetrodon, had large sails that might have helpedraise their body temperature. A fewrelict 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.[55]
The therapsids, a more advanced group of synapsids, appeared during theMiddle Permian and included the largest terrestrial animals in the Middle andLate 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 thePermian–Triassic mass extinction about 250 mya, the largest knownextinction inEarth's history, possibly related to theSiberian Traps volcanic event.
Only a few therapsids went on to be successful in the new earlyTriassic landscape; they includeLystrosaurus andCynognathus, the latter of which appeared later in the Early Triassic. However, they were accompanied by the earlyarchosaurs (soon to give rise to thedinosaurs). Some of these archosaurs, such asEuparkeria, were small and lightly built, while others, such asErythrosuchus, 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 thetherocephalians, which only lasted the first 20 million years of the Triassic period. The second were specialised, beaked herbivores known asdicynodonts (such as theKannemeyeriidae), 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 theeucynodonts from theOlenekian age, an early representative of which wasCynognathus.
Unlike the dicynodonts, which were large, the cynodonts became progressively smaller and more mammal-like as the Triassic progressed, though some forms likeTrucidocynodon remained large. The first mammaliaforms evolved from the cynodonts during the earlyNorian 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 theinner ear and allowing sophisticated hearing.
Whether through climate change, vegetation change, ecological competition, or a combination of factors, most of the remaining large cynodonts (belonging to theTraversodontidae) and dicynodonts (of the family Kannemeyeriidae) had disappeared by theRhaetian age, even before theTriassic–Jurassic extinction event that killed off most of the largenon-dinosaurian archosaurs. The remaining Mesozoic synapsids were small, ranging from the size of a shrew to the badger-like mammalRepenomamus.
During the Jurassic and Cretaceous, the remaining non-mammalian cynodonts were small, such asTritylodon. No cynodont grew larger than a cat. Most Jurassic and Cretaceous cynodonts wereherbivorous, though some werecarnivorous. The familyTritheledontidae, which first appeared near the end of the Triassic, was carnivorous and persisted well into theMiddle 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 ofQueensland, Australia.[56] If true, it would mean there is a significantghost lineage of Dicynodonts inGondwana. However, these fossils were re-described in 2019 as beingPleistocene in age, and possibly belonging to adiprotodontidmarsupial.[57]
Today, the 5,500 species of living synapsids, known as themammals, include both aquatic (cetaceans) and flying (bats) species, and the largest animal ever known to have existed (theblue whale). Humans are synapsids, as well. Most mammals areviviparous and give birth to live young rather than laying eggs with the exception being themonotremes.
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 rapiddigestion, these synapsids evolvedmastication (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.[58] This helped make it possible to support their higher metabolic demands.
Below is acladogram of the most commonly acceptedphylogeny of synapsids, showing a long stem lineage including Mammalia and successively more basal clades such as Theriodontia, Therapsida and Sphenacodontia:[59][60]
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 familyVaranopidae withCaseasauria 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 containingOphiacodontidae 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 acladogram modified from Benson's analysis (2012):[61]
However, more recent examination of the phylogeny of basal synapsids, incorporating newly described basal caseids and eothyridids,[62] returned Caseasauria to its position as the sister to all other synapsids. Brocklehurst et al. (2016)[62] demonstrated that many of the postcranial characters used by Benson (2012) to unite Caseasauria withSphenacodontidae andEdaphosauridae were absent in the newly discovered postcranial material of eothyridids, and were therefore acquired convergently.
^abSteen, Margaret C. (1934). "The amphibian fauna from the South Joggins. Nova Scotia".Journal of Zoology.104 (3):465–504.doi:10.1111/j.1096-3642.1934.tb01644.x.
^Angielczch, Kennenth; Kammerer, Christian F.; Frobisch, Jorg. (2013).Early Evolutionary History of Synapsida. Springer Science & Business Media.ISBN978-94-007-6841-3, p. 11
^Hopson, James A. (1987). "The Mammal-Like Reptiles: A Study of Transitional Fossils".The American Biology Teacher.49 (1):16–26.doi:10.2307/4448410.JSTOR4448410.
^Hildebran, M.; Goslow, G. (2001).Analysis of Vertebrate Structure (5th ed.). New York: John Wiley & Sons.ISBN0-471-29505-1.
^abMann, Arjan; Gee, Bryan M.; Pardo, Jason D.; Marjanović, David; Adams, Gabrielle R.; Calthorpe, Ami S.; Maddin, Hillary C.; Anderson, Jason S. (5 May 2020). Sansom, Robert (ed.). "Reassessment of historic 'microsaurs' from Joggins, Nova Scotia, reveals hidden diversity in the earliest amniote ecosystem".Papers in Palaeontology.6 (4). Wiley:605–625.Bibcode:2020PPal....6..605M.doi:10.1002/spp2.1316.ISSN2056-2802.
^Spindler, Frederik; Werneburg, Ralf; Schneider, Joerg W.; Luthardt, Ludwig; Annacker, Volker; Rößler, Ronny (2018). "First arboreal 'pelycosaurs' (Synapsida: Varanopidae) from the early Permian Chemnitz Fossil Lagerstätte, SE Germany, with a review of varanopid phylogeny".PalZ.92 (2):315–364.Bibcode:2018PalZ...92..315S.doi:10.1007/s12542-018-0405-9.S2CID133846070.
^Bajdek, Piotr; Qvarnström, Martin; Owocki, Krzysztof; Sulej, Tomasz; Sennikov, Andrey G.; Golubev, Valeriy K.; Niedźwiedzki, Grzegorz (2016). "Microbiota and food residues including possible evidence of pre-mammalian hair in Upper Permian coprolites from Russia".Lethaia.49 (4):455–477.Bibcode:2016Letha..49..455B.doi:10.1111/let.12156.
^Luo, Zhe-Xi; Meng, Qing-Jin; Grossnickle, David M.; Di, Liu; Neander, April I.; Zhang, Yu-Guang; Ji, Qiang (2017). "New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem".Nature.548 (7667):326–329.Bibcode:2017Natur.548..326L.doi:10.1038/nature23483.PMID28792934.S2CID4463476.
^Szalay, FS; Sargis, EJ; Stafford, BJ (2000).Small marsupial glider from the Paleocene of Itaboraí, Brazil. Meeting of the Society of Vertebrate Paleontology.Journal of Vertebrate Paleontology. Supplement 73A. Vol. 20.
^Modesto, Sean P.; Smith, Roger M. H.; Campione, Nicolás E.; Reisz, Robert R. (2011). "The last 'pelycosaur': a varanopid synapsid from the Pristerognathus Assemblage Zone, Middle Permian of South Africa".Naturwissenschaften.98 (12):1027–34.Bibcode:2011NW.....98.1027M.doi:10.1007/s00114-011-0856-2.PMID22009069.S2CID27865550.
^Espen M. Knutsen; Emma Oerlemans (2019). "The last dicynodont? Re-assessing the taxonomic and temporal relationships of a contentious Australian fossil".Gondwana Research.77:184–203.doi:10.1016/j.gr.2019.07.011.S2CID202908716.
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