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Untangling the Multiple Ecological Radiations of Early Mammals

2019; Elsevier BV; Volume: 34; Issue: 10 Linguagem: Inglês

10.1016/j.tree.2019.05.008

1872-8383

David M. Grossnickle, Stephanie M. Smith, Gregory P. Wilson,

Physiological and biochemical adaptations

Multiple stem and early mammal groups experienced large-scale ecological radiations, including Jurassic mammaliaforms, Late Cretaceous multituberculates, Late Cretaceous metatherians, and Paleogene placentals. Small insectivores or omnivores are the progenitors of each ecological radiation, which involve rapid diversifications of diets and modes of locomotion. There are three main periods of ecological diversification (Early–Middle Jurassic, Late Cretaceous, and Paleogene), each involving radiations of multiple mammalian groups. The Late Cretaceous radiations may have been triggered by the KTR and the Paleogene radiations were to have been likely catalyzed by the end-Cretaceous mass extinction event. Phylogenetic context and paleontological data are critical for examining ecological radiations in deep time, especially because many radiations involve stem lineages of modern clades that do not have living representatives. The ecological diversification of early mammals is one of the most globally transformative events in Earth’s history and the Cretaceous Terrestrial Revolution (KTR) and end-Cretaceous mass extinction are commonly hailed as catalysts. However, a confounding issue when examining this diversification is that it comprised nested radiations of mammalian subclades within the broader scope of mammalian evolution. In the past 200 million years, various independent groups experienced large-scale radiations, each involving ecological diversification from ancestral lineages of small insectivores; examples include Jurassic mammaliaforms, Late Cretaceous metatherians, and Cenozoic placentals. Here, we review these ecological radiations, highlighting the nuanced complexity of early mammal evolution, the value of ecomorphological fossil data, and the importance of phylogenetic context in macroevolutionary studies. The ecological diversification of early mammals is one of the most globally transformative events in Earth’s history and the Cretaceous Terrestrial Revolution (KTR) and end-Cretaceous mass extinction are commonly hailed as catalysts. However, a confounding issue when examining this diversification is that it comprised nested radiations of mammalian subclades within the broader scope of mammalian evolution. In the past 200 million years, various independent groups experienced large-scale radiations, each involving ecological diversification from ancestral lineages of small insectivores; examples include Jurassic mammaliaforms, Late Cretaceous metatherians, and Cenozoic placentals. Here, we review these ecological radiations, highlighting the nuanced complexity of early mammal evolution, the value of ecomorphological fossil data, and the importance of phylogenetic context in macroevolutionary studies. a period (ca 125–80 Ma) in the mid-Cretaceous during which there was considerable taxonomic turnover and subsequent diversification of terrestrial clades that are now prominent in modern ecosystems, including flowering plants, social insects, squamates, turtles, birds, and therian mammals [49.Lloyd G.T. et al.Dinosaurs and the Cretaceous terrestrial revolution.Proc. Biol. Sci. 2008; 275: 2483-2490Crossref PubMed Scopus (0) Google Scholar, 50.Benton M.J. The origins of modern biodiversity on land.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010; 365: 3667-3679Crossref PubMed Scopus (73) Google Scholar]. when during the day or night an organism is active – diurnal, active during daytime; nocturnal, active during the night; cathemeral, equally likely to be active at any point during the day or night; and crepuscular, active at dawn and dusk. the mass extinction event 66 million years ago that wiped out not only nonavian dinosaurs but up to 75% of all terrestrial and marine species worldwide. sedimentary rock layers with exceptionally preserved fossils. The ‘Lagerstätten’ mentioned here are specifically ‘Konservat-Lagerstätten’, which preserve fossilized organisms (e.g., mammalian skeletons), whereas ‘Konzentrat-Lagerstätten’ are deposits with disarticulated organic parts (e.g., bone beds). how an animal moves through the substrates in its environment. Examples include arboreal (tree using), scansorial (both ground and tree using), ambulatory (terrestrial walking), saltatorial (terrestrial hopping), and fossorial (digging). a group formed by the common ancestor of crown-group mammals and the Jurassic animal Morganucodon (e.g., [12.O’Leary M.A. et al.The placental mammal ancestor and the post-K–Pg radiation of placentals.Science. 2013; 339: 662-667Crossref PubMed Scopus (0) Google Scholar]) or Sinoconodon (e.g., [6.Kielan-Jaworowska Z. et al.Mammals from the Age of Dinosaurs: Origins, Evolution, and Structure. Columbia University Press, 2004Crossref Google Scholar]) and all descendants of that ancestor. The group is morphologically diagnosed by the primary jaw joint being between the dentary and squamosal bones. Mammaliaforms often exhibit some distinctly mammalian characteristics, but also retain some more basal characteristics (e.g., the mammaliaform Morganucodon had a dentary–squamosal jaw joint but also retained the secondary quadrate-articular jaw joint found in nonmammalian synapsids and reptiles). crown-group metatherian mammals; that is, the common ancestor of all living metatherian mammals and all descendants of that ancestor whether extant or extinct. Metatherians have a relatively short gestation period and give birth to underdeveloped young, which often complete development in a pouch, also called a marsupium. With about 300 extant species, marsupials are less taxonomically diverse than placentals (with about 4000 extant species). one of the three main groups of mammals with living representatives (along with placentals and marsupials). They lay eggs but also produce milk for their young. Living species include the echidnas (four species) and the platypus (one species). an extinct group of nontherian mammals named for their molar teeth, which exhibit multiple small cusps in rows. Multituberculates were numerically abundant and ecologically diverse on Mesozoic and early Cenozoic terrestrial landscapes for approximately 130 million years from the Jurassic to the Eocene. They are often considered morphologically and ecologically analogous to rodents, although the two groups are not closely related. a major global warming event that occurred at the Paleocene–Eocene boundary approximately 56 million years ago. Global temperatures rose by 5–8°C; this change has been associated with dramatic species turnover, taxonomic diversification, and ecological change in a variety of organisms, especially mammals. crown-group eutherian mammals; that is, the common ancestor of all living placental mammals and all descendants of that ancestor whether extant or extinct. Placental mammals have a chorioallantoic placenta for nutrient exchange between mother and fetus during gestation. Placentals also generally have longer gestation periods and give birth to more-developed young than marsupials. Most extant mammals are placentals (e.g., rodents, bats, primates, carnivores). the group of animals encompassing all amniote tetrapods with a synapsid pattern of skull fenestration (only lower temporal fenestra present). This group includes nonmammalian synapsids (e.g., Dimetrodon, Cynognathus) as well as all extant and extinct mammals and mammaliaforms. the group of mammals including Metatheria (marsupials and their extinct relatives) and Eutheria (placentals and their extinct relatives).