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Untangling the Multiple Ecological Radiations of Early Mammals

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Untangling the Multiple Ecological Radiations of Early Mammals TREE 2553 No. of Pages 14 Trends in Ecology & Evolution Review Untangling the Multiple Ecological Radiations of Early Mammals David M. Grossnickle ,1,* Stephanie M. Smith,2,@ and Gregory P. Wilson1,@ The ecological diversification of early mammals is one of the most globally trans- Highlights formative events in Earth’s history and the Cretaceous Terrestrial Revolution Multiple stem and early mammal (KTR) and end-Cretaceous mass extinction are commonly hailed as catalysts. groups experienced large-scale eco- However, a confounding issue when examining this diversification is that it logical radiations, including Jurassic mammaliaforms, Late Cretaceous comprised nested radiations of mammalian subclades within the broader multituberculates, Late Cretaceous scope of mammalian evolution. In the past 200 million years, various indepen- metatherians, and Paleogene placentals. dent groups experienced large-scale radiations, each involving ecological diversification from ancestral lineages of small insectivores; examples include Small insectivores or omnivores are the progenitors of each ecological radiation, Jurassic mammaliaforms, Late Cretaceous metatherians, and Cenozoic placen- which involve rapid diversifications of tals. Here, we review these ecological radiations, highlighting the nuanced dietsandmodesoflocomotion. complexity of early mammal evolution, the value of ecomorphological fossil data, and the importance of phylogenetic context in macroevolutionary studies. There are three main periods of ecologi- cal diversification (Early–Middle Jurassic, Late Cretaceous, and Paleogene), each involving radiations of multiple mamma- The Ecological Diversification of Mammals lian groups. The Late Cretaceous radia- Modern mammals are extraordinarily diverse, possessing body masses spanning eight orders of tions may have been triggered by the magnitude and occupying habitats on land, in water, and in air. By contrast, 200 million years ago KTR and the Paleogene radiations were to have been likely catalyzed by the (Ma) the earliest mammaliaforms (see Glossary) (i.e., mammals and their closest relatives) were end-Cretaceous mass extinction event. mostly small, terrestrial insectivores persisting in reptile-dominated ecosystems. The evolutionary story of how mammaliaforms endured the Mesozoic Era (252–66 Ma), or the Age of Dinosaurs, Phylogenetic context and paleontologi- and subsequently rose to ecological prominence has fascinated researchers for over 150 years cal data are critical for examining ecolog- ical radiations in deep time, especially [1–7]. Gaps in the fossil record and the lack of living representatives of many early mammaliaform because many radiations involve stem groups have hindered our ability to examine some aspects of mammalian history, including the lineages of modern clades that do not ecological diversity of many clades. However, recent fossil discoveries, advances in comparative have living representatives. techniques (e.g., morphometrics, micro-computed tomography), and the development of phylo- genetic methods and molecular clock analyses have led to a much richer and more complex body of evidence for early mammaliaform diversification (e.g., [6–14]), which we critically review here. Early mammaliaforms comprise multiple independent clades that came and went intermittently throughout the Mesozoic and early Cenozoic. Evolutionary success varied across these clades and several groups underwent major ecological radiations at different times [2–8,13–18]. Here, ecological radiation is defined as a geologically rapid diversification event that led to a broad array of ecologies. The ecological radiations of early mammaliaforms have become increasingly apparent as researchers 1 consider the evolution of these groups in a phylogenetic context and with robust ecomorphological Department of Biology, University of Washington, Seattle, WA, USA datasets [8,10,11,17–24]. The radiations originated independently from mostly small, insectivorous 2Integrative Research Center, Field ancestors and many involved stem lineages of extant mammalian clades. The primary objectives Museum of Natural History, Chicago, of this review are to: (i) highlight the recent and growing evidence for these distinct radiations; and IL, USA (ii) address confounding issues in assessing ecological diversity patterns in early mammaliaforms. Multiple Radiations in Early Mammaliaforms *Correspondence: [email protected] (D.M. Grossnickle). The observation that multiple mammaliaform groups have experienced large-scale ecological @Twitter: @scutisorex (S.M. Smith) and radiations is not new. For instance, paleontologist Henry Fairfield Osborn coined the term @gpwilson11 (G.P. Wilson). Trends in Ecology & Evolution, Month 2019, Vol. xx, No. xx https://doi.org/10.1016/j.tree.2019.05.008 1 © 2019 Elsevier Ltd. All rights reserved. Trends in Ecology & Evolution adaptive radiation in 1902 and noted six independent diversifications of early mammaliaform Glossary groups as examples of adaptive radiations [2]. These are temporally and geographically distinct Cretaceous Terrestrial Revolution diversifications that include some of the radiations highlighted in this review, such as the Jurassic (KTR): aperiod(ca 125–80 Ma) in the (201–145 Ma) radiation of mammaliaforms, the Australian radiation of marsupials, and radiations mid-Cretaceous during which there was of multiple eutherian groups, including placentals. Osborn argued that each radiation involved considerable taxonomic turnover and subsequent diversification of terrestrial fi the diversi cation of diets and locomotor modes from an ancestral, small insectivore (although clades that are now prominent in at the time there was minimal fossil evidence to support this claim for the earliest radiations). modern ecosystems, including flowering Considerable scientific progress has been made since Osborn’s time and we now recognize plants, social insects, squamates, turtles, birds, and therian mammals additional independent radiations within Mammaliaformes. Further, the adaptive radiation [49,50]. concept has been refined by researchers [25–31] and the ecological radiations discussed in Diel activity pattern: when during the this review may not all qualify as adaptive radiations under modern definitions (hence, we refer day or night an organism is active – to them as ecological radiations instead of adaptive radiations). Future studies can assess diurnal, active during daytime; nocturnal, active during the night; cathemeral, whether the ecological radiations of early mammaliaforms meet additional criteria that are equally likely to be active at any point often proposed for adaptive radiations, such as a greater speciation rate early in the radiation during the day or night; and crepuscular, [26,31], monophyly of the radiating group [27],an‘early burst’ of morphological evolution at the active at dawn and dusk. onset of the radiation [25], and the presence of novel ecological opportunities as catalysts for End-Cretaceous mass extinction fi event: the mass extinction event diversi cation [29,31]. 66 million years ago that wiped out not only nonavian dinosaurs but up to 75% Small Insectivores Give Rise to Mammalian Diversity of all terrestrial and marine species During the 320-million-year history of synapsids, there have been numerous examples of small worldwide. Lagerstätten: sedimentary rock layers insectivore or omnivore progenitors radiating into ecologically diverse clades [2,15,32].This with exceptionally preserved fossils. The pattern recurred in early mammaliaforms and is highlighted in Figure 1 and in Table S1 in the sup- ‘Lagerstätten’ mentioned here are plemental information online. From these insectivorous or omnivorous forerunners, numerous specifically ‘Konservat-Lagerstätten’, dietary specialists have repeatedly evolved in mammalian clades, suggesting parallel ecological which preserve fossilized organisms fi (e.g., mammalian skeletons), whereas diversi cations. In addition, derived locomotor modes repeatedly evolved from ground- or tree- ‘Konzentrat-Lagerstätten’ are deposits dwelling (i.e., ambulatory, scansorial, or arboreal) ancestors. This includes convergent evolution with disarticulated organic parts of fossorial, semiaquatic, gliding, and saltatorial locomotion in the Mesozoic Era [6,8,19,33]. (e.g., bone beds). Locomotor mode: how an animal Below we review the lines of evidence that suggest each radiation involved significant ecological moves through the substrates in its environment. Examples include arboreal divergence from a small, ancestral insectivore or omnivore. We group the radiations into three (tree using), scansorial (both ground and distinct time periods of considerable ecological diversification: (i) Early–Middle Jurassic tree using), ambulatory (terrestrial (201–163 Ma); (ii) Late Cretaceous (100–66 Ma); and (iii) Paleocene–Eocene (66–34 Ma). walking), saltatorial (terrestrial hopping), and fossorial (digging). Jurassic Radiations: Origins of Early Ecological Diversity Mammaliaforms: a group formed by the common ancestor of crown-group Tooth and jaw morphologies indicate insectivory or insect-based omnivory in most mammals and the Jurassic animal mammaliaforms from the Late Triassic and earliest Jurassic [6,11,34–37]. These early insecti- Morganucodon (e.g., [12])or vores gave rise to ecologically diverse lineages, with evidence suggesting rapid ecological radia- Sinoconodon (e.g., [6]) and all tions of multiple groups during the Early and Middle Jurassic [6,8,18,20] (Figure 1 and 2). Recent descendants of
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