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Untangling the Multiple Ecological Radiations of Early Mammals
Abstract
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.
Supplementary resource (1)
... Two hypotheses provide a framework to discuss the timing of metatherian taxonomic and ecomorphological diversification (see Grossnickle et al., 2019 for review). "The Early Rise Hypothesis," coined by Grossnickle et al. (2019), is related to the ecological radiation of crown-group angiosperms (flowering plants), which began after the . Angiosperms experienced a taxonomic radiation during the KTR (125-80 Ma; Wing and Boucher, 1998;Anderson et al., 2005;Magallón et al., 2013;Magallón et al., 2015), but the Early Rise Hypothesis is more closely linked to the post-KTR ecological (not taxonomic) rise of angiosperms (beginning by ca. ...
... 85-80 Ma), which may have been a more critical driver of increases in mammalian diversity (Meredith et al., 2011;Eriksson, 2016). The Early Rise Hypothesis is supported by macroevolutionary patterns of some mammal groups (Wilson et al., 2012;Grossnickle and Polly, 2013;Grossnickle and Newham, 2016;Chen et al., 2019;Grossnickle et al., 2019); for example, multituberculates increased both their taxonomic and ecomorphological diversity during the late Late Cretaceous (ca. 83-66 Ma; Wilson et al. 2012 ). ...
... Alternatively, the downstream effects of the KTR might have manifested among non-therian mammals only (e.g., multituberculates; Wilson et al., 2012), and despite the increased diversity of food resources and novel evolutionary adaptations of tribosphenic molars (e.g., increased grinding capabilities), therians were ecomorphologically constrained until the extinction of non-avian dinosaurs (e.g., Simpson, 1937;Van Valen and Sloan, 1977;Archibald, 1983Archibald, , 2011Stucky, 1990;Alroy, 1999;Grossnickle et al., 2019). This hypothesis, called "the Suppression Hypothesis" (Grossnickle and Newham, 2016), is supported by evidence of sharp increases in origination rates (Alroy, 1999), body size (Alroy, 1999;Smith et al. 2010), and morphological disparity (Halliday and Goswami, 2016) in early Cenozoic mammalian faunas. ...
Metatherian mammals were taxonomically rich and abundant in Late Cretaceous faunas of North America. Although much attention has been paid to metatherian taxonomy, a comprehensive, quantitative study on the ecomorphology of this clade is lacking. Here, we predict the diets of a large sample of metatherians using three-dimensional dental topographic analysis, with the aim to better understand macroevolutionary patterns in dental morphology and dietary diversity. Contrary to their taxonomic diversity patterns, our results show that dental disparity and dietary diversity did not significantly change throughout the Late Cretaceous and that most metatherians were invertivorous (diets of insects and soft-bodied invertebrates). Nevertheless, we also found that metatherians occupied a wide range of dietary niches and were arguably the most dietarily diverse of any mammalian clade of the Late Cretaceous. Regarding the timing of metatherian ecomorphological diversification, our results indicate that it began by the mid-Cretaceous in-step with the Cretaceous Terrestrial Revolution and the taxonomic diversification of angiosperms, prior to the ecological diversifications of multituberculates and eutherians that began in the latest Cretaceous and Paleocene.
... 23) and is marked by the iterative evolution of ecomorphologically diverse clades, culminating in extant taxa (monotremes, marsupials, placentals) displaying spectacular morphological and ecological diversity. Conventional wisdom states that throughout synapsid history, relatively small-bodied faunivores are dominant early in evolutionary radiations and they give rise to ecologically diverse clades 6,[24][25][26][27][28] . Previous work has shown that small-bodied faunivore is the dominant ancestral ecomorphotype early in mammaliaform radiations (see ref. 28 and citations therein), Tables 1 and 2). ...
... Conventional wisdom states that throughout synapsid history, relatively small-bodied faunivores are dominant early in evolutionary radiations and they give rise to ecologically diverse clades 6,[24][25][26][27][28] . Previous work has shown that small-bodied faunivore is the dominant ancestral ecomorphotype early in mammaliaform radiations (see ref. 28 and citations therein), Tables 1 and 2). For pelycosaur subclades, the only significant trend in body size through time was within Sphenacodontidae, which experienced a positive trend (Supplementary Table 1 and Extended with the pattern of increasing body size diversity in crown mammal groups often used to test Cope's rule 7,29,30 , or 'Alroy's Axiom' 31 , which states that lineages tend to evolve towards larger body size. ...
... For our primary analyses, we analysed five temporally successive major radiations: (1) non-therapsid pelycosaurs (hereafter 'pelycosaurs'), (2) non-cynodont therapsids (hereafter 'therapsids'), (3) non-mammaliaform cynodonts (hereafter 'cynodonts'), (4) non-therian mammaliaforms (hereafter 'mammaliaforms') and (5) therians (eutherian-placental and metatherian-marsupial lineages). Each of these radiations is marked by considerable ecological diversification (thus, hereafter we refer to them as 'ecological radiations'), with descendent lineages achieving a broad diversity of body masses and diets 23,27,28 (Supplementary Methods). We further examined radiations at a phylogenetically finer scale in supplementary analyses. ...
Evolutionary radiations generate most of Earth’s biodiversity, but are there common ecomorphological traits among the progenitors of radiations? In Synapsida (the mammalian total group), ‘small-bodied faunivore’ has been hypothesized as the ancestral state of most major radiating clades, but this has not been quantitatively assessed across multiple radiations. To examine macroevolutionary patterns in a phylogenetic context, we generated a time-calibrated metaphylogeny (‘metatree’) comprising 1,888 synapsid species from the Carboniferous through the Eocene (305–34 Ma) based on 269 published character matrices. We used comparative methods
to investigate body size and dietary evolution during successive synapsid radiations. Faunivory is the ancestral dietary regime of each major synapsid radiation, but relatively small body size is only established as the common ancestral state of radiations near the origin of Mammaliaformes in the Late Triassic. The faunivorous ancestors of synapsid radiations typically have numerous novel characters compared with their contemporaries, and these derived traits may have helped them to survive faunal turnover events and subsequently radiate.
... The evolutionary history of placental mammals is well-documented in the fossil record, ranging from the origin of basal synapsids in the late Carboniferous 300 million years ago (mya) to the first appearance of Mammalia in the Triassic (205 mya) and the later diversification of placentals at the beginning of the Cenozoic (66 mya) (Rowe, 1988;Fröbisch et al., 2011;Grossnickle et al., 2019). These lineages gradually transitioned from a sprawling posture, basal to amniotes, to a more upright posture. ...
... Mammals first appeared in the Triassic (205 mya) and diversified through the Mesozoic (Rowe, 1988;Grossnickle et al., 2019). The earliest mammals, exemplified by Morganucodon, had many characteristics associated with living mammals, particularly the dentary-squamosal joint, but fell stemward of crown Mammalia (Kemp, 2005). ...
... The Mesozoic ended 66 mya with the Cretaceous-Paleogene (KPg) mass extinction, which killed off most larger tetrapods, including non-avian dinosaurs and pterosaurs (Robertson et al. 2004;Schulte et al., 2010;Gulick et al., 2019). Placental mammals rapidly radiated in the wake of the KPg extinction, beginning the "Age of Mammals" (Davies et al., 2017;Grossnickle et al., 2019). Recognizable ancestors to crown orders of placentals, including primates and carnivorans, appeared at this time, but "archaic" placental groups, which have no clear affinities to modern orders, dominated the initial radiation ( Figure 1.3) Chester et al., 2015). ...
Mammals have diversified in locomotor mode to a greater extent than any other group, from fully aquatic whales and powered flight in bats to the fastest extant runners, cheetahs, and pronghorn. I focus on the lumbar vertebrae of placental mammals, a region of the spine that is
not found in most other tetrapods.. This region plays an important role in locomotion by facilitating flexing and bending in the back. My research asks how this feature evolved and diversified in function during the Paleogene radiation of mammals immediately after the extinction of the dinosaurs and how these changes related to locomotor diversification among the
major placental clades. I surveyed lumbar vertebrae from Paleogene mammals and tested how differences in morphology related to ancestry and locomotor function (66-23 million years ago). I categorized important features for the vertebrae and mapped these over a phylogenetic tree to assess which features evolved quickly and which evolved slowly. I then quantified the shape of the most intact fossils using geometric morphometrics and compared the 3D shape of fossil lumbar vertebrae
with that of modern. I found high variation across Paleogene mammals, suggesting that lumbar vertebrae were a key component to mammalian locomotion during this radiation, evolving quickly in response to changing function. Finally, I tested the function of unusually shaped articulations that were common in many Paleogene mammals using digital models of fossil
vertebrae to simulate the range of motion. This showed unexpected mobility in the spine of these early placental mammals. Together this work shows how the morphology and function of lumbar vertebrae have evolved throughout the Cenozoic and how phylogeny impacted this process.
... The diversity of mammalian adaptations, ranging from the fast and semelparous (reproducing only once in a lifetime; Stearns, 1992) life history of antechinus to the slow and long lives of bowhead whales (Perrin et al., 2009) has allowed mammals to occupy all the land (Burgin et al., 2018;Grossnickle et al., 2019), exploit air (Babich Morrow et al., 2021;Maina, 2000), and even inhabit the sea (Davis, 2019). Despite this wide ecological radiation (Grossnickle et al., 2019), evolutionary history and energetic constraints limit the set of life history strategies (i.e., combinations of life history traits) that are viable in nature (Grime & Pierce, 2012;Stearns, 1992). ...
... The diversity of mammalian adaptations, ranging from the fast and semelparous (reproducing only once in a lifetime; Stearns, 1992) life history of antechinus to the slow and long lives of bowhead whales (Perrin et al., 2009) has allowed mammals to occupy all the land (Burgin et al., 2018;Grossnickle et al., 2019), exploit air (Babich Morrow et al., 2021;Maina, 2000), and even inhabit the sea (Davis, 2019). Despite this wide ecological radiation (Grossnickle et al., 2019), evolutionary history and energetic constraints limit the set of life history strategies (i.e., combinations of life history traits) that are viable in nature (Grime & Pierce, 2012;Stearns, 1992). These limits restrict mammalian investments in survival, growth, and reproduction to two major dimensions of life history trait variation Gaillard et al., 1989;Healy et al., 2019;Oli, 2004). ...
Mammalian life history strategies can be characterised by a few axes of variation, conforming a space where species are positioned based on the life history strategies favoured in the environment they exploit. Yet, we still lack global descriptions of the diversity of realised mammalian life history and how this diversity is shaped by the environment. We used six life history traits to build a life history space covering worldwide mammalian adaptation, and we explored how environmental realms (land, air, water) influence mammalian life history strategies. We demonstrate that realms are tightly linked to distinct life history strategies. Aquatic and aerial species predominantly adhere to slower life history strategies, while terrestrial species exhibit faster life histories. Highly encephalised terrestrial species are a notable exception to these patterns. Furthermore, we show that different mode of life may play a significant role in expanding the set of strategies exploitable in the terrestrial realm. Additionally, species transitioning between terrestrial and aquatic realms, such as seals, exhibit intermediate life history strategies. Our results provide compelling evidence of the link between environmental realms and the life history diversity of mammals, highlighting the importance of differences in mode of life to expand life history diversity.
... Following their emergence in the Early Jurassic or Late Triassic, mammals quickly became established and rapidly diversified, adapting well to life alongside dinosaurs (Grossnickle et al., 2019;Hu et al., 2005;Luo, 2007;Luo et al., , 2015. Although the extinction of the dinosaurs opened up a multitude of niches for mammals to invade, their ability to do so successfully was underpinned by their pre-existing diversity. ...
... Although the extinction of the dinosaurs opened up a multitude of niches for mammals to invade, their ability to do so successfully was underpinned by their pre-existing diversity. They had long since adapted to a variety of ecological conditions on the land, in the sea, and in the airrunning, swimming, gliding, climbing, and diggingjust as they continue to do today (Chen & Wilson, 2015;Grossnickle et al., 2019;Hu et al., 2005;Ji et al., 2006;Luo, 2007;Luo et al., , 2015Luo et al., , 2017Meng et al., 2015). The deep and successful evolutionary history of the mammalian class has resulted in an incredible amount of morphological and behavioral diversity across the globe. ...
This volume presents an array of different case studies which take as primary material data sourced from the NOW (‘New and Old Worlds’) database of fossil mammals. The NOW database was one of the very first large paleobiological databases, and since 1996 it has been expanded from including mainly Neogene European land mammals to cover the entire Cenozoic at a global scale. In the last two decades the number of works that are based in the use of huge databases to explore ecological and evolutionary questions has increased exponentially, and even though the importance of big data in paleobiological research has been outlined in selected chapters of general works, no volume has appeared before this one which solely focuses on the databases as a primary source in reconstructing the past. The purpose of this book is to provide an illustrative volume showing the importance of big data in paleobiological research, and presenting a broad array of unpublished examples and case studies. The book is mainly aimed to professional palaeobiologists working with Cenozoic land mammals, but the scope of the book is broad enough to fit the interest for evolutionary biologists, paleoclimatologists and paleoecologists.
The volume is divided in four parts. The first part includes two chapters on the development of large paleobiological databases, providing a first-hand account on the logic and the functioning of these databases. This is a much-needed perspective which is ignored by most researchers and users of such databases and, even if centered in the NOW database, the lessons that can be learned from this part can be extended to other examples. After this introductory part, the body of the book follows and is divided into three parts: patterns in regional faunas; large scale patterns and processes; and ecological, biogeographical and evolutionary patterns of key taxa. Each chapter is written by well-known specialists in the field, with some participation of members of the NOW advisory board. The array of selected mammal taxa ranges from carnivores, equids, ruminants and rodents to the genus Homo. The topics studied also include the diversification and radiation of major clades, large-scale paleobiogeographical patterns, the evolution of ecomorphological patterns and paleobiological problems such as evolution of body size or species longevity. In most cases the results are discussed in relation to protracted environmental or paleogeographic changes.
... Following their emergence in the Early Jurassic or Late Triassic, mammals quickly became established and rapidly diversified, adapting well to life alongside dinosaurs (Grossnickle et al., 2019;Hu et al., 2005;Luo, 2007;Luo et al., , 2015. Although the extinction of the dinosaurs opened up a multitude of niches for mammals to invade, their ability to do so successfully was underpinned by their pre-existing diversity. ...
... Although the extinction of the dinosaurs opened up a multitude of niches for mammals to invade, their ability to do so successfully was underpinned by their pre-existing diversity. They had long since adapted to a variety of ecological conditions on the land, in the sea, and in the airrunning, swimming, gliding, climbing, and diggingjust as they continue to do today (Chen & Wilson, 2015;Grossnickle et al., 2019;Hu et al., 2005;Ji et al., 2006;Luo, 2007;Luo et al., , 2015Luo et al., , 2017Meng et al., 2015). The deep and successful evolutionary history of the mammalian class has resulted in an incredible amount of morphological and behavioral diversity across the globe. ...
Recent studies have demonstrated dramatic changes in North American rodent and lagomorph faunas through the Cenozoic, with open-habitat specialists (characterized by increased tooth crown height and adaptations for burrowing, jumping, or running) becoming common as open and arid habitats spread. These studies have primarily focused on continental scale analyses, but comparisons of regional and local scale changes are key to understanding how individual faunas changed over time and the roles exerted by topography and local climatic conditions on these faunal changes. Here, we use a database of all fossil rodents and lagomorphs in North America modified from NOW, MIOMAP, and FAUNMAP to compare faunas through time across nine distinct regions. Our analyses reveal asynchronous changes across the continent, with specialized dietary and locomotor adaptations in rodents and lagomorphs occurring earlier in relatively cool, arid regions at higher latitudes. Findings suggest topographic complexity and volcanic activity potentially drove aspects of ecomorphological evolution in rodents and lagomorphs. The attributes of open and arid-adapted taxa likely facilitated their spread from tectonically and volcanically active regions across the continent, as environmental conditions changed through the Cenozoic.KeywordsClimate changeHypsodontyMammal FaunasNorth AmericaRodentiaLagomorpha
... Following their emergence in the Early Jurassic or Late Triassic, mammals quickly became established and rapidly diversified, adapting well to life alongside dinosaurs (Grossnickle et al., 2019;Hu et al., 2005;Luo, 2007;Luo et al., 2011Luo et al., , 2015. Although the extinction of the dinosaurs opened up a multitude of niches for mammals to invade, their ability to do so successfully was underpinned by their pre-existing diversity. ...
... Although the extinction of the dinosaurs opened up a multitude of niches for mammals to invade, their ability to do so successfully was underpinned by their pre-existing diversity. They had long since adapted to a variety of ecological conditions on the land, in the sea, and in the airrunning, swimming, gliding, climbing, and diggingjust as they continue to do today (Chen & Wilson, 2015;Grossnickle et al., 2019;Hu et al., 2005;Ji et al., 2006;Luo, 2007;Luo et al., 2011Luo et al., , 2015Luo et al., , 2017Meng et al., 2015). ...
Tropical vegetation categories in Africa, America and Asia can be differentiated by their mammal communities. We studied 163 localities assigned to Olson’s (1983) vegetation categories in five ecosystems. Non-volant species over 500 g were classified into locomotion, body mass, and two hierarchical dietary groups, and the resulting community structures were analyzed using NPMANOVA and SIMPER. Results show the community structures are significantly different between most of Olson’s vegetation categories in Africa and America. In Asia, the differences are not significant, although there are a limited number of vegetation categories in our Asian dataset. In Africa, both dietary variables are the best at differentiating the vegetation categories followed by locomotion. In America, diet 2 is the best variable followed by the others. Body mass was not a good discriminator in Africa, but is moderately good in America. Specific differences between the continents and reasons underlying these differences are discussed.KeywordsCommunity structureContinentsEcovariableOlson’s (1983) vegetation categoriesNPMANOVASIMPERTropicsVegetation
... We infer that these diversification events are more likely to come from invertebrate omnivory, and less often from omnivores that incorporate all food types. This idea agrees with evidence that many early mammalian radiations originated from small insectivorous omnivores [45]. Understanding the difference in ecology and evolution of omnivorous diets could help explain some instances of mammalian diversification and evolution. ...
... It is also important to note that, while we found high transition rates from vertivory to incorporating more plant and invertebrate material, this trend does not appear to be a common one in the fossil record. Many early mammals are considered to have been invertivorous [45]. In addition, hypercarnivory has been shown to act as an evolutionary ratchet causing hypercarnivores to further specialize on meat consumption, which makes them more vulnerable to extinction [47]. ...
Mammalian omnivores are a broad group of species that are often treated uniformly in ecological studies. Here, we incorporate omnivorous dietary differences to investigate previously found mammalian macroevolutionary and macroecological trends. We investigate the frequency with which vertebrate prey, invertebrate prey, fibrous plant material and non-fibrous plant material co-occur in the diets of terrestrial mammals. We quantify the body size distributions and phylogenetic signal of different omnivorous diets and use multistate reversible jump Markov chain Monte Carlo methods to assess the transition rates between diets on the mammalian phylogenetic tree. We find omnivores that consume all four food types are relatively rare, as most omnivores consume only invertebrate prey and non-fibrous plants. In addition, omnivores that only consume invertebrate prey, many of which are from Rodentia, are on average smaller than omnivores that incorporate vertebrate prey. Our transition models have high rates from invertivorous omnivory to herbivory, and from vertivory to prey mixing and ultimately invertivory. We suggest prey type is an important aspect of omnivore macroevolution and macroecology, as it is correlated with body mass, evolutionary history and diet-related evolutionary transition rates. Future work should avoid lumping omnivores into one category given the ecological variety of omnivore diets and their strong evolutionary influence.
... The huge variety of skull and jaw shapes, dental morphologies, and occlusal relationships reflect the broad dietary ecology of mammal relatives from the Mesozoic. Adding to the evidence derived from dental features, their diverse postcranial anatomy (i.e., body and limb bones) shows adaptations to different substrates with different locomotor modes to occupy different niches within a habitat (e.g., Chen & Wilson, 2015;Grossnickle et al., 2019). Almost all diet groups of terrestrial mammals are known from Mesozoic fossils: insectivory, omnivory, carnivory, scavenging, and even feeding on colonial insects convergent to myrmecophagy of some modern mammals (Luo, 2007). ...
The complex evolutionary history behind modern mammalian chewing performance and hearing function is a result of several changes in the entire skeletomuscular system of the skull and lower jaw. Lately, exciting multifunctional 3D analytical methods and kinematic simulations of feeding functions in both modern and fossil mammals and their cynodont relatives approach this topic, giving fresh insights into the history of mammalian masticatory behaviors and their evolutionary trends. One crucial transformation in this context is the segregation of postdentary bones (becoming the mammalian middle ear) from the lower jaw, which is posited to have led to the important functional decoupling of the hearing and feeding systems. Evolution of the middle ear is regarded as the key transition that enhanced both mammalian chewing performance and hearing capacity. Three major functional parts undergo substantial evolutionary changes in this process that are anatomically linked to each other: the lower jaw and dentition, middle ear, and inner ear. Sound, transmitted via vibrations of the bony middle ear elements to the inner ear, is converted into movements of the endolymph fluid that shift hair cells of the organ of Corti, triggering neural stimuli perceived as hearing. Structural changes in one part of the system influence the function of the other two. In this review, I highlight recent advances in research focusing on the enhancement of both chewing performance and hearing ability in mammalian history to feature the mechanisms that led to the decoupling of the hearing system (i.e., middle and inner ear) from the feeding system.
... Understanding the dietary habits of species is crucial for assessing functional diversity, evolutionary patterns, and the ecological roles they play (Verde Arregoitia and D'Elía 2021). The diet data of vertebrates, including those from species previously considered strictly herbivorous, offer valuable insights into their niches and can significantly inform conservation and management strategies (González-Maya et al. 2017;Grossnickle et al. 2019). Despite the challenges inherent in characterizing diets due to complex foraging patterns (Ungar 2010;Nielsen et al. 2018), recent findings on the Central American agouti reveal its opportunistic feeding behaviors, including predation on small vertebrates. ...
La guatusa centroamericana, Dasyprocta punctata, ha sido tradicionalmente considerada un herbívoro, alimentándose principalmente de frutos y semillas. Sin embargo, existen informes de este roedor consumiendo 3 especies de vertebrados: un ratón (en cautiverio), un ave y una lagartija gusano. En este estudio, añadimos 2 nuevas especies de vertebrados a la dieta de la guatusa: 1 ave y 1 mamífero. Llevamos a cabo investigaciones y guiamos tours de historia natural en la región de Monteverde, Costa Rica. Monteverde es bien conocido por sus reservas biológicas y sus actividades de ecoturismo. Los poblados de Monteverde y Santa Elena están situados dentro del Bosque Nuboso Tropical Montano, una franja altitudinal relativamente estrecha con cobertura de nubes frecuente durante gran parte del año. En 2 ocasiones separadas, observamos guatusas depredando especies de vertebrados en Monteverde. El 8 de junio de 2023, vimos a una guatusa adulta con un armadillo de nueve bandas juvenil, Dasypus novemcinctus, en la boca. El 12 de julio de 2024, observamos a otra guatusa persiguiendo y consumiendo 2 polluelos de la codorniz serrana pechinegra, Odontophorus leucolaemus. Estos 2 nuevos ítems de presa sugieren tendencias carnívoras oportunistas de la guatusa. Parece ser que este roedor captura animales jóvenes que no representan una amenaza significativa ni requieren un esfuerzo considerable para ser capturados, ni causan daños colaterales. De esta manera, la guatusa obtiene algunos nutrientes esenciales que no obtiene de su dieta habitual basada en plantas durante tiempos de escasez.
... These adaptations, which include morphological, physiological, and behavioral specializations, are reflected in traits such as eye shape, sensory systems, and endothermy. These traits have evolved in response to light, temperature, and predation risk (Grossnickle 2019). ...
Activity patterns provide important information about the ecology and behavior of species, however, knowledge about the activity of many arboreal mammal species remains scarce in tropical and subtropical regions. This paper describes the activity pattern of arboreal and semi-arboreal mammals in a tropical forest in southwestern Oaxaca, Mexico. Hypotheses were formulated suggesting seasonal variations in response to resource availability, and that species of the same trophic guild would adjust their activity in response to interference behaviors. The study was conducted over two years by photo-trapping. Camera traps were placed at ground, understory, and canopy levels in a tropical forest. The overlap coefficient among diurnal species ranged from 0.67 to 0.83, while for nocturnal species it ranged from 0.8 to 0.94. Virginia opossum, Didelphis virginiana and Mexican mouse opossum, Marmosa mexicana showed statistically significant differences in activity between seasons. No statistically significant differences were observed in the activity pattern between nocturnal species; however, for diurnal species, differences were found between White-nosed coati Nasua narica and Gray squirrel Sciurus aureogaster and Tayra Eira barbara and Gray squirrel. Most species present a similar activity pattern, spatial segregation may allow their coexistence. This is one of the first studies of quantifications of temporal patterns for arboreal and semi-arboreal species in Mexico.
... The jaw joint of Brasilodon was apparently capable of functioning without a reinforcing secondary contact, and articulation took place solely through the small quadrate-articular joint. Miniaturization has been correlated with the evolution of other key mammalian traits including metabolic rate, thermoregulation and insectivorous ecology [13][14][15][16][17][18][79][80][81] , and it seems likely that small body size was also involved in driving evolution of the mammalian jaw joint. However, the relatively larger size of some tritylodontids like Kayentatherium suggests further complexity, and other factors such as muscle reorganization, feeding ecology and masticatory behaviour may have contributed 30,49,74,82 . ...
The acquisition of the load-bearing dentary–squamosal jaw joint was a key step in mammalian evolution1–5. Although this innovation has received decades of study, questions remain over when and how frequently a mammalian-like skull–jaw contact evolved, hindered by a paucity of three-dimensional data spanning the non-mammaliaform cynodont–mammaliaform transition. New discoveries of derived non-mammaliaform probainognathian cynodonts from South America have much to offer to this discussion. Here, to address this issue, we used micro-computed-tomography scanning to reconstruct the jaw joint anatomy of three key probainognathian cynodonts: Brasilodon quadrangularis, the sister taxon to Mammaliaformes6–8, the tritheledontid-related Riograndia guaibensis⁹ and the tritylodontid Oligokyphus major. We find homoplastic evolution in the jaw joint in the approach to mammaliaforms, with ictidosaurs (Riograndia plus tritheledontids) independently evolving a dentary–squamosal contact approximately 17 million years before this character first appears in mammaliaforms of the Late Triassic period10–12. Brasilodon, contrary to previous descriptions6–8, lacks an incipient dentary condyle and squamosal glenoid and the jaws articulate solely using a plesiomorphic quadrate–articular joint. We postulate that the jaw joint underwent marked evolutionary changes in probainognathian cynodonts. Some probainognathian clades independently acquired ‘double’ craniomandibular contacts, with mammaliaforms attaining a fully independent dentary–squamosal articulation with a conspicuous dentary condyle and squamosal glenoid in the Late Triassic. The dentary–squamosal contact, which is traditionally considered to be a typical mammalian feature, therefore evolved more than once and is more evolutionary labile than previously considered.
... Ecological opportunities arising after the Cretaceous-Paleogene boundary (KPg) led mammals to a significant increase in both interordinal cladogenesis (i.e., the origin of taxonomic orders) and intraordinal cladogenesis (i.e., diversification within these orders), ultimately contributing to their vast diversity seen today (Meredith et al. 2011;Benevento, Benson, and Friedman 2019). However, the origins of mammals date back to the Mesozoic era (~200 Mya), and the specific locations sustaining these different radiations remain largely unknown (Grossnickle, Smith, and Wilson 2019). While it is recognised that mammals present high phylogenetic turnover in mountainous areas worldwide (Peixoto et al. 2017), it remains unclear whether this turnover is primarily driven by the generation of recent lineages, conservation of ancient ones or a combination of both (Azevedo et al. 2020). ...
Aim: To describe worldwide distribution of mammalian cradles and museums using the rates of phylogenetic lineage turnoveras a surrogate. Additionally, we investigated the influences of current water–energy dynamics, climate instability, past climatechanges and elevational ranges on the distribution of these evolutionary zones.
Location: Global.
Time Period: Current.
Major Taxa Studied: Terrestrial mammals.
Methods: We developed a new methodology that consists of calculating the spatial phylogenetic turnover for non- overlappingtemporal segments of phylogenetic trees. By calculating the relative turnover in each tree segment, we quantified the rate ofaccumulation of phylogenetic turnover through time. We depicted cold and hotspots of rates of lineage turnover using bivariatemaps and examined the effects of environmental factors using a path model.
Results: The distributions of cradles and museums of biodiversity are primarily driven by water–energy dynamics. Environmentswith higher water availability than energetic demand predominantly act as cradles, as seen in tropical rainforests, while xeric-like environments predominantly serve as museums. Conversely, regions undergoing higher historical climate changes becomecradles, such as in higher northern latitudes, while climatically stable areas function as museums. Mountains play a dual role,acting as both cradles and museums by generating new lineages along their elevation bands while simultaneously providingclimate refuges for ancient mammal lineages.
Main Conclusions: Our findings demonstrate that cradles and museums are not merely a dichotomy but exist along an evolu-tionary continuum. Furthermore, they reveal how spatial patterns of mammalian cradles and museums are intricately shaped bybiogeographical processes governed by environmental forces. Uncovering these hidden effects provides insights into the ecolog-ical mechanisms by which ongoing climate changes continually shape evolutionary assemblages over time.
... Mesozoic mammals were thought to be small fossorial and arboreal species that occupied ecological niches similar to small-sized (<1 kg) living taxa (Osborn 1902;Kielan-Jaworowska et al. 2004;Archibald 2011). However, it has recently been discovered that stem mammals were ecologically diverse in size, diet and locomotion (Chen & Wilson 2015;Benevento et al. 2019;Grossnickle et al. 2019;Morales-García et al. 2021). The fifth mass extinction at the end of the Mesozoic (c. ...
Mammals exhibit ecology‐related diversity in long bone morphology, revealing an ample spectrum of adaptations both within and between clades. Their occupation of unique ecological niches in postcranial morphology is thought to have occurred at different chronological phases in relation to abiotic factors such as climate and biotic interactions amongst major clades. Mammalian morphologies rapidly evolved throughout the Cenozoic, with several orders following different paths in locomotory adaptations. We assessed morphological variation in limb proportions for a rich sample of extant and fossil large mammalian clades (mainly carnivores and ungulates) to test associations with ecological adaptations and to identify temporal patterns of diversification. Phylogenetic relationships among species were incorporated into the analysis of limb bone proportions, showing significant morphological changes in relation to species substrate preference. Major climatic events appeared to have no temporal impact on patterns of morphological diversification, expressed as morphological disparity, in either clades or ecological groups. Linear stochastic differential equations supported a double‐wedge diversification model for limb proportions of carnivorous clades (‘Creodonta’ and Carnivora). The concomitant increase in morphological disparity throughout the Cenozoic for the orders Carnivora and Artiodactyla had a significative impact on the disparity of Perissodactyla supporting biotic interaction as primary driver of mammalian morphological diversification. Our findings challenge the classic idea of abiotic factors as primary driving forces in the evolution of postcranial morphologies for large terrestrial mammals, and propose clade competition as a key factor in temporal diversification.
... In the early Cenozoic (66-40 Ma ago), mammals experienced a large-scale, rapid diversification in body mass, diet, diel activity patterns and life history traits (Grossnickle et al. 2019). The main extant orders diversified mainly in the Eocene, spreading in a wide diversity of ecological niches (Gingerich 2006, Rose 2006. ...
Maintaining thermal homeostasis in water is a major challenge for semi-aquatic mammals, which entails morphological, behavioural and physiological adaptations. Foraging strategies and dietary-induced thermogenesis (DIT) contribute to regulating body temperature in cold environments. As DIT differs among macronutrients, semi-aquatic mammals may be expected to regulate their macronutrient ratios to enhance their capability of thermoregulating.
We estimated the nutritional intake target of a widespread semi-aquatic mustelid, Eurasian otter Lutra lutra by reviewing the available literature on otters' diet throughout Europe and assessing the nutritional composition of non-commercial fish species forming the bulk of otter diet through laboratory analyses.
The macronutrient intake target for the otter was assessed as 61% protein and 39% lipid energy ratios. The mean percent protein energy was higher than that reported for typical hypercarnivores and tended to increase with decreasing water temperatures.
The additional source of heat provided by the thermogenic effect induced by protein digestion may contribute to balance heat loss, compensating for the costs associated with protein overconsumption.
If, as suggested by fossil records, semi-aquatic habits appeared after the development of otter's ‘fish specialist’ dentition, the thermogenic effect of its fish-based diet may have promoted the tight relationship occurring between otters and water habitats.
... The farther back we go in the past, the higher the probability that lineages will have experienced more ecological and geographical shifts. In other words, the complexity and number of sources of ecological opportunity encountered by a lineage likely increase over time (Bouchenak-Khelladi et al., 2015;Grossnickle et al., 2019;Lagomarsino et al., 2016). This multitude of events leaves signals in evolutionary trajectories, with rate magnitudes varying dramatically across the tree of life (Alfaro et al., 2009;Cooney & Thomas, 2021;Jetz et al., 2012;Rabosky et al., 2013). ...
Evolution proceeds unevenly across the tree of life, with some lineages accumulating diversity more rapidly than others. Explaining this disparity is challenging as similar evolutionary triggers often do not result in analogous shifts across the tree, and similar shifts may reflect different evolutionary triggers. We used a combination of approaches to directly consider such context-dependency and untangle the complex network of processes that shape macroevolutionary dynamics, focusing on Pleurodonta, a diverse radiation of lizards. Our approach shows that some lineage-wide signatures are lost when conditioned on sublineages: while viviparity appears to accelerate diversification, its effect size is overestimated by its association with the Andean mountains. Conversely, some signals that erode at broader phylogenetic scales emerge at shallower ones. Mountains, in general, do not affect speciation rates; rather, the occurrence in the Andean mountains specifically promotes diversification. Likewise, the evolution of larger sizes catalyzes diversification rates, but only within certain ecological and geographical settings. We caution that conventional methods of fitting models to entire trees may mistakenly assign diversification heterogeneity to specific factors despite evidence against their plausibility. Our study takes a significant stride toward disentangling confounding factors and identifying plausible sources of ecological opportunities in the diversification of large evolutionary radiations.
... To date, the evolution and functional morphology of molar crowns have been examined extensively for early mammals, including dryolestids (Crompton 1971;Crompton & Jenkins, 1968;Schultz & Martin 2014). The advent of key innovations such as the tribosphenic molar and precise dental occlusion are just two examples of how changes in dental morphology can increase biomechanical efficiency of mastication and facilitate more versatile feeding adaptations (Davis, 2011;Grossnickle et al., 2019;Luo, 2007;Luo et al., 2001;Martin et al., 2020;Schultz & Martin, 2011. However, before CT scanning became widely available to examine the root structures inside the jaws (Self, 2015a, b), few studies have fully explored the evolutionary morphology of tooth roots or investigated the functional relationship between crown and root structures (but see Sulej et al., 2020). ...
... The positive effects of colonization time on root-level phylogenetic dispersion tendencies, rather than clustering tendencies (P 4.2 ), may relate to the persistence of ancient lineages and distantly related colonizers over colonization time. For instance, the mammal communities in this study included ancient lineages of Marsupials in America and Placentalia that diverged in the Cretaceous (~160 Mya) and lineages that radiated after the Palaeogene (~66 Mya) Grossnickle et al., 2019;O'Leary et al., 2013). ...
Aim
Tropical regions harbour over half of the world's mammals and birds, but how their communities have assembled over evolutionary timescales remains unclear. To compare eco‐evolutionary assembly processes between tropical mammals and birds, we tested how hypotheses concerning niche conservatism, environmental stability, environmental heterogeneity and time‐for‐speciation relate to tropical vertebrate community phylogenetic and functional structure.
Location
Tropical rainforests worldwide.
Time period
Present.
Major taxa studied
Ground‐dwelling and ground‐visiting mammals and birds.
Methods
We used in situ observations of species identified from systematic camera trap sampling as realized communities from 15 protected tropical rainforests in four tropical regions worldwide. We quantified standardized phylogenetic and functional structure for each community and estimated the multi‐trait phylogenetic signal (PS) in ecological strategies for the four regional species pools of mammals and birds. Using linear regression models, we test three non‐mutually exclusive hypotheses by comparing the relative importance of colonization time, palaeo‐environmental changes in temperature and land cover since 3.3 Mya, contemporary seasonality in temperature and productivity and environmental heterogeneity for predicting community phylogenetic and functional structure.
Results
Phylogenetic and functional structure showed non‐significant yet varying tendencies towards clustering or dispersion in all communities. Mammals had stronger multi‐trait PS in ecological strategies than birds (mean PS: mammal = 0.62, bird = 0.43). Distinct dominant processes were identified for mammal and bird communities. For mammals, colonization time and elevation range significantly predicted phylogenetic clustering and functional dispersion tendencies respectively. For birds, elevation range and contemporary temperature seasonality significantly predicted phylogenetic and functional clustering tendencies, respectively, while habitat diversity significantly predicted functional dispersion tendencies.
Main conclusions
Our results reveal different eco‐evolutionary assembly processes structuring contemporary tropical mammal and bird communities over evolutionary timescales that have shaped tropical diversity. Our study identified marked differences among taxonomic groups in the relative importance of historical colonization and sensitivity to environmental change.
... However, this is not the only optimal path on this landscape, as moving back towards the ancestral cynodont peak is also Pareto optimal. These multiple optima may have facilitated the disparate evolution of mammaliaforms 65 (which was not certified by peer review) is the author/funder. All rights reserved. ...
The 'sprawling-parasagittal' postural transition is a key part of mammalian evolution, associated with sweeping reorganization of the postcranial skeleton in mammals compared to their forebears, the non-mammalian synapsids. However, disputes over forelimb function in fossil synapsids render the precise nature of the 'sprawling-parasagittal' transition controversial. We shed new light on the origins of mammalian posture, using evolutionary adaptive landscapes to integrate 3D humerus shape and functional performance data across a taxonomically comprehensive sample of fossil synapsids and extant comparators. We find that the earliest pelycosaur-grade synapsids had a unique mode of sprawling, intermediate between extant reptiles and monotremes. Subsequent evolution of synapsid humerus form and function showed little evidence of a direct progression from sprawling pelycosaurs to parasagittal mammals. Instead, posture was evolutionarily labile, and the ecological diversification of successive synapsid radiations was accompanied by variation in humerus morphofunctional traits. Further, synapsids frequently evolve towards parasagittal postures, diverging from the reconstructed optimal evolutionary path; the optimal path only aligns with becoming increasingly mammalian in derived cynodonts. We find the earliest support for habitual parasagittal postures in stem therians, implying that synapsids evolved and radiated with distinct forelimb trait combinations for most of their recorded history.
... Combining paleontological-the primary source of infor mation on biodiversity in the distant past-and neontological data, together with advances in analytical methods, have shed light on the intricate dynamics of diversification across various lineages and through time (3)(4)(5)(6)(7). Abiotic factors like continental fragmentation and temperature fluctuations have been suggested as significant drivers of diversification (8,9), as well as key innovations or biotic changes, such as the Angiosperm Terrestrial Revolution (ATR, 100 to 50 Ma) (10)(11)(12)(13). All these factors have been primarily associated with bursts of diversification (i.e., the difference between origination and extinction). ...
With ~14,000 extant species, ants are ubiquitous and of tremendous ecological importance. They have undergone remarkable diversification throughout their evolutionary history. However, the drivers of their diversity dynamics are not well quantified or understood. Previous phylogenetic analyses have suggested patterns of diversity dynamics associated with the Angiosperm Terrestrial Revolution (ATR), but these studies have overlooked valuable information from the fossil record. To address this gap, we conducted a comprehensive analysis using a large dataset that includes both the ant fossil record (~24,000 individual occurrences) and neontological data (~14,000 occurrences), and tested four hypotheses proposed for ant diversification: co-diversification, competitiontive extinction, hyper-specialization, and buffered extinction. Taking into account biases in the fossil record, we found three distinct diversification periods (the latest Cretaceous, Eocene, and Oligo-Miocene) and one extinction period (Late Cretaceous). The competitive extinction hypothesis between stem and crown ants is not supported. Instead, we found support for the co-diversification, buffered extinction, and hyper-specialization hypotheses. The environmental changes of the ATR, mediated by the angiosperm radiation, likely played a critical role in buffering ants against extinction and favoring their diversification by providing new ecological niches, such as forest litter and arboreal nesting sites, and additional resources. We also hypothesize that the decline and extinction of stem ants during the Late Cretaceous was due to their hyper-specialized morphology, which limited their ability to expand their dietary niche in changing environments. This study highlights the importance of a holistic approach when studying the interplay between past environments and the evolutionary trajectories of organisms.
... So, the evidence of fossil spiny palms from the latest Maastrichtian-earliest Danian sediments of the Deccan Intertrappean beds of Madhya Pradesh may be a rough measure of the former distribution and predation intensity of large herbivores that are now extinct. We assume these large herbivores might have been dinosaurs and not mammals because Late Cretaceous mammals tend to be much smaller than those that exist today, or in the early Cenozoic (Grossnickle et al., 2019). Based on evidence from the western USA, it seems that it was only after the K-Pg that mammal body mass began to exceed 50 kg (Lyson et al., 2019). ...
... Placental mammals radiated after the end-Cretaceous mass extinction 66 Mya, rapidly increasing in size and evolving an incredible diversity of ecologies (Davies et al. 2017, Grossnickle et al. 2019, Halliday et al. 2019, Lyson et al. 2019, Benevento et al. 2023. A potentially critical, yet nearly unstudied, component of this diversification is the ribless lumbar region of the spine that forms a unique structural connection between the ribcage and pelvis not found in most non-mammalian vertebrates (Slijper 1946). ...
After the end-Cretaceous mass extinction, placental mammals rapidly diversified in size and locomotor mode, setting the stage for mammals to move into almost every habitat on Earth. Locomotion in extant mammals includes unique sagittal flexion of the trunk primarily driven by lumbar vertebrae, a ribless region of the spine. Consequently, variation in lumbar morphology is associated with a wide variety of locomotor styles. While the origin of this region in early therian mammals in the Mesozoic has been studied, along the therian stem, the later functional diversification of lumbar morphology in placental mammals, the dominant extant group, has been essentially unstudied. We measured the shape of lumbar vertebrae from early placental mammals to test how body size, locomotor specialization, and phylogeny interacted in the diversification of lumbar function after the end-Cretaceous mass extinction. We used 3D geometric morphometrics to quantify shape and compare variation in these Paleogene mammals to modern. We found that Paleogene mammals had high disparity in lumbar morphology and that this variation correlated with size and locomotor style. Surprisingly, several “archaic” placentals, like hyaenodontids, showed highly mobile lumbar morphology. These findings show that lumbar vertebrae formed an important and evolvable functional unit at the beginning of the Cenozoic.
... The decoupling event of hearing and chewing apparatuses is well established based on the evidence of different evolutionary stages in early eutherians, evidenced by the discovery of the ossified MC and inner ear in Cokotherium 31 , the Meckelian sulcus for MC and middle ear in Ambolestes 30 , and the detached middle ear in Microtherulum (Fig. 5b). The evolution of chewing apparatuses involves several aspects, such as the evolution of tooth structure (increase in shearing and grinding function from triconodont to tribosphenic tooth, or increase in morphological complexity of multicusped tooth in allotherians) and the evolution of molar occlusion (e.g., anteriorly directed occlusion in cladotherians and posteriorly directed occlusion in allotherians) 62,64,65 . Adaptation for efficient chewing has been proposed as the underlying mechanism for the decoupling event 20,25 , and allotherians represent the earliest clade to evolve DME in the Middle-Late Jurassic 9,20,23 . ...
The middle ear ossicles in modern mammals are repurposed from postdentary bones in non-mammalian cynodonts. Recent discoveries by palaeontological and embryonic studies have developed different models for the middle ear evolution in mammaliaforms. However, little is known about the evolutionary scenario of the middle ear in early therians. Here we report a detached middle ear preserved in a new eutherian mammal from the Early Cretaceous Jehol Biota. The well-preserved articulation of the malleus and incus suggest that the saddle-shaped incudomallear joint is a major apomorphy of Early Cretaceous eutherians. By contrast to the distinct saddle-like incudomallear articulation in therians, differences between the overlapping versus the half-overlapping incudomallear joints in monotremes and stem mammals would be relatively minor. The middle ear belongs to the microtype by definition, indicating its adaptation to high-frequency hearing. Current evidence indicates that significant evolutionary innovations of the middle ear in modern therians evolved in Early Cretaceous.
... this function has not been explored in the fossil record (Boszczyk et al., 2001;Gambaryan, 1974;Slijper, 1946). Placental mammals, the dominant extant group, first experienced a major radiation after the end Cretaceous mass extinction as they rapidly increased in size and diversified into new niches (Alroy, 1999;Grossnickle et al., 2019). This radiation included first appearances of many crown orders, but the first placental mammals to reach large size belonged to "archaic" groups, such as the carnivorous creodonts. ...
The unique morphology of mammalian lumbar vertebrae allows the spine to flex and extend in the sagittal plane during locomotion. This movement increases stride length and allows mammals to efficiently breathe while running with an asymmetric gait. In extant mammals, the amount of flexion that occurs varies across different locomotor styles, with dorsostable runners relying more on movement of long limbs to run and dorsomobile runners incorporating more flexion of the back. Although long limbs and a stabilized lumbar region are commonly associated with each other in extant mammals, many "archaic" placental mammals with short limbs had lumbar vertebrae with rev-olute zygapophyses. These articulations with an interlocking S-shape are found only in artiodactyls among extant mammals and have been hypothesized to stabilize against flexion of the back. This would suggest that archaic placental mammals may not have incorporated dorsoventral flexion into locomotion to the same extent as extant mammals with similar proportions. We tested the relative mobility of fossil lumbar vertebrae from two early placental mammals, the creodonts Patriofelis and Limnocyon, to see how these vertebrae may have functioned. We compared range of motion (ROM) between the original vertebrae , with revolute morphology and digitally altered vertebrae with a flat morphology. We found that the revolute morphology had relatively little effect on dorsoventral flexion and instead that it likely prevented disarticulation due to shear forces on the spine. These results show that flexion of the spine has been an important part of mammalian locomotion for at least 50 million years.
... However, the substantial interordinal and intraordinal diversification of crown mammals occurred in Middle-Late Jurassic and Late Cretaceous (Fig. 5), representing a delayed early burst model (Close et al., 2015), implying the existence of enormous ghost lineages of crown mammals in the Early Jurassic. The ecological diversity of mammaliaforms displayed a burst led primarily by stem groups in Early Jurassic, increased during Middle-Late Jurassic and maintained in Early Cretaceous (Close et al., 2015;Grossnickle and Polly, 2013;Grossnickle et al., 2019), as spectacularly illustrated by the Yanliao and Jehol biotas. This pattern may have been influenced by the breakup of Pangea and the key anatomical or physiological innovations in mammal lineages as they responded to changing environments (Close et al., 2015). ...
... Only a small fraction of the more complex macroevolutionary changes will succeed, but those that do can be the found ers of novel taxa displaying major adaptive innovations. Taxonomic and adaptive radiations after mass extinctions indicate that there is no single outcome for successful ecologically-triggered macroevolutionary changes (Ezcurra & Butler, 2018;Grossnickle, Smith, & Wilson, 2019;Magallón, Sánchez-Reyes, & Gómez-Acevedo, 2019;Soltis & Soltis, 2014). The survivors that give rise to major lineages must provide a novel basis for ongoing adaptive changes. ...
A unique exploration of teleonomy—also known as “evolved purposiveness”—as a major influence in evolution by a broad range of specialists in biology and the philosophy of science.
The evolved purposiveness of living systems, termed “teleonomy” by chronobiologist Colin Pittendrigh, has been both a major outcome and causal factor in the history of life on Earth. Many theorists have appreciated this over the years, going back to Lamarck and even Darwin in the nineteenth century. In the mid-twentieth century, however, the complex, dynamic process of evolution was simplified into the one-way, bottom-up, single gene-centered paradigm widely known as the modern synthesis. In Evolution “On Purpose,” edited by Peter A. Corning, Stuart A. Kauffman, Denis Noble, James A. Shapiro, Richard I. Vane-Wright, and Addy Pross, some twenty theorists attempt to modify this reductive approach by exploring in depth the different ways in which living systems have themselves shaped the course of evolution.
Evolution “On Purpose” puts forward a more inclusive theoretical synthesis that goes far beyond the underlying principles and assumptions of the modern synthesis to accommodate work since the 1950s in molecular genetics, developmental biology, epigenetic inheritance, genomics, multilevel selection, niche construction, physiology, behavior, biosemiotics, chemical reaction theory, and other fields. In the view of the authors, active biological processes are responsible for the direction and the rate of evolution. Essays in this collection grapple with topics from the two-way “read-write” genome to cognition and decision-making in plants to the niche-construction activities of many organisms to the self-making evolution of humankind. As this collection compellingly shows, and as bacterial geneticist James Shapiro emphasizes, “The capacity of living organisms to alter their own heredity is undeniable.”
... The Cretaceous-Paleogene (K-Pg) mass extinction 66 million years ago (Ma) is a pivotal event in evolutionary history, resulting in the formation of the mammalian-dominated terrestrial ecosystems present today (Simpson, 1937). The Paleocene biotic recovery of mammals transitioned into an evolutionary radiation, particularly of placentals (but see dos Reis et al., 2014 for discussion of molecular evidence suggesting a latest Cretaceous radiation for placental mammals), associated with increases in body mass (Alroy, 1999;Smith et al., 2010;Wilson, 2013), taxonomic richness (Lillegraven, 1972;Maas & Krause, 1994;Wilson, 2014;Wilson et al., 2021), and ecological disparity (Chen et al., 2019;Grossnickle & Newham, 2016;Grossnickle et al., 2019;Halliday & Goswami, 2016;Wilson, 2013). This important interval in mammalian history has been studied using a variety of taxonomic and, to a lesser extent, ecological proxies (e.g., Archibald, 1983;DeBey & Wilson, 2014;DeBey & Wilson, 2017;Lillegraven & Eberle, 1999;Lyson et al., 2019;Maas & Krause, 1994;Smith et al., 2018;Wilson, 2013Wilson, , 2014. ...
... Estimated ancestral compositions are . Given that mammals originated before fleshy fruit plants (Eriksson 2016), this suggests that ancestral mammals were generalist invertebrate feeders, which is consistent with the current hypothesis, based on the fossil record and ancestral diet reconstruction, of a generalist insectivorous diet in early mammals (Gill et al. 2014;Grossnickle et al. 2019). We found the gut microbiota composition of modern birds to be only weakly structured by diet compared with that of mammals, making the inferred ancestral microbiota composition of birds less informative in this respect (no strong clustering in the PCA plots; PermANOVA testing the effect of diet: R 2 ∼0.03, p < 0.001, in birds vs. . ...
How host-associated microbial communities evolve as their hosts diversify remains equivocal: How conserved is their composition? What was the composition of ancestral microbiota? Do microbial taxa covary in abundance over millions of years? Multivariate phylogenetic models of trait evolution are key to answering similar questions for complex host phenotypes, yet they are not directly applicable to relative abundances, which usually characterize microbiota. Here, we extend these models in this context, thereby providing a powerful approach for estimating phylosymbiosis (the extent to which closely related host species harbor similar microbiota), ancestral microbiota composition, and integration (evolutionary covariations in bacterial abundances). We apply our model to the gut microbiota of mammals and birds. We find significant phylosymbiosis that is not entirely explained by diet and geographic location, indicating that other evolutionary-conserved traits shape microbiota composition. We identify main shifts in microbiota composition during the evolution of the two groups and infer an ancestral mammalian microbiota consistent with an insectivorous diet. We also find remarkably consistent evolutionary covariations among bacterial orders in mammals and birds. Surprisingly, despite the substantial variability of present-day gut microbiota, some aspects of their composition are conserved over millions of years of host evolutionary history.
... Similarly, early mammaliaforms survived the Triassic-Jurassic mass extinction, and therians 285 survived the KTR and K-Pg mass extinction(Grossnickle et al. 2019). In each case, the opening 286 of ecological niche space through the removal of previous incumbents seems to be the key step 287 in beginning the subsequent diversification. ...
Evolutionary radiations generate most of Earth’s biodiversity, but are there common ecomorphological traits among the progenitors of radiations? In Synapsida (mammalian total group), ‘small-bodied faunivore’ has been hypothesized as the ancestral state of most major radiating clades, but this has not been quantitatively assessed across multiple radiations. To examine macroevolutionary patterns in a phylogenetic context, we generated a time-calibrated meta-phylogeny (‘metatree’) comprising 2,128 synapsid species from the Carboniferous through the Eocene (305–34 Ma), based on 270 published character matrices. We used comparative methods to investigate body size and dietary evolution during successive synapsid radiations. Faunivory is the ancestral diet of each major synapsid radiation, but small body size is only established as the common ancestral state of radiations near the origin of Mammaliaformes in the Late Triassic. The faunivorous ancestors of synapsid radiations typically have numerous novel characters compared to their contemporaries, and these derived traits may have helped them to survive faunal turnover events and subsequently radiate.
... This is because while these taxa all exhibit the same positive shift in their Cretaceous δ 13 C bioapatite samples as is observed in the dinosaurs, they do not exhibit the same pattern in their δ 13 C bioapatite in the modern subtropical coastal plain, where the δ 13 C diet of all of these modern taxa falls within C 3 ranges (Fig. 2C). These taxa are also not exclusively aquatic or faunivorous, as small Late Cretaceous terrestrial mammals are reconstructed as having a range of omnivorous to herbivorous diets (Grossnickle et al. 2019), relatively similar to the small omnivorous mammals sampled from the modern system. ...
Biogeochemical analyses of organisms’ tissues provide direct proxies for diets, behaviors, and environmental interactions that have proven invaluable for studies of extant and extinct species. Applying these to Cretaceous ecosystems has at times produced anomalous results, however, as dinosaurs preserve unusually positive stable carbon isotope compositions relative to extant C 3 -feeding vertebrates. This has been hypothesized to be a unique property of dinosaur dietary physiology, with potential significance for our interpretations of their paleobiology. We test that hypothesis through multi-taxic stable carbon isotope analyses of a spatiotemporally constrained locality in the Late Cretaceous of Canada, and compare the results to a modern near-analogue environment in Louisiana. The stable carbon isotope anomaly is present in all sampled fossil vertebrates, dinosaur or not. This suggests another more widespread factor is responsible. Examinations of diagenetic effects suggest that, where present, they are insufficient to explain the isotope anomaly. The isotope anomaly is therefore not primarily the result of a unique dietary physiology of dinosaurs, but rather a mix of factors impacting all taxa, such as environmental and/or source-diet differences. Our study underscores the importance of multi-taxic samples from spatiotemporally constrained localities in testing hypotheses of extinct organisms and ecosystems, and in the use of modern data to “ground truth” when evaluating analogue versus non-analogue conditions in greenhouse paleoecosystems.
Mass extinctions are natural experiments on the short- and long-term consequences of pushing biotas past breaking points, often with lasting effects on the structure and function of biodiversity. General properties of mass extinctions—exceptionally severe, taxonomically broad, global losses of taxa—are starting to come into focus through comparisons among dimensions of biodiversity, including morphological, functional, and phylogenetic diversity. Notably, functional diversity tends to persist despite severe losses of taxonomic diversity, whereas taxic and morphological losses may or may not be coupled. One of the biggest challenges in synthesizing and extracting general consequences of these events has been that they are often driven by multiple, interacting pressures, and the taxa and their traits vary among events, making it difficult to link single stressors to specific traits. Ongoing improvements in the taxonomic and stratigraphic resolution of these events for multiple clades will sharpen tests for selectivity and help to isolate hitchhiking effects, whereby organismal traits are carried by differential survival or extinction of taxa owing to other organismal or higher-level attributes, such as geographic-range size. Direct comparative analyses across multiple extinction events will also clarify the impacts of particular drivers on taxa, functional traits, and morphologies. It is not just the extinction filter that deserves attention, as the longer-term impact of extinctions derives in part from their ensuing rebounds. More work is needed to uncover the biotic and abiotic circumstances that spur some clades into re-diversification while relegating others to marginal shares of biodiversity. Combined insights from mass extinction filters and their rebounds bring a macroevolutionary view to approaching the biodiversity crisis in the Anthropocene, helping to pinpoint the clades, functional groups, and morphologies most vulnerable to extinction and failed rebounds.
Many endotherms from diverse taxonomic groups can respond to environmental changes through torpor, that is, by greatly reducing their energy expenditure for up to 24 hours (daily torpor) or longer (hibernation). We currently have a poor understanding of how torpor evolved across endotherms and its associations with physiological traits and ecological factors.
To fill this gap, we thoroughly examine the evolutionary patterns of torpor and its links with 21 key physiological and ecological variables across 1338 extant endotherms.
We find that daily torpor and hibernation are parts of an evolutionary torpor continuum, and that there are several, albeit weak, associations between torpor and species' physiological or environmental characteristics. Furthermore, we show that early endotherm ancestors likely did not hibernate and that this trait evolved multiple times in independent lineages.
Overall, our results suggest that the remarkable variation in torpor patterns across extant endotherms cannot solely be attributed to environmental niches, but partly arises from independent gains of daily torpor and hibernation in various clades.
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Following the end-Cretaceous mass extinction, mammals underwent an increase in body size, taxonomic diversity and ecological specialization throughout the Paleocene, exemplifying their adaptability. One especially enigmatic group is the “Triisodontidae”, medium- to large-sized ungulate-like placentals from the Paleocene which are best known from their teeth that exhibit adaptations towards carnivory. The “triisodontids” were the first large carnivorous mammals and pre-date, and may have given rise to, Mesonychia, a group of more specialized placental carnivores. The “triisodontids” have been well-described from dental material, although very little is known about their postcrania. Here, we describe the postcrania of Triisodon crassicuspis–the most completely represented species of the genus to date–from a specimen (NMMNH P-72096) recovered from basal Torrejonian strata of the Nacimiento Formation in the San Juan Basin, New Mexico. Anatomical comparisons reveal that the forelimb long bones of Tri. crassicuspis are robust relative to its size, more so than other “triisodontids”. Attachment sites on the ulna are evidence of well-developed muscles involved in powerful extension and flexion of the manus. In Tri. crassicuspis, the range of pronation-supination was limited as evident from the humeroradial morphology. Qualitative functional assessment of osteological features of the forelimb of Tri. crassicuspis is suggestive of terrestrial locomotion with at least moderate digging ability. Re-analyses of the dentition confirmed that Tri. crassicuspis had specializations for carnivory, and provide a body mass estimate of ca. 32–44 kg based on dental proxies. In summary, Tri. crassicuspis was a relatively large and powerful terrestrial animal, and one of the first known placentals to fill a largely carnivorous niche.
Large igneous provinces erupt highly reactive, predominantly basaltic lavas onto Earth’s surface, which should boost the weathering flux leading to long-term CO2 drawdown and cooling following cessation of volcanism. However, throughout Earth’s geological history, the aftermaths of multiple Phanerozoic large igneous provinces are marked by unexpectedly protracted climatic warming and delayed biotic recovery lasting millions of years beyond the most voluminous phases of extrusive volcanism. Here we conduct geodynamic modelling of mantle melting and thermomechanical modelling of magma transport to show that rheologic feedbacks in the crust can throttle eruption rates despite continued melt generation and CO2 supply. Our results demonstrate how the mantle-derived flux of CO2 to the atmosphere during large igneous provinces can decouple from rates of surface volcanism, representing an important flux driving long-term climate. Climate–biogeochemical modelling spanning intervals with temporally calibrated palaeoclimate data further shows how accounting for this non-eruptive cryptic CO2 can help reconcile the life cycle of large igneous provinces with climate disruption and recovery during the Permian–Triassic, Mid-Miocene and other critical moments in Earth’s climate history. These findings underscore the key role that outgassing from intrusive magmas plays in modulating our planet’s surface environment.
Los mamíferos modernos, surgidos a partir del grupo Synapsida hace 323 millones de años, presentan una gran diversidad morfológica, ecológica y evolutiva. La comprensión de la historia evolutiva de este grupo es vital, pero también representa un gran reto debido al carácter gradual de su evolución y por la presencia de convergencias evolutivas. En el presente escrito se presenta una breve síntesis del panorama general del origen y la evolución de los mamíferos modernos.
The nasal cavity of living mammals is a unique structural complex among tetrapods, acquired along a series of major morphological transformations that occurred mainly during the Mesozoic Era, within the Synapsida clade. Particularly, non-mammaliaform cynodonts document several morphological changes in the skull, during the Triassic Period, that represent the first steps of the mammalian bauplan. We here explore the nasal cavity of five cynodont taxa, namely Thrinaxodon, Chiniquodon, Prozostrodon, Riograndia, and Brasilodon, in order to discuss the main changes within this skull region. We did not identify ossified turbinals in the nasal cavity of these taxa and if present, as non-ossified structures, they would not necessarily be associated with temperature control or the development of endothermy. We do, however, notice a complexification of the cartilage anchoring structures that divide the nasal cavity and separate it from the brain region in these forerunners of mammals.
The evolutionary histories of major clades, including mammals, often comprise changes in their diversification dynamics, but how these changes occur remains debated. We combined comprehensive phylogenetic and fossil information in a new “birth-death diffusion” model that provides a detailed characterization of variation in diversification rates in mammals. We found an early rising and sustained diversification scenario, wherein speciation rates increased before and during the Cretaceous-Paleogene (K-Pg) boundary. The K-Pg mass extinction event filtered out more slowly speciating lineages and was followed by a subsequent slowing in speciation rates rather than rebounds. These dynamics arose from an imbalanced speciation process, with separate lineages giving rise to many, less speciation-prone descendants. Diversity seems to have been brought about by these isolated, fast-speciating lineages, rather than by a few punctuated innovations.
Adaptive radiations are bursts in biodiversity that generate new evolutionary lineages and phenotypes. However, because they typically occur over millions of years, it is unclear how their macroevolutionary dynamics vary through time and among groups of organisms. Phyllostomid bats radiated extensively for diverse diets—from insects to vertebrates, fruit, nectar, and blood—and we use their molars as a model system to examine the dynamics of adaptive radiations. Three-dimensional shape analyses of lower molars of Noctilionoidea (Phyllostomidae and close relatives) indicate that different diet groups exhibit distinct morphotypes. Comparative analyses further reveal that phyllostomids are a striking example of a hierarchical radiation; phyllostomids’ initial, higher-level diversification involved an “early burst” in molar morphological disparity as lineages invaded new diet-affiliated adaptive zones, followed by subsequent lower-level diversifications within adaptive zones involving less dramatic morphological changes. We posit that strong selective pressures related to initial shifts to derived diets may have freed molars from morpho-functional constraints associated with the ancestral molar morphotype. Then, lineages with derived diets (frugivores and nectarivores) diversified within broad adaptive zones, likely reflecting finer-scale niche partitioning. Importantly, the observed early burst pattern is only evident when examining molar traits that are strongly linked to diet, highlighting the value of ecomorphological traits in comparative studies. Our results support the hypothesis that adaptive radiations are commonly hierarchical and involve different tempos and modes at different phylogenetic levels, with early bursts being more common at higher levels.
The mammalian crown originated during the Mesozoic and subsequently radiated into the substantial array of forms now extant. However, for about 100 million years before the crown's origin, a diverse array of stem mammalian lineages dominated terrestrial ecosystems. Several of these stem lineages overlapped temporally and geographically with the crown mammals during the Mesozoic, but by the end of the Cretaceous crown mammals make up the overwhelming majority of the fossil record. The progress of this transition between ecosystems dominated by stem mammals and those dominated by crown mammals is not entirely clear, in part due to a distinct separation of analyses and datasets. Analyses of macroevolutionary patterns tend to focus on either the Mammaliaformes or the non-mammalian cynodonts, with little overlap in the datasets, preventing direct comparison of the diversification trends. Here I analyse species richness and biogeography of Synapsida as a whole during the Mesozoic, allowing comparison of the patterns in the mammalian crown and stem within a single framework. The analysis reveals the decline of the stem mammals occurred in two discrete phases. The first phase occurred between the Triassic and Middle Jurassic, during which the stem mammals were more restricted in their geographic range than the crown mammals, although within localities their species richness remained at levels seen previously. The second phase was a decline in species richness, which occurred during the Lower Cretaceous. The results show the decline of stem mammals, including tritylodontids and several mammaliaform groups, was not tied to a specific event, nor a gradual decline, but was instead a multiphase transition.
Theria represent an extant clade that comprises placental and marsupial mammals. Here we report on the discovery of a new Late Cretaceous mammal from southern Patagonia, Patagomaia chainko gen. et sp. nov., represented by hindlimb and pelvic elements with unambiguous therian features. We estimate Patagomaia chainko attained a body mass of 14 kg, which is considerably greater than the 5 kg maximum body mass of coeval Laurasian therians. This new discovery demonstrates that Gondwanan therian mammals acquired large body size by the Late Cretaceous, preceding their Laurasian relatives, which remained small-bodied until the beginning of the Cenozoic. Patagomaia supports the view that the Southern Hemisphere was a cradle for the evolution of modern mammalian clades, alongside non-therian extinct groups such as meridiolestidans, gondwanatherians and monotremes.
Vertebrate‐mediated seed dispersal is a common attribute of many living plants, and variation in the size and abundance of fleshy diaspores is influenced by regional climate and by the nature of vertebrate seed dispersers among present‐day floras. However, potential drivers of large‐scale variation in the abundance and size distributions of fleshy diaspores through geological time, and the importance of geographic variation, are incompletely known. This knowledge gap is important because fleshy diaspores are a key mechanism of energy transfer from photosynthesis to animals and may in part explain the diversification of major groups within birds and mammals. Various hypotheses have been proposed to explain variation in the abundance and size distribution of fleshy diaspores through time, including plant–frugivore co‐evolution, angiosperm diversification, and changes in vegetational structure and climate. We present a new data set of more than 800 georeferenced fossil diaspore occurrences spanning the Triassic–Oligocene, across low to mid‐ to high palaeolatitudes. We use this to quantify patterns of long‐term change in fleshy diaspores, examining the timing and geographical context of important shifts as a test of the potential evolutionary and climatic explanations. We find that the fleshy fruit sizes of angiosperms increased for much of the Cretaceous, during the early diversification of angiosperms from herbaceous ancestors with small fruits. Nevertheless, this did not cause a substantial net change in the fleshy diaspore size distributions across seed plants, because gymnosperms had achieved a similar size distribution by at least the Late Triassic. Furthermore, gymnosperm‐dominated Mesozoic ecosystems were mostly open, and harboured low proportions of specialised frugivores until the latest Cretaceous, suggesting that changes in vegetation structure and plant–frugivore co‐evolution were probably not important drivers of fleshy diaspore size distributions over long timescales. Instead, fleshy diaspore size distributions may be largely constrained by physical or life‐history limits that are shared among groups and diversify as a plant group expands into different growth forms/sizes, habitats, and climate regimes. Mesozoic gymnosperm floras had a low abundance of fleshy diaspores (<50% fleshy diaspore taxa), that was surpassed by some low‐latitude angiosperm floras in the Cretaceous. Eocene angiosperm floras show a mid‐ to high latitude peak in fleshy fruit abundance, with very high proportions of fleshy fruits that even exceed those seen at low latitudes both in the Eocene and today. Mid‐ to high latitude proportions of fleshy fruits declined substantially over the Eocene–Oligocene transition, resulting in a shift to more modern‐like geographic distributions with the highest proportion of fleshy fruits occurring in low‐latitude tropical assemblages. This shift was coincident with global cooling and the onset of Southern Hemisphere glaciation, suggesting that rapid cooling at mid‐ and high latitudes caused a decrease in availability of the climate conditions most favourable for fleshy fruits in angiosperms. Future research could be focused on examining the environmental niches of modern fleshy fruits, and the potential effects of climate change on fleshy fruit and frugivore diversity.
The evolution and biodiversity of ageing have long fascinated scientists and the public alike. While mammals, including long‐lived species such as humans, show a marked ageing process, some species of reptiles and amphibians exhibit very slow and even the absence of ageing phenotypes. How can reptiles and other vertebrates age slower than mammals? Herein, I propose that evolving during the rule of the dinosaurs left a lasting legacy in mammals. For over 100 million years when dinosaurs were the dominant predators, mammals were generally small, nocturnal, and short‐lived. My hypothesis is that such a long evolutionary pressure on early mammals for rapid reproduction led to the loss or inactivation of genes and pathways associated with long life. I call this the ‘longevity bottleneck hypothesis’, which is further supported by the absence in mammals of regenerative traits. Although mammals, such as humans, can evolve long lifespans, they do so under constraints dating to the dinosaur era.
The significant extinctions in Earth history have largely been unpredictable in terms of what species perish and what traits make species susceptible. The extinctions occurring during the late Pleistocene are unusual in this regard, because they were strongly size-selective and targeted exclusively large-bodied animals (i.e., megafauna, >1 ton) and disproportionately, large-bodied herbivores. Because these animals are also at particular risk today, the aftermath of the late Pleistocene extinctions can provide insights into how the loss or decline of contemporary large-bodied animals may influence ecosystems. Here, we review the ecological consequences of the late Pleistocene extinctions on major aspects of the environment, on communities and ecosystems, as well as on the diet, distribution and behavior of surviving mammals. We find the consequences of the loss of megafauna were pervasive and left legacies detectable in all parts of the Earth system. Furthermore, we find that the ecological roles that extinct and modern megafauna play in the Earth system are not replicated by smaller-bodied animals. Our review highlights the important perspectives that paleoecology can provide for modern conservation efforts.
In molars without permanent eruption, wear deeply modifies the geometry of the crown. To test for a signature of diet on wear dynamics, the molar geometry was compared between commensal house mice, relying on an omnivorous-granivorous diet, and Sub-Antarctic relatives, characterized by a switch towards a more ‘predatory’ behaviour. Laboratory-bred offspring of commensal mice served as a reference by providing mice of known age. Molar geometry was quantified using dense 3D semi-landmark based descriptors of the whole molar row and the upper molar only.
Laboratory offspring displayed a decreased rate of wear compared to their commensal relatives, due to reduced mastication in mice fed ad libitum. Sub-Antarctic mice displayed a similarly decreased rate of molar wear, in agreement with an optimization towards incisor biting to seize prey. Laboratory offspring and Sub-Antarctic mice were further characterized by straight molar rows, whereas in commensal mice, the erupting third molar deviated away from the longitudinal alignment with the other molars, due to masticatory loadings.
Quantifying changes in molar geometry could thus contribute to trace subtle diet variations, and provide a direct insight into the constraints during mastication, shedding light on the functional role of adaptive changes in molar geometry.
A prominent hypothesis in the diversification of placental mammals after the Cretaceous–Palaeogene (K/Pg) boundary suggests that the extinction of non‐avian dinosaurs resulted in the ecological release of mammals, which were previously constrained to small body sizes and limited species richness. This ‘dinosaur incumbency hypothesis’ may therefore explain increases in mammalian diversity via expansion into larger body size niches, that were previously occupied by dinosaurs, but does not directly predict increases in other body size classes. To evaluate this, we estimate sampling‐standardized diversity patterns of terrestrial North American fossil mammals within body size classes, during the Cretaceous and Palaeogene. We find strong evidence for post‐extinction diversity increases in all size classes. Increases in the diversity of small‐bodied species (less than 100 g, the common body size class of Cretaceous mammals, and much smaller than the smallest non‐avialan dinosaurs ( c . 400 g)) were similar to those of larger species. We propose that small‐bodied mammals had access to greater energetic resources or were able to partition resources more finely after the K/Pg mass extinction. This is likely to be the result of a combination of widespread niche clearing due to the K/Pg mass extinctions, alongside a suite of biotic and abiotic changes that occurred during the Late Cretaceous and across the K/Pg boundary, such as shifting floral composition, and novel key innovations among eutherian mammals.
The growth of complexity is an unsolved and underappreciated problem. We consider possible causes of this growth, hypotheses testing, molecular mechanisms, complexity measures, cases of simplification, and significance for biomedicine. We focus on a general ability of regulation, which is based on the growing information storage and processing capacities, as the main proxy of complexity. Natural selection is indifferent to complexity. However, complexification can be inferred from the same first principle, on which natural selection is founded. Natural selection depends on potentially unlimited reproduction under limited environmental conditions. Because of the demographic pressure, the simple ecological niches become fulfilled and diversified (due to species splitting and divergence). Diversification increases complexity of biocenoses. After the filling and diversification of simple niches, the more complex niches can arise. This is the 'atomic orbitals' (AO) model. Complexity has many shortcomings but it has an advantage. This advantage is ability to regulatory adaptation, including behavioral, formed in the evolution by means of genetic adaptation. Regulatory adaptation is much faster than genetic one because it is based on the information previously accumulated via genetic adaptation and learning. Regulatory adaptation further increases complexity of biocenoses. This is the 'regulatory advantage' (RA) model. The comparison of both models allows testable predictions. We focus on the animal evolution because of the appearance of higher regulatory level (nervous system), which is absent in other lineages, and relevance to humans (including biomedical aspects).
Organisms primarily influence ecosystems through their functional traits when they are physically active. Following the nocturnal bottleneck, the expansion of mammals into the daytime expanded mammalian functional diversity (FD), however there is also notable overlap in trait space across diel niches leading to redundant FD. We explore how the unique and redundant contribution of each diel niche varies spatially and in relation to natural variation in light and temperature. Global. Extant mammals. Based on five major functional traits (body mass, litter size, diet breadth, foraging strata, habitat breadth) for 5033 extant terrestrial mammals, we determine biogeographical variation in nocturnal, crepuscular, cathemeral and diurnal FD. We calculate the proportion of mammalian FD that is unique to each diel niche, and the proportion that is redundant across the daily cycle. The diversification of mammals into the daytime resulted in the creation of new FD (28.5% of FD is not nocturnal; Lower Quartile 17.3%; Upper Quartile 38.2%). Most of this expansion occurred at higher latitudes where uniquely cathemeral FD dominates (>55°N, 41.1% of mammalian FD; Lower Quartile 33.3%, Upper Quartile 53.6%), associated with fewer hours of biologically useful moonlight and daylight. Where there are more hours of biologically useful daylight, unique diurnal FD is common. However, more than half of non‐nocturnal FD is redundant, increasing ecosystem stability as different species carry out similar functions at different times of day, and suggesting that many mammals have not diversified far from their nocturnal ancestors. Over much of the land surface more than a half of FD only occurs at night, underscoring the importance of nocturnal mammals for ecosystems. Understanding diel variation in FD not only informs on community structure and ecosystem function but also on ecosystem functional persistence in the Anthropocene, with pressures at night being particularly concerning.
Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals. Molecular data and the fossil record can give conflicting views of the evolutionary past. For instance, empirical palaeontological evidence by itself tends to favour the 'explosive model' of diversification for extant placental mammals 1 , in which the orders with living representatives both originated and rapidly diversified soon after the Cretaceous/Tertiary (K/T) mass extinction event that eliminated non-avian dinosaurs and many other, mostly marine 2 , taxa 65.5 million years (Myr) ago 1,3,4. By contrast, molecular data consistently push most origins of the same orders back into the Late Cretaceous period 5-9 , leading to alternative scenarios in which placental line-ages persist at low diversity for some period of time after their initial origins ('phylogenetic fuses'; see ref. 10) before undergoing evolutionary explosions 1,11. Principal among these scenarios is the 'long-fuse model' 1 , which postulates an extended lag between the Cretaceous origins of the orders and the first split among their living representatives (crown groups) immediately after the K/T boundary 8. Some older molecular studies advocate a 'short-fuse model' of diversification 1 , where even the basal crown-group divergences within some of the larger placental orders occur well within the Cretaceous period 5-7. A partial molecular phylogeny emphasizing divergences among placental orders suggested that over 20 lineages with extant descendants (henceforth, 'extant lineages') survived the K/T boundary 8. However, the total number of extant lineages that pre-date the extinction event and whether or not they radiated immediately after it remain unknown. The fossil record alone does not provide direct answers to these questions. It does reveal a strong pulse of diversification in stem eutherians immediately after the K/T boundary 4,12 , but few of the known Palaeocene taxa can be placed securely within the crown groups of extant orders comprising Placentalia 4. The latter only rise to prominence in fossils known from the Early Eocene epoch onwards (,50 Myr ago) after a major faunal reorganization 4,13,14. The geographical patchiness of the record complicates interpretations of this near-absence of Palaeocene crown-group fossils 14-16 : were these clades radiating throughout the Palaeocene epoch in parts of the world where the fossil record is less well known; had they not yet originated; or did they have very long fuses, remaining at low diversity until the major turnover at the start of the Eocene epoch? The pattern of diversification rates through time, to which little attention has been paid so far, might hold the key to answering these questions. If the Cretaceous fauna inhibited mammalian diversification , as is commonly assumed 1 , and all mammalian lineages were able to radiate after their extinction, then there should be a significant increase in the net per-lineage rate of extant mammalian diversification , r (the difference between the per-lineage speciation and extinction rates), immediately after the K/T mass extinction. This hypothesis, along with the explosive, long-and short-fuse models, can be tested using densely sampled phylogenies of extant species, which contain information about the history of their diversification rates 17-20. Using modern supertree algorithms 21,22 , we construct the first virtually complete species-level phylogeny of extant mammals from over 2,500 partial estimates, and estimate divergence times (with confidence intervals) throughout it using a 66-gene alignment in conjunction with 30 cladistically robust fossil calibration points. Our analyses of the supertree indicate that the principal splits underlying the diversification of the extant lineages occurred (1) from 100-85 Myr ago with the origins of the extant orders, and (2) in or after the Early Eocene (agreeing with the upturn in their diversity known from the fossil record 4,13,14), but not immediately after the K/T boundary, where diversification rates are unchanged. Our findings-that more extant placental lineages survived the K/T boundary than previously recognized and that fewer arose immediately after it than previously suspected-extend the phylogenetic fuses of many extant orders and indicate that the end-Cretaceous mass extinction event had, at best, a minor role in driving the diversification of the present-day mam-malian lineages. A supertree with divergence times for extant mammals The supertree contains 4,510 of the 4,554 extant species recorded in ref. 23, making it 99.0% complete at the species level (Fig. 1; see also
The radiation of mammals after the Cretaceous/Palaeogene (K/Pg) boundary was a major event in the evolution of terrestrial ecosystems. Multiple studies point to increases in maximum body size and body size disparity, but patterns of disparity for other traits are less clear owing to a focus on different indices and subclades. We conducted an inclusive comparison of jaw functional disparity from the Early Jurassic-latest Eocene, using six mechanically relevant mandibular ratios for 256 species representing all major groups. Jaw functional disparity across all mammals was low throughout much of the Mesozoic and remained low across the K/Pg boundary. Nevertheless, the K/Pg boundary was characterized by a pronounced pattern of turnover and replacement, entailing a substantial reduction of non-therian and stem-therian disparity, alongside a marked increase in that of therians. Total mammal disparity exceeded its Mesozoic maximum for the first time during the Eocene, when therian mammals began exploring previously unoccupied regions of function space. This delay in the rise of jaw functional disparity until the Eocene probably reflects the duration of evolutionary recovery after the K/Pg mass extinction event. This contrasts with the more rapid expansion of maximum body size, which occurred in the Palaeocene.
Resolving the timing and pattern of early placental mammal evolution has been confounded by conflict among divergence date estimates from interpretation of the fossil record and from molecular-clock dating studies. Despite both fossil occurrences and molecular sequences favouring a Cretaceous origin for Placentalia, no unambiguous Cretaceous placental mammal has been discovered. Investigating the differing patterns of evolution in morphological and molecular data reveals a possible explanation for this conflict. Here, we quantified the relationship between morphological and molecular rates of evolution. We show that, independent of divergence dates, morphological rates of evolution were slow relative to molecular evolution during the initial divergence of Placentalia, but substantially increased during the origination of the extant orders. The rapid radiation of placentals into a highly morphologically disparate Cenozoic fauna is thus not associated with the origin of Placentalia, but post-dates superordinal origins. These findings predict that early members of major placental groups may not be easily distinguishable from one another or from stem eutherians on the basis of skeleto-dental morphology. This result supports a Late Cretaceous origin of crown placentals with an ordinal-level adaptive radiation in the early Paleocene, with the high relative rate permitting rapid anatomical change without requiring unreasonably fast molecular evolutionary rates. The lack of definitive Cretaceous placental mammals may be a result of morphological similarity among stem and early crown eutherians, providing an avenue for reconciling the fossil record with molecular divergence estimates for Placentalia.
We here establish a new mammaliaform genus and species, Galulatherium jenkinsi (Mammalia), from the Upper
Cretaceous Galula Formation in the Rukwa Rift Basin of southwestern Tanzania. This represents the first named
taxon of a mammaliaform from the entire Late Cretaceous of continental Afro-Arabia, an interval of 34 million years.
Preliminary study of the holotypic and only known specimen (a partial dentary) resulted in tentative assignation to the
Gondwanatheria, a poorly known, enigmatic clade of Late Cretaceous–Paleogene Gondwanan mammals (Krause et al.
2003). The application of advanced imaging (μCT) and visualization techniques permits a more detailed understanding
of key anatomical features of the new taxon. It reveals that the lower dentition consisted of a large, procumbent lower
incisor and four cheek teeth, all of which were evergrowing (hypselodont). Importantly, all of the teeth appear devoid
of enamel. Comparisons conducted with a range of Mesozoic and selected Cenozoic mammaliaform groups document
a number of features (e.g., columnar, enamel-less and evergrowing teeth, with relatively simple occlusal morphology)
expressed in Galulatherium that are reminiscent of several distantly related groups, making taxonomic assignment
difficult at this time. Herein we retain the provisional referral of Galulatherium (RRBP 02067) to Gondwanatheria; it is
most similar to sudamericids such as Lavanify and Bharratherium from the Late Cretaceous of Madagascar and India,
respectively, in exhibiting relatively simple, high-crowned, columnar cheek teeth. Other features (e.g., enamel-less dentition)
are shared with disparate forms such as the Late Jurassic Fruitafossor and toothed xenarthrans (e.g., sloths), here
attributed to convergence. Revised analyses of the depositional context for the holotype place it as having lived sometime
between the late Turonian and latest Campanian (roughly 91–72 million years ago). This enhanced geochronological
context helps to refine the palaeobiogeographical significance of Galulatherium among Cretaceous mammals in general
and those from Gondwanan landmasses specifically.
The fossil record provides one of the strongest tests of the hypothesis that diversity within local communities is constrained over geological timescales. Constraints to diversity are particularly controversial in modern terrestrial ecosystems, yet long-term patterns are poorly understood. Here we document patterns of local richness in Phanerozoic terrestrial tetrapods using a global data set comprising 145,332 taxon occurrences from 27,531 collections. We show that the local richness of non-flying terrestrial tetrapods has risen asymptotically since their initial colonization of land, increasing at most threefold over the last 300 million years. Statistical comparisons support phase-shift models, with most increases in local richness occurring: (1) during the colonization of land by vertebrates, concluding by the late Carboniferous; and (2) across the Cretaceous/Paleogene boundary. Individual groups, such as mammals, lepidosaurs and dinosaurs also experienced early increases followed by periods of stasis often lasting tens of millions of years. Mammal local richness abruptly tripled across the Cretaceous/Paleogene boundary, but did not increase over the next 66 million years. These patterns are consistent with the hypothesis that diversity is constrained at the local-community scale. © 2019, The Author(s), under exclusive licence to Springer Nature Limited.
Haramiyidans' are extinct mammaliaforms often clustered with Multituberculata as Allotheria, and with a fossil record extending from the Upper Triassic to possibly the Upper Cretaceous. For many decades, 'haramiyidans' were known only from isolated teeth, and their relationships to other mammaliaforms remain unclear. With the discovery of several euharamiyidans represented by skeletal specimens from the Jurassic Yanliao Biota, northwestern China, our knowledge of this group has significantly advanced. Nonetheless, much morphology, including dentition and occlusal patterns, has only been briefly described for most taxa, and phylogenetic reconstruction and interpretation of the biology of the group still remain unclear or controversial. Here we provide systematic descriptions of the dental wear of shenshouids (Qishou and Shenshou) from the Yanliao Biota. We reconstruct the occlusal mode of shenshouids and compare it with those of other taxa based on our observation of specimens of most known 'haramiyidan' taxa. Several occlusal patterns are recognized. In particular, that of Thomasia, Haramiyavia and Maiopatagium is similar to the multituberculate M1/m1 occlusal relationship and probably represents the primitive occlusal condition in 'haramiyidans'. The occlusal mode of shenshouids resembles the multituberculate M2/m2 occlu-sion. The double-engaged mode in Arboroharamiya and Vilevolodon, as well as that of Eleutherodon, represents a more advanced occlusal pattern. The diverse dental occlu-sions suggest diverse diet adaptations and resource partitioning from co-existing taxa in the Jurassic forests; they also reflect mosaic evolutionary transformations and complicated phylogenetic relationships within the group. Some aspects of the dental evolution remain challenging and require further vigorous testing.
The incorporation of stratigraphic data into phylogenetic analysis has a long history of debate, but is not currently standard practice for palaeontologists. Bayesian tip-dating (or morphological clock) phylogenetic methods have returned these arguments to the spotlight, but how tip-dating affects the recovery of evolutionary relationships has yet to be fully explored. Here we show, through analysis of several datasets with multiple phylogenetic methods, that topologies produced by tip-dating are outliers when compared to topologies produced by parsimony and undated Bayesian methods, which retrieve broadly similar trees. Unsurprisingly, trees recovered by tip-dating have better fit to stratigraphy than trees recovered by other methods, due to trees with better stratigraphic fit being assigned a higher prior probability. Differences in stratigraphic fit and tree topology between tip-dating and other methods appear to be concentrated in parts of the tree with weaker character signal and a stronger influence of the prior, as shown by successive deletion of the most incomplete taxa from a sauropod dataset. Tip-dating applied to Mesozoic mammals firmly rejects a monophyletic Allotheria, and strongly supports diphyly of haramiyidans, with the late Triassic Haramiyavia and Thomasia forming a clade with tritylodontids, which is distant from the middle Jurassic euharamiyidans. This result is not sensitive to the controversial age of the eutherian Juramaia. A Test of the age of Juramaia using a less restrictive prior reveals strong support from the data for an Early Cretaceous age. Our results suggest that tip-dating incorporates stratigraphic data in an intuitive way, with good stratigraphic fit a prior expectation that can be overturned by strong evidence from character data.
The uneven distribution of species in the tree of life is rooted in unequal speciation and extinction among groups. Yet the causes of differential diversification are little known despite their relevance for sustaining biodiversity into the future. Here we investigate rates of species diversification across extant Mammalia, a compelling system that includes our own closest relatives. We develop a new phylogeny of nearly all ~6000 species using a 31-gene supermatrix and fossil node- and tip-dating approaches to establish a robust evolutionary timescale for mammals. Our findings link the causes of uneven modern species richness with ecologically-driven variation in diversification rates, including 24 detected rate shifts. Speciation rates are a stronger predictor of among-clade richness than clade age, countering claims of clock-like speciation in large phylogenies. Surprisingly, rate heterogeneity in recent radiations shows limited association with latitude, despite the well-known richness increase toward the equator. Instead, we find a deeper-time association where clades of high-latitude species have the highest speciation rates, suggesting that species durations are shorter outside than inside the tropics. At shallower timescales (i.e., young clades), diurnality and low vagility are both linked to greater speciation rates and extant richness. High turnover among small-ranged allopatric species may erase the signal of vagility in older clades, while diurnality may adaptively reduce competition and extinction. These findings highlight the underappreciated joint roles of ephemeral (turnover-based) and adaptive (persistence-based) diversification processes, which manifest as speciation gradients in recent and more ancient radiations to explain the evolution of mammal diversity.
Phylogenies of mammals based on morphological data continue to show several major areas of conflict with the current consensus view of their relationships, which is based largely on molecular data. This raises doubts as to whether current morphological character sets are able to accurately resolve mammal relationships. We tested this under a hypothetical ‘best case scenario’ by using ancestral state reconstruction (under both maximum parsimony and maximum likelihood) to infer the morphologies of fossil ancestors for all clades present in a recent comprehensive DNA sequence-based phylogeny of mammals, and then seeing what effect the subsequent inclusion of these predicted ancestors had on unconstrained phylogenetic analyses of morphological data. We found that this resulted in topologies that are highly congruent with the current consensus phylogeny, at least when the predicted ancestors are assumed to be well preserved and densely sampled. Most strikingly, several analyses recovered the monophyly of clades that have never been found in previous morphology-only studies, such as Afrotheria and Laurasiatheria. Our results suggest that, at least in principle, improvements in the fossil record—specifically the discovery of fossil taxa that preserve the ancestral or near-ancestral morphologies of the nodes in the current consensus—may be sufficient to largely reconcile morphological and molecular estimates of mammal phylogeny, even using current morphological character sets.
Diel activity pattern (DAP) is a key aspect of an animal's ecology, but it is difficult to infer when behavior cannot be directly observed, as in the fossil record. Various anatomical correlates have therefore been used to attempt to classify DAP. Eyeball dimensions are good predictors of DAP because they relate directly to light sensitivity of the eye. Osteological characters, such as scleral ring dimensions, are also reliable proxies, but bony orbit dimensions alone have proven less reliable because soft tissues other than the eyeball can affect orbit size and shape. However, it would be useful if bony orbit dimensions could be used to determine DAP, particularly for mammals, which have no scleral ring, and nonmammalian synapsids, which infrequently preserve scleral rings. We investigated the possibility of predicting DAP in sciurids (Mammalia: Rodentia: Sciuridae) using orbit measurements and other cranial dimensions, and a variety of quantitative methods, including phylogenetic flexible discriminant analysis, classification trees, and logistic regression. The latter two methods do not require a priori assignment of DAP and therefore reflect the situation in a fossil data set. We find that although there are some interfering phylogenetic factors, nocturnal and non-nocturnal sciurids can be differentiated from one another with over 80% accuracy using all methods investigated here; attempts to differentiate crepuscular animals from nocturnal and diurnal species proved much less successful. Our results indicate that these analyses offer several viable options for predicting DAP in the fossil record, but such analyses should be conducted in a phylogenetic context whenever possible. Anat Rec, 2018.
The Stagodontidae include the largest metatherians known from the Cretaceous of North America. Of the recognized species of the stagodontid genus Eodelphis, E. cutleri is larger and has a more robust dentary, more inflated premolars, and third premolars specialized for crushing, as opposed to the more gracile E. browni. These differences have led to the hypothesis that an E. cutleri-like ancestor gave rise to Didelphodon—another, mostly younger, stagodontid, which has been interpreted as a durophagous predator-scavenger. If correct, E. cutleri would be expected to show more morphological adaptation toward durophagy than E. browni does. Here, we describe two new dentary fossils referable to E. browni and test the evolutionary hypothesis by applying beam theory to estimate bending force capabilities of 22 dentaries of Cretaceous stagodontids and other metatherians. The resulting diversity of bending force profiles of the sampled dentaries implies that Cretaceous metatherians had a wide range of feeding behaviors. Among the stagodontids, E. cutleri has a mediolateral bending force profile of the dentary that is more similar to that of Didelphodon than it is to that of E. browni; whereas its dorsoventral bending force profile is more similar to that of E. browni. These results indicate that anteriorly the dentary of E. cutleri was capable of resisting high torsional stresses from hard-object feeding but lacked other dorsoventral buttressing associated with exceptionally high bite forces of Didelphodon. Our results imply that some morphological changes associated with durophagy evolved twice within this clade, independently in E. cutleri and Didelphodon.
A new Paleogene metatherian from locality IAA 1/90, Marambio (Seymour) Island in the Antarctic Peninsula is described. Pujatodon ektopos, gen. et sp. nov., is recognized on the basis of a tiny lower left molar recovered from early Eocene (late Ypresian) levels of the Cucullaea I Allomember, La Meseta Formation. The tooth is characterized by its small size, bunoid aspect, short trigonid with closely set paraconid and metaconid, wide and long talonid, the development of an incipient cingulid at the labial base of the crown between the trigonid and talonid, and an expanded posterior cingulid. Body mass estimations for the new taxon range from 83.13 to 153.15 g. Its enamel microstructure shows the earliest evidence among metatherians of aligned prisms, as well as of interprismatic sheets of matrix. The analysis of other parameters, like body mass, molar morphometric index, and wear facets, suggests that the molars of Pujatodon were primarily adapted to the processing of fruits, nuts, seeds, and/or hard insects. Several features suggest the allocation of this specimen among basal polydolopimorphians (Prepidolopidae or, more probably, Glasbiidae). The discovery of the specimen MLP 14-I-10-20 could offer new insights on the origins and early diversification of Australidelphian marsupials in southern (and northern?) continents. It also adds significant information on the diversity of Antarctic Paleogene mammals, their evolution, habits, and historical biogeography.
The evolution of the mammalian jaw is one of the most important innovations in vertebrate history, and underpins the exceptional radiation and diversification of mammals over the last 220 million years1,2. In particular, the transformation of the mandible into a single tooth-bearing bone and the emergence of a novel jaw joint-while incorporating some of the ancestral jaw bones into the mammalian middle ear-is often cited as a classic example of the repurposing of morphological structures3,4. Although it is remarkably well-documented in the fossil record, the evolution of the mammalian jaw still poses the paradox of how the bones of the ancestral jaw joint could function both as a joint hinge for powerful load-bearing mastication and as a mandibular middle ear that was delicate enough for hearing. Here we use digital reconstructions, computational modelling and biomechanical analyses to demonstrate that the miniaturization of the early mammalian jaw was the primary driver for the transformation of the jaw joint. We show that there is no evidence for a concurrent reduction in jaw-joint stress and increase in bite force in key non-mammaliaform taxa in the cynodont-mammaliaform transition, as previously thought5-8. Although a shift in the recruitment of the jaw musculature occurred during the evolution of modern mammals, the optimization of mandibular function to increase bite force while reducing joint loads did not occur until after the emergence of the neomorphic mammalian jaw joint. This suggests that miniaturization provided a selective regime for the evolution of the mammalian jaw joint, followed by the integration of the postdentary bones into the mammalian middle ear.
Background:
Recent molecular dating estimates for placental mammals echo fossil inferences for an explosive interordinal diversification, but typically place this event some 10-20 million years earlier than the Paleocene fossils, among apparently more "primitive" mammal faunas.
Results:
However, current models of molecular evolution do not adequately account for parallel rate changes, and result in dramatic divergence underestimates for large, long-lived mammals such as whales and hominids. Calibrating among these taxa shifts the rate model errors deeper in the tree, inflating interordinal divergence estimates. We employ simulations based on empirical rate variation, which show that this "error-shift inflation" can explain previous molecular dating overestimates relative to fossil inferences. Molecular dating accuracy is substantially improved in the simulations by focusing on calibrations for taxa that retain plesiomorphic life-history characteristics. Applying this strategy to the empirical data favours the soft explosive model of placental evolution, in line with traditional palaeontological interpretations - a few Cretaceous placental lineages give rise to a rapid interordinal diversification following the 66 Ma Cretaceous-Paleogene boundary mass extinction.
Conclusions:
Our soft explosive model for the diversification of placental mammals brings into agreement previously incongruous molecular, fossil, and ancestral life history estimates, and closely aligns with a growing consensus for a similar model for bird evolution. We show that recent criticism of the soft explosive model relies on ignoring both experimental controls and statistical confidence, as well as misrepresentation, and inconsistent interpretations of morphological phylogeny. More generally, we suggest that the evolutionary properties of adaptive radiations may leave current molecular dating methods susceptible to overestimating the timing of major diversification events.
Molecular estimates of the divergence of placental and marsupial mammals and their broader clades (Eutheria and Metatheria, respectively) fall primarily in the Jurassic period. Supporting these estimates, Juramaia-the oldest purported eutherian-is from the early Late Jurassic (160 million years ago) of northeastern China. Sinodelphys-the oldest purported metatherian-is from the same geographic area but is 35 million years younger, from the Jehol biota. Here we report a new Jehol eutherian, Ambolestes zhoui, with a nearly complete skeleton that preserves anatomical details that are unknown from contemporaneous mammals, including the ectotympanic and hyoid apparatus. This new fossil demonstrates that Sinodelphys is a eutherian, and that postcranial differences between Sinodelphys and the Jehol eutherian Eomaia-previously thought to indicate separate invasions of a scansorial niche by eutherians and metatherians-are instead variations among the early members of the placental lineage. The oldest known metatherians are now not from eastern Asia but are 110 million years old from western North America, which produces a 50-million-year ghost lineage for Metatheria.
Changes in mammalian faunal composition and structure following the Cretaceous- Paleogene mass extinction are central to understanding not only how terrestrial communities recovered from this ecological perturbation but also the evolution of archaic groups leading to extant mammalian clades. Here, we analyzed changes in mammalian local faunas during the earliest Paleogene biotic recovery on a small spatiotemporal scale. We compiled samples of mammals from four localities in the Hell Creek Formation and Tullock Member of the Fort Union Formation, in the McGuire Creek area, McCone County, Montana, USA, and placed these localities into a high-precision chronostratigraphic framework using ⁴⁰Ar/³⁹Ar tephra ages and magnetostratigraphy. Within this framework, we quantitatively compared faunal composition, heterogeneity, and richness among McGuire Creek local faunas and made broader comparisons to other earliest Paleogene faunas from throughout the Western Interior of North America. In the first ~320 k.y. of the recovery, mammalian local faunas at McGuire Creek, all of which can be placed in the Puercan 1 North American Land Mammal Age (NALMA) interval zone, underwent modest increases in taxonomic richness and heterogeneity, indicating the beginning of biotic recovery; however, no Mc- Guire Creek fauna reached fully recovered levels of taxonomic richness. Further, appearance of immigrant taxa such as Purgatorius in younger McGuire Creek faunas demonstrates important compositional changes within the Pu1 of McGuire Creek. These results highlight the difficulties with describing the nuanced mammalian recovery process using the NALMA system and emphasize the increasing importance of high-precision dating, especially when comparing faunas across large geographic distances.
Haramiyida was a successful clade of mammaliaforms, spanning the Late Triassic period to at least the Late Jurassic period, but their fossils are scant outside Eurasia and Cretaceous records are controversial1-4. Here we report, to our knowledge, the first cranium of a large haramiyidan from the basal Cretaceous of North America. This cranium possesses an amalgam of stem mammaliaform plesiomorphies and crown mammalian apomorphies. Moreover, it shows dental traits that are diagnostic of isolated teeth of supposed multituberculate affinities from the Cretaceous of Morocco, which have been assigned to the enigmatic 'Hahnodontidae'. Exceptional preservation of this specimen also provides insights into the evolution of the ancestral mammalian brain. We demonstrate the haramiyidan affinities of Gondwanan hahnodontid teeth, removing them from multituberculates, and suggest that hahnodontid mammaliaforms had a much wider, possibly Pangaean distribution during the Jurassic-Cretaceous transition.
The end-Cretaceous extinction led to a massive faunal turnover, with placental mammals radiating in the wake of nonavian dinosaurs. Fossils indicate that Cretaceous stem placentals were generally insectivorous, whereas their earliest Cenozoic descendants occupied a variety of dietary niches. It is hypothesized that this dietary radiation resulted from the opening of niche space, following the extinction of dinosaurian carnivores and herbivores. We provide the first genomic evidence for the occurrence and timing of this dietary radiation in placental mammals. By comparing the genomes of 107 placental mammals, we robustly infer that chitinase genes (CHIAs), encoding enzymes capable of digesting insect exoskeletal chitin, were present as five functional copies in the ancestor of all placental mammals, and the number of functional CHIAs in the genomes of extant species positively correlates with the percentage of invertebrates in their diets. The diverse repertoire of CHIAs in early placental mammals corroborates fossil evidence of insectivory in Cretaceous eutherians, with descendant lineages repeatedly losing CHIAs beginning at the Cretaceous/Paleogene (K/Pg) boundary as they radiated into noninsectivorous niches. Furthermore, the timing of gene loss suggests that interordinal diversification of placental mammals in the Cretaceous predates the dietary radiation in the early Cenozoic, helping to reconcile a long-standing debate between molecular timetrees and the fossil record. Our results demonstrate that placental mammal genomes, including humans, retain a molecular record of the post-K/Pg placental adaptive radiation in the form of numerous chitinase pseudogenes.
New dental and dentary fossils collected in the Upper Cretaceous La Colonia Formation in central Patagonia provide new evidence on the morphology, feeding ecology, and relationships of the enigmatic mammal Reigitherium. The newly discovered specimens described here include elements of the upper dentition and several partial dentaries, elucidating fundamental questions of serial homology and postcanine dental formula (four premolars and three molars). This new evidence supports a nested position of Reigitherium within the advanced meridiolestidan clade Mesungulatoidea. Apomorphic features of the upper and lower molariform elements include intense enamel crenulation circumscribed within the primary trigon and trigonid, elevated cingulids, and the neomorphic appearance of cusps/cuspulids, all of which increase overall crown complexity. A Dental Topography Analysis comparing Reigitherium and its sister taxon Peligrotherium to Cretaceous and Cenozoic therians demonstrates functional similarity between the mesungulatoids and South American marsupial taxa that succeed them in the small-to medium-sized herbivore niche during the Paleocene. Previous taxonomic attributions of Reigitherium are discussed and comparisons with other meridiolestidans highlight the remarkable radiation of this group in the Cretaceous of South America.
The two major approaches to studying macroevolution in deep time are the fossil record and reconstructed relationships among extant taxa from molecular data. Results based on one approach sometimes conflict with those based on the other, with inconsistencies often attributed to inherent flaws of one (or the other) data source. What is unquestionable is that both the molecular and fossil records are limited reflections of the same evolutionary history, and any contradiction between them represents a failure of our existing models to explain the patterns we observe. Fortunately, the different limitations of each record provide an opportunity to test or calibrate the other, and new methodological developments leverage both records simultaneously. However, we must reckon with the distinct relationships between sampling and time in the fossil record and molecular phylogenies. These differences impact our recognition of baselines, and the analytical incorporation of age estimate uncertainty. These differences in perspective also influence how different practitioners view the past and evolutionary time itself, bearing important implications for the generality of methodological advancements, and differences in the philosophical approach to macroevolutionary theory across fields.
Gliding is a distinctive locomotion type that has been identified in only three mammal species from the Mesozoic era. Here we describe another Jurassic glider that belongs to the euharamiyidan mammals and shows hair details on its gliding membrane that are highly similar to those of extant gliding mammals. This species possesses a five-boned auditory apparatus consisting of the stapes, incus, malleus, ectotympanic and surangular, representing, to our knowledge, the earliest known definitive mammalian middle ear. The surangular has not been previously identified in any mammalian middle ear, and the morphology of each auditory bone differs from those of known mammals and their kin. We conclude that gliding locomotion was probably common in euharamiyidans, which lends support to idea that there was a major adaptive radiation of mammals in the mid-Jurassic period. The acquisition of the auditory bones in euharamiyidans was related to the formation of the dentary-squamosal jaw joint, which allows a posterior chewing movement, and must have evolved independently from the middle ear structures of monotremes and therian mammals.
Eutherian mammals (Placentalia and all mammals phylogenetically closer to placentals than to marsupials) comprise the vast majority of extant Mammalia. Among these there is a phenomenal range of forms and sizes, but the origins of crown group placentals are obscure. They lie within the generally tiny mammals of the Mesozoic, represented for the most part by isolated teeth and jaws, and there is strongly conflicting evidence from phenomic and molecular data as to the date of origin of both Eutheria and Placentalia. The oldest purported eutherians are Juramaia from the Upper Jurassic of China, and Eomaia and Acristatherium from the Lower Cretaceous, also of China. Based on dental characters and analyses of other morphological and molecular data, doubt has recently been cast on the eutherian affinities of the Chinese taxa and consequently on the date of emergence of Eutheria. Until now, the only tribosphenic mammal recorded from the earliest
Cretaceous (Berriasian) Purbeck Group of Britain was the stem tribosphenidan Tribactonodon. Here we document two new tribosphenic mammals from the Purbeck Group, Durlstotherium gen. nov. and Durlstodon gen. nov., showing highly derived eutherian molar characters that support the early emergence of this clade, prior to the Cretaceous.
Most modern mammals, including strictly diurnal species, exhibit sensory adaptations to nocturnal activity that are thought to be the result of a prolonged nocturnal phase or ‘bottleneck’ during early mammalian evolution. Nocturnality may have allowed mammals to avoid antagonistic interactions with diurnal dinosaurs during the Mesozoic. However, understanding the evolution of mammalian activity patterns is hindered by scant and ambiguous fossil evidence. While ancestral reconstructions of behavioural traits from extant species have the potential to elucidate these patterns, existing studies have been limited in taxonomic scope. Here, we use an extensive behavioural dataset for 2,415 species from all extant orders to reconstruct ancestral activity patterns across Mammalia. We find strong support for the nocturnal origin of mammals and the Cenozoic appearance of diurnality, although cathemerality (mixed diel periodicity) may have appeared in the late Cretaceous. Simian primates are among the earliest mammals to exhibit strict diurnal activity, some 52–33 million years ago. Our study is consistent with the hypothesis that temporal partitioning between early mammals and dinosaurs during the Mesozoic led to a mammalian nocturnal bottleneck, but also demonstrates the need for improved phylogenetic estimates for Mammalia.
There is a well-established discrepancy between paleontological and molecular data regarding the timing of the origin and diversification of placental mammals. Molecular estimates place interordinal diversification dates in the Cretaceous, while no unambiguous crown placental fossils have been found prior to the end-Cretaceous mass extinction. Here, the completeness of the eutherian fossil record through geological time is evaluated to assess the suggestion that a poor fossil record is largely responsible for the difference in estimates of placental origins. The completeness of fossil specimens was measured using the character completeness metric, which quantifies the completeness of fossil taxa as the percentage of phylogenetic characters available to be scored for any given taxon. Our data set comprised 33 published cladistic matrices representing 445 genera, of which 333 were coded at the species level.
There was no significant difference in eutherian completeness across the Cretaceous/Paleogene (K/Pg) boundary. This suggests that the lack of placental mammal fossils in the Cretaceous is not due to a poor fossil record but more likely represents a genuine absence of placental mammals in the Cretaceous. This result supports the “explosive model” of early placental evolution, whereby placental mammals originated around the time of the K/Pg boundary and diversified soon after.
No correlation was found between the completeness pattern observed in this study and those of previous completeness studies on birds and sauropodomorph dinosaurs, suggesting that different factors affect the preservation of these groups. No correlations were found with various isotope proxy measures, but Akaike information criterion analysis found that eutherian character completeness metric scores were best explained by models involving the marine-carbonate strontium-isotope ratios ( ⁸⁷ Sr/ ⁸⁶ Sr), suggesting that tectonic activity might play a role in controlling the completeness of the eutherian fossil record.
Stem mammaliaforms are Mesozoic forerunners to mammals, and they offer critical evidence for the anatomical evolution and ecological diversification during the earliest mammalian history. Two new eleutherodonts from the Late Jurassic period have skin membranes and skeletal features that are adapted for gliding. Characteristics of their digits provide evidence of roosting behaviour, as in dermopterans and bats, and their feet have a calcaneal calcar to support the uropagatium as in bats. The new volant taxa are phylogenetically nested with arboreal eleutherodonts. Together, they show an evolutionary experimentation similar to the iterative evolutions of gliders within arboreal groups of marsupial and placental mammals. However, gliding eleutherodonts possess rigid interclavicle-clavicle structures, convergent to the avian furculum, and they retain shoulder girdle plesiomorphies of mammaliaforms and monotremes. Forelimb mobility required by gliding occurs at the acromion-clavicle and glenohumeral joints, is different from and convergent to the shoulder mobility at the pivotal clavicle-sternal joint in marsupial and placental gliders.
Stem mammaliaforms are forerunners to modern mammals, and they achieved considerable ecomorphological diversity in their own right. Recent discoveries suggest that eleutherodontids, a subclade of Haramiyida, were more species-rich during the Jurassic period in Asia than previously recognized. Here we report a new Jurassic eleutherodontid mammaliaform with an unusual mosaic of highly specialized characteristics, and the results of phylogenetic analyses that support the hypothesis that haramiyidans are stem mammaliaforms. The new fossil shows fossilized skin membranes that are interpreted to be for gliding and a mandibular middle ear with a unique character combination previously unknown in mammaliaforms. Incisor replacement is prolonged until well after molars are fully erupted, a timing pattern unique to most other mammaliaforms. In situ molar occlusion and a functional analysis reveal a new mode of dental occlusion: dual mortar-pestle occlusion of opposing upper and lower molars, probably for dual crushing and grinding. This suggests that eleutherodontids are herbivorous, and probably specialized for granivory or feeding on soft plant tissues. The inferred dietary adaptation of eleutherodontid gliders represents a remarkable evolutionary convergence with herbivorous gliders in Theria. These Jurassic fossils represent volant, herbivorous stem mammaliaforms associated with pre-angiosperm plants that appear long before the later, iterative associations between angiosperm plants and volant herbivores in various therian clades.
Theria comprises all but three living mammalian genera and is one of the most ecologically pervasive clades on Earth. Yet, the origin and early history of therians and their close relatives (i.e., cladotherians) remains surprisingly enigmatic. A critical biological function that can be compared among early mammal groups is mastication. Morphometrics and modeling analyses of the jaws of Mesozoic mammals indicate that cladotherians evolved musculoskeletal anatomies that increase mechanical advantage during jaw rotation around a dorsoventrally-oriented axis (i.e., yaw) while decreasing the mechanical advantage of jaw rotation around a mediolaterally-oriented axis (i.e., pitch). These changes parallel molar transformations in early cladotherians that indicate their chewing cycles included significant transverse movement, likely produced via yaw rotation. Thus, I hypothesize that cladotherian molar morphologies and musculoskeletal jaw anatomies evolved concurrently with increased yaw rotation of the jaw during chewing cycles. The increased transverse movement resulting from yaw rotation may have been a crucial evolutionary prerequisite for the functionally versatile tribosphenic molar morphology, which underlies the molars of all therians and is retained by many extant clades.
Marsupial mammal relatives (stem metatherians) from the Mesozoic Era (252–66 million years ago) are mostly known from isolated teeth and fragmentary jaws. Here we report on the first near-complete skull remains of a North American Late Cretaceous metatherian, the stagodontid Didelphodon vorax. Our phylogenetic analysis indicates that marsupials or their closest relatives evolved in North America, as part of a Late Cretaceous diversification of metatherians, and later dispersed to South America. In addition to being the largest known Mesozoic therian mammal (node-based clade of eutherians and metatherians), Didelphodon vorax has a high estimated bite force and other craniomandibular and dental features that suggest it is the earliest known therian to invade a durophagous predator–scavenger niche. Our results broaden the scope of the ecomorphological diversification of Mesozoic mammals to include therian lineages that, in this case, were linked to the origin and evolution of marsupials.
The Mesozoic marked a time of experimentation in the tooth morphology of early mammals. One particular experiment involved the movement of three points, or cusps, on the surface of a molar tooth from a line into a triangle. This transition is exemplified by two extinct insectivorous mammals, Morganucodon (cusps in a line) and Kuehneotherium (cusps in a triangle). Here we test whether this difference in cusp arrangement, alongside cusp heights and angles between cusps, is associated with differences in the ability of the teeth to fracture proxy-insect prey. We gathered measurements from molar teeth of both species and used them to create physical models. We then measured the force, time and energy at fracture and peak force, and the amount of damage inflicted by the models on hard and soft gels encased in a tough film that mimicked the material properties of insects. The Morganucodon model required less force and energy to fracture hard gels and reach peak force compared with Kuehneotherium. Kuehneotherium required a similar time, force and energy to fracture soft gels but reduced the time, force and energy to reach peak force. More importantly, Kuehneotherium also inflicted more damage to both the hard and the soft gels. These results suggest that changes in dental morphology in some early mammals was driven primarily by selection for maximizing damage, and secondarily for maximizing biomechanical efficiency for a given food material property.
The effect of the Cretaceous-Palaeogene (K-Pg) mass extinction on the evolution of many groups, including placental mammals, has been hotly debated. The fossil record suggests a sudden adaptive radiation of placentals immediately after the event, but several recent quantitative analyses have reconstructed no significant increase in either clade origination rates or rates of character evolution in the Palaeocene. Here we use stochastic methods to date a recent phylogenetic analysis of Cretaceous and Palaeocene mammals and show that Placentalia likely originated in the Late Cretaceous, but that most intraordinal diversification occurred during the earliest Palaeocene. This analysis reconstructs fewer than 10 placental mammal lineages crossing the K-Pg boundary. Moreover,we showthat rates of morphological evolution in the 5 Myr interval immediately after the K-Pg mass extinction are three times higher than background rates during the Cretaceous. These results suggest that the K-Pg mass extinction had a marked impact on placental mammal diversification, supporting the view that an evolutionary radiation occurred as placental lineages invaded new ecological niches during the Early Palaeocene. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
Mammalian faunas in North America experienced dramatic change during the Cretaceous, with earlier faunas characterized by eutriconodontans, symmetrodontans, and unspecialized therians giving way to a major diversification of therian lineages by the Campanian– Maastrichtian. The Aquilan North American Land Mammal Age (NALMA), originally based on the well-studied fauna of the Milk River Formation (Santonian) of southern Alberta, records the start of this transition. Notable are first appearances of pediomyoid marsupialiforms and the eutherian Paranyctoides, and last occurrences of eutriconodontans and symmetrodontans. The Campanian Wahweap Formation has yielded a similar fauna, but until now the John Henry Member of the Straight Cliffs Formation was the only other unit of known Santonian age from which fossil mammals have been recovered, leaving this transitional interval represented by limited sampling. The Eagle Formation in central and northern Montana is considered to be laterally equivalent to the Milk River Formation, with northernmost exposures correlated to the upper Santonian, based on palynomorphs and magnetostratigraphy. Here, we describe the first fossil mammals known from the Eagle Formation. A relatively small rock sample yielded a rich, diverse assemblage including two genera of spalacotheriid symmetrodonts, several “alphadontid” marsupialiforms and the large pediomyoid Aquiladelphis, and at least two eutherians including Paranyctoides. Multituberculates, to be described separately, are also abundant and diverse. The Eagle Formation assemblage is broadly similar in composition to that from the Milk River Formation, but shares the spalacotheriid Spalacotheridium with older units, including the Straight Cliffs Formation from southern Utah. These initial results provide another biostratigraphic data point linking Santonian faunas across a broad latitudinal range, and encourage reevaluation of the Aquilan NALMA.
It is often postulated that mammalian diversity was suppressed during the Mesozoic Era and increased rapidly after the Cretaceous–Palaeogene (K– Pg) extinction event.We test this hypothesis by examining macroevolutionary patterns in early therian mammals, the group that gave rise to modern placentals and marsupials. We assess morphological disparity and dietary trends using morphometric analyses of lower molars, and we evaluate generic level taxonomic diversity patterns using techniques that account for sampling biases. In contrast with the suppression hypothesis, our results suggest that an ecomorphological diversification of therians began 10-20 Myr prior to the K–Pg extinction event, led by disparate metatherians and Eurasian faunas. This diversification is concurrent with ecomorphological radiations of multituberculate mammals and flowering plants, suggesting that mammals as a whole benefitted from the ecological rise of angiosperms. In further contrast with the suppression hypothesis, therian disparity decreased immediately after the K–Pg boundary, probably due to selective extinction against ecological specialists and metatherians. However, taxonomic diversity trends appear to have been decoupled from disparity patterns, remaining low in the Cretaceous and substantially increasing immediately after the K–Pg extinction event. The conflicting diversity and disparity patterns suggest that earliest Palaeocene extinction survivors, especially eutherian dietary generalists, underwent rapid taxonomic diversification without considerable morphological diversification. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
How did evolution generate the extraordinary diversity of vertebrates on land? Zero species are known prior to ~380 million years ago, and more than 30,000 are present today. An expansionist model suggests this was achieved by large and unbounded increases, leading to substantially greater diversity in the present than at any time in the geological past. This model contrasts starkly with empirical support for constrained diversification in marine animals, suggesting different macroevolutionary processes on land and in the sea. We quantify patterns of vertebrate standing diversity on land during the Mesozoic-early Paleogene interval, applying sample-standardization to a global fossil dataset containing 27,260 occurrences of 4,898 non-marine tetrapod species. Our results show a highly stable pattern of Mesozoic tetrapod diversity at regional and local levels, underpinned by a weakly positive, but near-zero, long-term net diversification rate over 190 million years. Species diversity of non-flying terrestrial tetrapods less than doubled over this interval, despite the origins of exceptionally diverse extant groups within mammals, squamates, amphibians, and dinosaurs. Therefore, although speciose groups of modern tetrapods have Mesozoic origins, rates of Mesozoic diversification inferred from the fossil record are slow compared to those inferred from molecular phylogenies. If high speciation rates did occur in the Mesozoic, then they seem to have been balanced by extinctions among older clades. An apparent 4-fold expansion of species richness after the Cretaceous/Paleogene (K/Pg) boundary deserves further examination in light of potential taxonomic biases, but is consistent with the hypothesis that global environmental disturbances such as mass extinction events can rapidly adjust limits to diversity by restructuring ecosystems, and suggests that the gradualistic evolutionary diversification of tetrapods was punctuated by brief but dramatic episodes of radiation.
In the aftermaths of mass extinction events, during radiations of clades, and in several other evolutionary scenarios, there is often a decoupling of taxonomic diversity and morphological disparity. The placental mammal radiation after the end-Cretaceous mass extinction is one of the archetypal adaptive radiations, but the change in morphological disparity of the entire skeleton has never been quantified across this important boundary. We reconstruct ancestral morphologies of 680 discrete morphological characters onto dated phylogenies of 177 mostly Cretaceous and Palaeogene eutherians (placental mammals and their stem relatives). Using a new approach to incorporate morphologies representing ghost lineages, we assess three measures of morphological disparity (sum of ranges, sum of variances and mean pairwise dissimilarity) across stage-level time bins within the Cretaceous and Palaeogene. We find that the range-based metric suggests that eutherian disparity increased immediately after the end-Cretaceous mass extinction, while both variance-based metrics declined from the Campanian to the Maastrichtian, but showed no change in disparity from the Maastrichtian to the Puercan - the first North American Land Mammal Age of the Paleocene. Increases in variance-based metrics lag behind the range-based metric and per-lineage accumulation rate, suggesting that the response of mammals to the Cretaceous-Palaeogene event was characterized by an early radiation that increased overall morphospace occupation, followed later by specialization that resulted in increased dissimilarity.
Significance
The origins and earliest evolution of mammals can be deciphered by studying Late Triassic fossil relatives of modern mammals. The computed tomography study of Haramiyavia from the Late Triassic has revealed new information about the skull evolution and dental function in the forerunners of mammals. Haramiyavia had a unique way of chewing. Its teeth of multiple cusp-rows were adapted to omnivory or herbivory and are distinctive from the teeth of other early mammal relatives that are presumed to be insectivorous. On the mammal family tree Haramiyavia occupies a position crucial for dating the initial appearance of the major mammalian groups. Our reanalysis affirms that the earliest diversification of mammals occurred in the Jurassic.
The Mesozoic era (252–66 million years ago), known as the domain of dinosaurs, witnessed a remarkable ecomorphological diversity of early mammals. The key mammalian characteristics originated during this period and were prerequisite for their evolutionary success after extinction of the non-avian dinosaurs 66 million years ago. Many ecomorphotypes familiar to modern mammal fauna evolved independently early in mammalian evolutionary history. Here we report a 125-million-year-old eutriconodontan mammal from Spain with extraordinary preservation of skin and pelage that extends the record of key mammalian integumentary features into the Mesozoic era. The new mammalian specimen exhibits such typical mammalian features as pelage, mane, pinna, and a variety of skin structures: keratinous dermal scutes, protospines composed of hair-like tubules, and compound follicles with primary and secondary hairs. The skin structures of this new Mesozoic mammal encompass the same combination of integumentary features as those evolved independently in other crown Mammalia, with similarly broad structural variations as in extant mammals. Soft tissues in the thorax and abdomen (alveolar lungs and liver) suggest the presence of a muscular diaphragm. The eutriconodont has molariform tooth replacement, ossified Meckel’s cartilage of the middle ear, and specialized xenarthrous articulations of posterior dorsal vertebrae, convergent with extant xenarthran mammals, which strengthened the vertebral column for locomotion.
Although herbivory probably first appeared over 300 million years ago, it only became established as a common feeding strategy during Late Permian times. Subsequently, herbivory evolved in numerous lineages of terrestrial vertebrates, and the acquisition of this mode of feeding was frequently associated with considerable evolutionary diversification in those lineages. This book, originally published in 2000, represented the first comprehensive overview of the evolution of herbivory in land-dwelling amniote tetrapods in recent years. In Evolution of Herbivory in Terrestrial Vertebrates leading experts review the structural adaptations for, and the evolutionary history of, feeding on plants in the major groups of land-dwelling vertebrates, especially dinosaurs and ungulate mammals. As such it will be the definitive reference source on this topic for evolutionary biologists and vertebrate paleontologists alike.
Significance
Amazing fossil discoveries over the last 30 years have led to the paleontological consensus that some Mesozoic mammaliaforms underwent ecomorphological diversification in the midst of dinosaurs. However, the ecological structure of Mesozoic mammaliaform communities remains unclear. Here, we quantify the ecological structure of extinct and extant small-bodied mammaliaform communities aiming to identify evolutionary and ecological drivers that have influenced those communities through time. We used body size, diet, and locomotion of constituent species to plot ecospace occupation and calculate ecological richness and disparity of those communities. We propose that the interplay of Late Cretaceous dental evolution, the rise of angiosperms, and competition with other vertebrates were critical in shaping the ecological structure of small-bodied mammaliaform communities through time.
Life history and behavioral traits are often difficult to discern from the fossil record, but evolutionary rates of genes and their changes over time can be inferred from extant genomic data. Under the neutral theory, molecular evolutionary rate is a product of mutation rate and the proportion of neutral mutations [1, 2]. Mutation rates may be shared across the genome, whereas proportions of neutral mutations vary among genes because functional constraints vary. By analyzing evolutionary rates of 1,185 genes in a phylogeny of 89 mammals, we extracted historical profiles of functional constraints on these rates in the form of gene-branch interactions. By applying a novel statistical approach to these profiles, we reconstructed the history of ten discrete traits related to activity, diet, and social behaviors. Our results indicate that the ancestor of placental mammals was solitary, seasonally breeding, insectivorous, and likely nocturnal. The results suggest placental diversification began 10-20 million years before the K-Pg boundary (66 million years ago), with some ancestors of extant placental mammals becoming diurnal and adapted to different diets. However, from the Paleocene to the Eocene-Oligocene transition (EOT, 33.9 mya), we detect a post-K-Pg nocturnal bottleneck where all ancestral lineages of extant placentals were nocturnal. Although diurnal placentals may have existed during the elevated global temperatures of the Paleocene-Eocene thermal maximum [3], we hypothesize that diurnal placentals were selectively extirpated during or after the global cooling of the EOT, whereas some nocturnal lineages survived due to preadaptations to cold environments [4].
Significance
We produced a genome-scale dataset from representatives of all placental mammal orders to infer diversification timing relative to the Cretaceous–Paleogene (KPg) boundary. Our sensitivity analyses show that divergence time estimates within placentals are considerably biased by the specific way in which a given dataset is processed. We examined the performance of various dating approaches using a comprehensive scheme of likelihood analyses and computational simulations, allowing us to identify the optimal molecular clock parameters, gene sets, and gene partitioning schemes for reliable dating. Based on the optimal methodology, we present a hypothesis of mammalian divergence timing that is more consistent with the fossil record than previous molecular clock reconstructions, suggesting that placental mammals underwent a continuous radiation across the KPg boundary.
The seventy-fifth anniversary of the Journal of Paleontology presents a felicitous opportunity to review major changes in interpretation of mammalian phylogeny. Founding of the journal coincides with the nascence of the career of the most influential paleomammalogist of the past century, George Gaylord Simpson (1902-1984). It occurred at a time when now-archaic models for mammalian systematics and evolution, such as the aristogenesis of H. F. Osborn (1857-1935) and the typological concept of taxa, were prevalent (e.g., Simpson, 1945). These models were soon to give way to “new ways of going at things” (Laporte, 2000, p. 87); most significantly, the incorporation of quantitative methods and the evolutionary synthesis (Simpson, 1944). Subsequent decades witnessed the rise and/or sophistication of other applications and perspectives in fossil-based interpretation of mammalian systematics, including form-function analysis (e.g., Szalay, 1994) and, particularly, cladistic approaches (e.g., McKenna, 1975). Within these broad ideological frameworks, major paradigm shifts have resulted from new discoveries, conceptual changes, or (most commonly) a combination of both. Finally, mammalian systematics currently lie at the verge of a monumental paradigm shift, providing important direction for the future.
The end-Cretaceous mass extinction ranks among the most severe extinctions of all time; however, patterns of extinction and recovery remain incompletely understood. In particular, it is unclear how severe the extinction was, how rapid the recovery was, and how sampling biases might affect our understanding of these processes. To better understand terrestrial extinction and recovery and how sampling influences these patterns, we collected data on the occurrence and abundance of fossil mammals to examine mammalian diversity across the K-Pg boundary in North America. Our data show that the extinction was more severe and the recovery more rapid than previously thought. Extinction rates are markedly higher than previously estimated: of 59 species, 4 survived (93% species extinction, 86% of genera). Survival is correlated with geographic range size and abundance, with widespread, common species tending to survive. This creates a sampling artifact in which rare species are both more vulnerable to extinction and less likely to be recovered, such that the fossil record is inherently biased towards the survivors. The recovery was remarkably rapid. Within 300,000 years, local diversity recovered and regional diversity rose to twice Cretaceous levels, driven by increased endemicity; morphological disparity increased above levels observed in the Cretaceous. The speed of the recovery tends to be obscured by sampling effects; faunas show increased endemicity, such that a rapid, regional increase in diversity and disparity is not seen in geographically restricted studies. Sampling biases that operate against rare taxa appear to obscure the severity of extinction and the pace of recovery across the K-Pg boundary, and similar biases may operate during other extinction events. This article is protected by copyright. All rights reserved.
With more than 100 species, living South American marsupials
(Mammalia, Metatheria) give only a glimpse of the much higher taxonomic and
ecological diversity acquired by metatherians throughout the Cenozoic Era. The
term Metatheria designs a taxon within Mammalia that includes not only
Marsupialia but also all therian mammals more related to Marsupialia than to
Eutheria. Several features (e.g., epipubic ones) formerly considered as diagnostic of
Metatheria are now regarded either a primitive condition or not present in all
members of this group. Other derived features, such as the presence of a shelf-like,
inflected angular process in the lower jaw, are consistently present in all metatherians.
A brief characterization of all major South American, Cenozoic metatherian
lineages is given: “basal ameridelphians,” Sparassodonta, Didelphimorphia,
Paucituberculata, Microbiotheria, and Polydolopimorphia (the latter including
Polydolopiformes and Bonapartheriiformes). Three periods can be distinguished in
the history of our knowledge of Cenezoic South American Metatheria: the first one
(1878–1930) is intimately linked to Florentino Ameghino, Argentina’s most
notable paleontologist; much of our knowledge on extinct metatherians from South
America was elaborated by him. The second period (1930–1977) occurred under
the influence of George Gaylord Simpson’s ideas. Bryan Patterson and Rosendo
Pascual also had an important imprint in South America’s Mammalian
Paleontology. The third period (1977-present) is currently evolving under new
phylogenetic, taxonomic, and paleobiogeographic paradigms; influences are multiple
and major reviews of specific lineages are currently in the making. A final note
on the incompleteness of Cenozoic South America’s fossil record is made: only the
mid to high latitudes, basically in the Southern Cone, are moderately well-sampled
in their terrestrial fossil record.
Schowalteria clemensi n.g. n.sp., from the Late Cretaceous Scollard Formation, Red Deer River Valley is the first Mesozoic taeniodont to be discovered. Although more primitive in important features of the postcanine dentition than the conoryctid Onychodectes (of mid-Puercan age, New Mexico, and previously the most primitive tacniodont known), S. clemensi most resembles the advanced, stylinodontid taeniodonts in incisor morphology, canine specializations, facial proportions, and zygomatic arch construction. The dentition of Schowalteria indicates that the purported affinity of palaeoryctid insectivorans with Onychodectes is based only on homoplastic resemblances, leaving taeniodont relationships unresolved.
Mammals are the dominant large animals of today, occurring in virtually every environment. This book is an account of the remarkable fossil records that document their origin since the extinction of the dinosaurs. Tracing their evolution over the last 35 million years. For the first time presented in one single volume Kemp unveils the exciting DNA sequence evidence which coupled with fossil evidence challenges current thinking on the relationships amongst mammal and their inferred history.