Eutherian Orders Research Articles

Disparity of turbinal bones in placental mammals.

Turbinals are key bony elements of the mammalian nasal cavity, involved in heat and moisture conservation as well as olfaction. While turbinals are well known in some groups, their diversity is poorly understood at the scale of placental mammals, which span 21 orders. Here, we investigated the turbinal bones and associated lamellae for one representative of each extant order of placental mammals. We segmented and isolated each independent turbinal and lamella and found an important diversity of variation in the number of turbinals, as well as their size, and shape. We found that the turbinal count varies widely, from zero in the La Plata dolphin, (Pontoporia blainvillei) to about 110 in the African bush elephant (Loxodonta africana). Multiple turbinal losses and additional gains took place along the phylogeny of placental mammals. Some changes are clearly attributed to ecological adaptation, while others are probably related to phylogenetic inertia. In addition, this work highlights the problem of turbinal nomenclature in some placental orders with numerous and highly complex turbinals, for which homologies are extremely difficult to resolve. Therefore, this work underscores the importance of developmental studies to better clarify turbinal homology and nomenclature and provides a standardized comparative framework for further research.

The effects of ordered multistate morphological characters on phylogenetic analyses of eutherian mammals

Multistate morphological characters are routinely used in phylogenetic analyses. Individual multistate characters may be treated as linearly ordered, partially ordered, or unordered. Each option implies a hypothesis of character evolution, and significant debate surrounds the appropriateness of ordering multistate characters. Several previous analyses support ordering multistate morphological characters when the character states form a morphocline. Here, we explore the effects of ordering a subset of characters in the largest morphological character matrix that is available for placental mammals. All multistate characters were assessed and were ordered only if the character states were meristic or hypothesized to form a morphocline. We then performed parsimony analyses, with and without molecular scaffolds, to examine the effects of ordering on placental mammal phylogeny. We also performed pseudoextinction analyses, which treated designated extant taxa as extinct by eliminating them from the molecular scaffold and scoring soft-tissue characters as missing, to determine if ordered or unordered characters would more accurately reconstruct the relationships of pseudoextinct placental orders. Character ordering affected the placement of a variety of taxa in non-scaffolded analyses, but the effects were less evident in scaffolded analyses. Nevertheless, one of the islands of most parsimonious trees with the ordered data set and a scaffold for extant taxa supported the inclusion of Leptictida, including the Late Cretaceous Gypsonictops, inside of crown Placentalia. Our analyses rarely supported the monophyly of Tamirtheria, the Late Cretaceous-Paleogene stem-based clade that is hypothesized to be the sister to Placentalia. Pseudoextinction analyses using ordered and unordered characters both reconstructed 12 of 19 pseudoextinct orders in positions that are incongruent with a well-supported molecular scaffold. These results suggest that the use of ordered multistate characters does not increase the proportion of well-supported molecular clades that are reconstructed with the largest available phenomic data set for placental mammals.

The evolution of ultraconserved elements in vertebrates.

Ultraconserved elements (UCEs) were discovered two decades ago, arbitrarily defined as sequences that are identical over a length ≥200 bp in the human, mouse and rat genomes. The definition was subsequently extended to sequences ≥100 bp identical in at least three of five mammalian genomes (including dog and cow), and shown to have undergone rapid expansion from ancestors in fish and strong negative selection in birds and mammals. Since then, many more genomes have become available, allowing better definition and more thorough examination of UCE distribution and evolutionary history. We developed a fast and flexible analytical pipeline for identifying UCEs in multiple genomes, dedUCE, which allows manipulation of minimum length, sequence identity, and number of species with a detectable UCE according to specified parameters. We suggest an updated definition of UCEs as sequences ≥100 bp and ≥97% sequence identity in ≥50% of placental mammal orders (12813 UCEs). By mapping UCEs to ∼200 species we find that placental UCEs appeared early in vertebrate evolution, well before land colonisation, suggesting the evolutionary pressures driving UCE selection were present in aquatic environments in the Cambrian-Devonian periods. Most (>90%) UCEs likely appeared after the divergence of gnathostomes from jawless predecessors, were largely established in sequence identity by early Sarcopterygii evolution - before the divergence of lobe-finned fishes from tetrapods - and became near fixed in the amniotes. UCEs are mainly located in the introns of protein-coding and non-coding genes involved in neurological and skeletomuscular development, enriched in regulatory elements, and dynamically expressed throughout embryonic development.

Morphofunctional characteristics оs penis of mammals

ABSTRACT The aim of this work was to analyze the issues of the morphofunctional organization of the baculum (os penis) of mammals. In many mammals, to give strength and density to the organ, bone tissue is present in the penis, which forms the bone of the penis (os penis or baculum). This structure is evolutionarily young; it is present only in representatives of the evolutionarily youngest class of vertebrates - the class of mammals. The baculum is present in the penis of both marsupials and representatives of the orders of placental mammals (many rodents, some chiropterans, pinnipeds, cetaceans, some predators, prosimians and some monkeys). Bone tissue is usually located in the anterior region of the penis between the cavernous and spongy bodies. The baculum is an unpaired bone of an elongated shape; it can have the shape of a rod or plate, straight or curved. In cross-section, in representatives of different species, the bone can be round, square, triangular, or flat. Most often, the baculum is a cylindrical rod, expanded at the base and apex; in the proximal and distal parts there are outgrowths of various shapes. The histogenesis of bone tissue during the formation of the os penis in embryogenesis occurs via indirect osteogenesis. At the site of the future os penis, a cartilaginous model is formed from the mesenchyme, in place of which bone tissue then develops. The basis of the baculum is formed by lamellar bone tissue, in which osteons are well expressed. In the superficial zones of the baculum, coarse fibrous (reticulofibrous) bone tissue, as well as fibrous cartilaginous tissue, was identified. The baculum has been found to increase the overall rigidity of the penis when flexing during copulation. It was revealed that larger baculums are present in mammals, which are characterized by a longer duration of copulation.

Metagenomics uncovers dietary adaptations for chitin digestion in the gut microbiota of convergent myrmecophagous mammals.

In mammals, myrmecophagy (ant and termite consumption) represents a striking example of dietary convergence. This trait evolved independently at least five times in placentals with myrmecophagous species comprising aardvarks, anteaters, some armadillos, pangolins, and aardwolves. The gut microbiome plays an important role in dietary adaptation, and previous analyses of 16S rRNA metabarcoding data have revealed convergence in the composition of the gut microbiota among some myrmecophagous species. However, the functions performed by these gut bacterial symbionts and their potential role in the digestion of prey chitinous exoskeletons remain open questions. Using long- and short-read sequencing of fecal samples, we generated 29 gut metagenomes from nine myrmecophagous and closely related insectivorous species sampled in French Guiana, South Africa, and the United States. From these, we reconstructed 314 high-quality bacterial genome bins of which 132 carried chitinase genes, highlighting their potential role in insect prey digestion. These chitinolytic bacteria belonged mainly to the family Lachnospiraceae, and some were likely convergently recruited in the different myrmecophagous species as they were detected in several host orders (i.e., Enterococcus faecalis, Blautia sp.), suggesting that they could be directly involved in the adaptation to myrmecophagy. Others were found to be more host-specific, possibly reflecting phylogenetic constraints and environmental influences. Overall, our results highlight the potential role of the gut microbiome in chitin digestion in myrmecophagous mammals and provide the basis for future comparative studies performed at the mammalian scale to further unravel the mechanisms underlying the convergent adaptation to myrmecophagy. IMPORTANCE Myrmecophagous mammals are specialized in the consumption of ants and/or termites. They do not share a direct common ancestor and evolved convergently in five distinct placental orders raising questions about the underlying adaptive mechanisms involved and the relative contribution of natural selection and phylogenetic constraints. Understanding how these species digest their prey can help answer these questions. More specifically, the role of their gut microbial symbionts in the digestion of the insect chitinous exoskeleton has not been investigated in all myrmecophagous orders. We generated 29 new gut metagenomes from nine myrmecophagous species to reconstruct more than 300 bacterial genomes in which we identified chitin-degrading enzymes. Studying the distribution of these chitinolytic bacteria among hosts revealed both shared and specific bacteria between ant-eating species. Overall, our results highlight the potential role of gut symbionts in the convergent dietary adaptation of myrmecophagous mammals and the evolutionary mechanisms shaping their gut microbiota.

The ear region of the Philippine flying lemur Cynocephalus volans (Placentalia, Dermoptera).

The placental order Dermoptera, which includes two extant species, the Philippine and Sunda flying lemurs, Cynocephalus volans and Galeopterus variegatus, respectively, is generally held to be the sister group of Primates. Yet, little has been reported on their cranial anatomy. Here, the anatomy of the ear region is described and illustrated for a juvenile and adult C. volans based on CT scans. The inclusion of a juvenile is essential as nearly all cranial sutures are fused in the adult. Soft tissues are reconstructed based on sectioned histological pre- and postnatal specimens previously reported by the author. Numerous unusual features are identified, including: a small parasphenoid beneath the basisphenoid, a tensor tympani fossa on the epitympanic wing of the squamosal, a cavum supracochleare for the geniculate ganglion of the facial nerve that is not enclosed in the petrosal bone, a secondary facial foramen between the petrosal and squamosal, a secondary posttemporal foramen leading to the primary one, a subarcuate fossa that is floored in part by a large contribution from the squamosal, a body of the incus larger than the head of the malleus, and a crus longum of the incus that lacks an osseous connection to the lenticular process. Documentation of the anatomy of the Philippine flying lemur ear region is an essential first step in morphological phylogenetic analyses where features of the basicranium are widely sampled.

Rapid divergence of a gamete recognition gene promoted macroevolution of Eutheria

BackgroundSpeciation genes contribute disproportionately to species divergence, but few examples exist, especially in vertebrates. Here we test whether Zan, which encodes the sperm acrosomal protein zonadhesin that mediates species-specific adhesion to the egg’s zona pellucida, is a speciation gene in placental mammals.ResultsGenomic ontogeny reveals that Zan arose by repurposing of a stem vertebrate gene that was lost in multiple lineages but retained in Eutheria on acquiring a function in egg recognition. A 112-species Zan sequence phylogeny, representing 17 of 19 placental Orders, resolves all species into monophyletic groups corresponding to recognized Orders and Suborders, with <5% unsupported nodes. Three other rapidly evolving germ cell genes (Adam2, Zp2, and Prm1), a paralogous somatic cell gene (TectA), and a mitochondrial gene commonly used for phylogenetic analyses (Cytb) all yield trees with poorer resolution than the Zan tree and inferior topologies relative to a widely accepted mammalian supertree. Zan divergence by intense positive selection produces dramatic species differences in the protein’s properties, with ordinal divergence rates generally reflecting species richness of placental Orders consistent with expectations for a speciation gene that acts across a wide range of taxa. Furthermore, Zan’s combined phylogenetic utility and divergence exceeds those of all other genes known to have evolved in Eutheria by positive selection, including the only other mammalian speciation gene, Prdm9.ConclusionsSpecies-specific egg recognition conferred by Zan’s functional divergence served as a mode of prezygotic reproductive isolation that promoted the extraordinary adaptive radiation and success of Eutheria.

Odorant-binding proteins in canine anal sac glands indicate an evolutionarily conserved role in mammalian chemical communication

BackgroundChemical communication is an important aspect of the behavioural ecology of a wide range of mammals. In dogs and other carnivores, anal sac glands are thought to convey information to conspecifics by secreting a pallet of small volatile molecules produced by symbiotic bacteria. Because these glands are unique to carnivores, it is unclear how their secretions relate to those of other placental mammals that make use of different tissues and secretions for chemical communication. Here we analyse the anal sac glands of domestic dogs to verify the secretion of proteins and infer their evolutionary relationship to those involved in the chemical communication of non-carnivoran mammals.ResultsProteomic analysis of anal sac gland secretions of 17 dogs revealed the consistently abundant presence of three related proteins. Homology searches against online databases indicate that these proteins are evolutionary related to ‘odorant binding proteins’ (OBPs) found in a wide range of mammalian secretions and known to contribute to chemical communication. Screening of the dog’s genome sequence show that the newly discovered OBPs are encoded by a single cluster of three genes in the pseudoautosomal region of the X-chromosome. Comparative genomic screening indicates that the same locus is shared by a wide range of placental mammals and that it originated at least before the radiation of extant placental orders. Phylogenetic analyses suggest a dynamic evolution of gene duplication and loss, resulting in large gene clusters in some placental taxa and recurrent loss of this locus in others. The homology of OBPs in canid anal sac glands and those found in other mammalian secretions implies that these proteins maintained a function in chemical communication throughout mammalian evolutionary history by multiple shifts in expression between secretory tissues involved in signal release and nasal mucosa involved in signal reception.ConclusionsOur study elucidates a poorly understood part of the biology of a species that lives in close association with humans. In addition, it shows that the protein repertoire underlying chemical communication in mammals is more evolutionarily stable than the variation of involved glands and tissues would suggest.

The effects of fossil taxa, hypothetical predicted ancestors, and a molecular scaffold on pseudoextinction analyses of extant placental orders.

Pseudoextinction analyses, which simulate extinction in extant taxa, use molecular phylogenetics to assess the accuracy of morphological phylogenetics. Previous pseudoextinction analyses have shown a failure of morphological phylogenetics to place some individual placental orders in the correct superordinal clade. Recent work suggests that the inclusion of hypothetical ancestors of extant placental clades, estimated by ancestral state reconstructions of morphological characters, may increase the accuracy of morphological phylogenetic analyses. However, these studies reconstructed direct hypothetical ancestors for each extant taxon based on a well-corroborated molecular phylogeny, which is not possible for extinct taxa that lack molecular data. It remains to be determined if pseudoextinct taxa, and by proxy extinct taxa, can be accurately placed when their immediate hypothetical ancestors are unknown. To investigate this, we employed molecular scaffolds with the largest available morphological data set for placental mammals. Each placental order was sequentially treated as pseudoextinct by exempting it from the molecular scaffold and recoding soft morphological characters as missing for all its constituent species. For each pseudoextinct data set, we omitted the pseudoextinct taxon and performed a parsimony ancestral state reconstruction to obtain hypothetical predicted ancestors. Each pseudoextinct order was then evaluated in seven parsimony analyses that employed combinations of fossil taxa, hypothetical predicted ancestors, and a molecular scaffold. In treatments that included fossils, hypothetical predicted ancestors, and a molecular scaffold, only 8 of 19 pseudoextinct placental orders (42%) retained the same interordinal placement as on the molecular scaffold. In treatments that included hypothetical predicted ancestors but not fossils or a scaffold, only four placental orders (21%) were recovered in positions that are congruent with the scaffold. These results indicate that hypothetical predicted ancestors do not increase the accuracy of pseudoextinct taxon placement when the immediate hypothetical ancestor of the taxon is unknown. Hypothetical predicted ancestors are not a panacea for morphological phylogenetics.

The earliest Asian bats (Mammalia: Chiroptera) address major gaps in bat evolution.

Bats dispersed widely after evolving the capacity for powered flight, and fossil bats are known from the early Eocene of most continents. Until now, however, bats have been conspicuously absent from the early Eocene of mainland Asia. Here, we report two teeth from the Junggar Basin of northern Xinjiang, China belonging to the first known early Eocene bats from Asia, representing arguably the most plesiomorphic bat molars currently recognized. These teeth combine certain bat synapomorphies with primitive traits found in other placental mammals, thereby potentially illuminating dental evolution among stem bats. The Junggar Basin teeth suggest that the dentition of the stem chiropteran family Onychonycteridae is surprisingly derived, although their postcranial anatomy is more primitive than that of any other Eocene bats. Additional comparisons with stem bat families Icaronycteridae and Archaeonycteridae fail to identify unambiguous synapomorphies for the latter taxa, raising the possibility that neither is monophyletic as currently recognized. The presence of highly plesiomorphic bats in the early Eocene of central Asia suggests that this region was an important locus for the earliest, transitional phases of bat evolution, as has been demonstrated for other placental mammal orders including Lagomorpha and Rodentia.

Astrapotherium from the Middle Miocene Collón Cura Formation and the Decline of Astrapotheres in Southern South America

Astrapotherium is the better-known member of the placental Order Astrapotheria. This large herbivorous inhabited the Patagonian ecosystems during Early and middle Miocene times. The genus is widely represented in the Early Miocene Santa Cruz Formation, with a dozen of nominal species, of which A. magnum and A. burmeisteri are the only ones herein considered as valid. The middle Miocene record was limited to few fragmentary remains from the Rio Frias Formation and presumably from the Collon Cura Formation, described as A. hesperinum Cabrera 1940, here interpreted as nomen vanum. Here we describe an almost complete skull with associated mandible derived from the Collon Cura Formation in the vicinities of Comallo, in Rio Negro Province (Argentina). It is largely the most complete astrapothere material from middle Miocene rocks of high latitudes, and it is referred to a new species, Astrapotherium guillei. It differs from the remaining species essentially in lacking P3, achieved convergently with the latest diverging uruguaytheriines. The astrapotheriines diversified in high latitudes during the Early Miocene, but they retained an stereotyped morphotype and became progressively less diverse, unlike their Northern counterparts (the Uruguaytheriinae). Astrapotherium guillei is the latest known Patagonian astrapothere and represents the final expression of the Astrapotheriinae´s decline. doi: 10.5710/AMGH.15.07.2019.3258

Data partitioning and correction for ascertainment bias reduce the uncertainty of placental mammal divergence times inferred from the morphological clock.

Bayesian estimates of divergence times based on the molecular clock yield uncertainty of parameter estimates measured by the width of posterior distributions of node ages. For the relaxed molecular clock, previous works have reported that some of the uncertainty inherent to the variation of rates among lineages may be reduced by partitioning data. Here we test this effect for the purely morphological clock, using placental mammals as a case study. We applied the uncorrelated lognormal relaxed clock to morphological data of 40 extant mammalian taxa and 4,533 characters, taken from the largest published matrix of discrete phenotypic characters. The morphologically derived timescale was compared to divergence times inferred from molecular and combined data. We show that partitioning data into anatomical units significantly reduced the uncertainty of divergence time estimates for morphological data. For the first time, we demonstrate that ascertainment bias has an impact on the precision of morphological clock estimates. While analyses including molecular data suggested most divergences between placental orders occurred near the K‐Pg boundary, the partitioned morphological clock recovered older interordinal splits and some younger intraordinal ones, including significantly later dates for the radiation of bats and rodents, which accord to the short‐fuse hypothesis.

Mammalian Auditory Cortex Structure as the Basis of Cortical Sound Processing

The basic morphological aspects of auditory cortex organization in different orders of eutherian mammals are considered in the present review. The modern data describing a partitioning of mammalian auditory cortex into subfields are presented. A detailed observation of the structural organization of primary auditory cortex is given, as well as a review of recent morphological data about secondary auditory areas. Another section describes the system of auditory cortical projections. The data are considered from the perspective of possible homologies existing between the auditory cortices in different mammalian species.

Genomic evidence reveals a radiation of placental mammals uninterrupted by the KPg boundary

The timing of the diversification of placental mammals relative to the Cretaceous-Paleogene (KPg) boundary mass extinction remains highly controversial. In particular, there have been seemingly irreconcilable differences in the dating of the early placental radiation not only between fossil-based and molecular datasets but also among molecular datasets. To help resolve this discrepancy, we performed genome-scale analyses using 4,388 loci from 90 taxa, including representatives of all extant placental orders and transcriptome data from flying lemurs (Dermoptera) and pangolins (Pholidota). Depending on the gene partitioning scheme, molecular clock model, and genic deviation from molecular clock assumptions, extensive sensitivity analyses recovered widely varying diversification scenarios for placental mammals from a given gene set, ranging from a deep Cretaceous origin and diversification to a scenario spanning the KPg boundary, suggesting that the use of suboptimal molecular clock markers and methodologies is a major cause of controversies regarding placental diversification timing. We demonstrate that reconciliation between molecular and paleontological estimates of placental divergence times can be achieved using the appropriate clock model and gene partitioning scheme while accounting for the degree to which individual genes violate molecular clock assumptions. A birth-death-shift analysis suggests that placental mammals underwent a continuous radiation across the KPg boundary without apparent interruption by the mass extinction, paralleling a genus-level radiation of multituberculates and ecomorphological diversification of both multituberculates and therians. These findings suggest that the KPg catastrophe evidently played a limited role in placental diversification, which, instead, was likely a delayed response to the slightly earlier radiation of angiosperms.

Inactivation of thermogenic UCP1 as a historical contingency in multiple placental mammal clades.

Mitochondrial uncoupling protein 1 (UCP1) is essential for nonshivering thermogenesis in brown adipose tissue and is widely accepted to have played a key thermoregulatory role in small-bodied and neonatal placental mammals that enabled the exploitation of cold environments. We map ucp1 sequences from 133 mammals onto a species tree constructed from a ~51-kb sequence alignment and show that inactivating mutations have occurred in at least 8 of the 18 traditional placental orders, thereby challenging the physiological importance of UCP1 across Placentalia. Selection and timetree analyses further reveal that ucp1 inactivations temporally correspond with strong secondary reductions in metabolic intensity in xenarthrans and pangolins, or in six other lineages coincided with a ~30 million-year episode of global cooling in the Paleogene that promoted sharp increases in body mass and cladogenesis evident in the fossil record. Our findings also demonstrate that members of various lineages (for example, cetaceans, horses, woolly mammoths, Steller's sea cows) evolved extreme cold hardiness in the absence of UCP1-mediated thermogenesis. Finally, we identify ucp1 inactivation as a historical contingency that is linked to the current low species diversity of clades lacking functional UCP1, thus providing the first evidence for species selection related to the presence or absence of a single gene product.

RUNX2 repeat variation does not drive craniofacial diversity in marsupials

BackgroundRunt-related transcription factor 2 (RUNX2) is a transcription factor essential for skeletal development. Variation within the RUNX2 polyglutamine / polyalanine (QA) repeat is correlated with facial length within orders of placental mammals and is suggested to be a major driver of craniofacial diversity. However, it is not known if this correlation exists outside of the placental mammals.ResultsHere we examined the correlation between the RUNX2 QA repeat ratio and facial length in the naturally evolving sister group to the placental mammals, the marsupials. Marsupials have a diverse range of facial lengths similar to that seen in placental mammals. Despite their diversity there was almost no variation seen in the RUNX2 QA repeat across individuals spanning the entire marsupial infraclass. The extreme conservation of the marsupial RUNX2 QA repeat indicates it is under strong purifying selection. Despite this, we observed an unexpectedly high level of repeat purity.ConclusionsUnlike within orders of placental mammals, RUNX2 repeat variation cannot drive craniofacial diversity in marsupials. We propose conservation of the marsupial RUNX2 QA repeat is driven by the constraint of accelerated ossification of the anterior skeleton to facilitate life in the pouch. Thus, marsupials must utilize alternate pathways to placental mammals to drive craniofacial evolution.

Systematics and stratigraphical range of the hegetotheriids Hegetotheriopsis sulcatus and Prohegetotherium sculptum (Mammalia: Notoungulata)

Hegetotheriidae is one of the most advanced clades within the endemic South American placental Order Notoungulata. The species Hegetotheriopsis sulcatus Kramarz & Paz, 2013 differs from all other known hegetotheriids in having a peculiar combination of cranial and dental features, some of them shared with Archaeohyracidae (sister group of Hegetotheriidae). A previous cladistic analysis supported H. sulcatus as the earliest diverging hegetotheriid. Nevertheless, a more recent analysis, based on a different data matrix, concluded that this species is an advanced form within the family, with the little-known Prohegetotherium sculptum Ameghino, 1897 (late Oligocene) being the most basal taxon. Here we present a revision of the concept and the content of P. sculptum based on a re-examination of the type specimens. We find that this material exhibits several dental and cranial characters not recognized in all previous studies; we conclude that no specimen other than the types can be assigned to P. sculptum, and that all the synonymies previously proposed (i.e. P. shumwayi and P. crassus) are unfounded. A new cladistic analysis, combining characters from the two aforementioned analyses, confirms the position of H. sulcatus as the earliest diverging hegetotheriid. The taxon was originally described based on remains from early Miocene deposits in central and northern Patagonia (Sarmiento, Chichinales and Cerro Bandera formations). Here we report new material from the late Oligocene of Cabeza Blanca (central Patagonia), and reassign other material previously attributed to Prohegetotherium from presumably equivalent levels at Quebrada Fiera (central West Argentina). These remains extend the occurrence of H. sulcatus back to the late Oligocene, and fill an important gap of the early record of Hegetotheriidae.

Pangolin genomes and the evolution of mammalian scales and immunity.

Pangolins, unique mammals with scales over most of their body, no teeth, poor vision, and an acute olfactory system, comprise the only placental order (Pholidota) without a whole-genome map. To investigate pangolin biology and evolution, we developed genome assemblies of the Malayan (Manis javanica) and Chinese (M. pentadactyla) pangolins. Strikingly, we found that interferon epsilon (IFNE), exclusively expressed in epithelial cells and important in skin and mucosal immunity, is pseudogenized in all African and Asian pangolin species that we examined, perhaps impacting resistance to infection. We propose that scale development was an innovation that provided protection against injuries or stress and reduced pangolin vulnerability to infection. Further evidence of specialized adaptations was evident from positively selected genes involving immunity-related pathways, inflammation, energy storage and metabolism, muscular and nervous systems, and scale/hair development. Olfactory receptor gene families are significantly expanded in pangolins, reflecting their well-developed olfaction system. This study provides insights into mammalian adaptation and functional diversification, new research tools and questions, and perhaps a new natural IFNE-deficient animal model for studying mammalian immunity.

A mixed relaxed clock model

Over recent years, several alternative relaxed clock models have been proposed in the context of Bayesian dating. These models fall in two distinct categories: uncorrelated and autocorrelated across branches. The choice between these two classes of relaxed clocks is still an open question. More fundamentally, the true process of rate variation may have both long-term trends and short-term fluctuations, suggesting that more sophisticated clock models unfolding over multiple time scales should ultimately be developed. Here, a mixed relaxed clock model is introduced, which can be mechanistically interpreted as a rate variation process undergoing short-term fluctuations on the top of Brownian long-term trends. Statistically, this mixed clock represents an alternative solution to the problem of choosing between autocorrelated and uncorrelated relaxed clocks, by proposing instead to combine their respective merits. Fitting this model on a dataset of 105 placental mammals, using both node-dating and tip-dating approaches, suggests that the two pure clocks, Brownian and white noise, are rejected in favour of a mixed model with approximately equal contributions for its uncorrelated and autocorrelated components. The tip-dating analysis is particularly sensitive to the choice of the relaxed clock model. In this context, the classical pure Brownian relaxed clock appears to be overly rigid, leading to biases in divergence time estimation. By contrast, the use of a mixed clock leads to more recent and more reasonable estimates for the crown ages of placental orders and superorders. Altogether, the mixed clock introduced here represents a first step towards empirically more adequate models of the patterns of rate variation across phylogenetic trees.This article is part of the themed issue ‘Dating species divergences using rocks and clocks’.

Cool sperm: why some placental mammals have a scrotum.

Throughout the Cenozoic, the fitness benefits of the scrotum in placental mammals presumably outweighed the fitness costs through damage, yet a definitive hypothesis for its evolution remains elusive. Here, I present an hypothesis (Endothermic Pulses Hypothesis) which argues that the evolution of the scrotum was driven by Cenozoic pulses in endothermy, that is, increases in normothermic body temperature, which occurred in Boreotheria (rodents, primates, lagomorphs, carnivores, bats, lipotyphylans and ungulates) in response to factors such as cursoriality and climate adaptation. The model argues that stabilizing selection maintained an optimum temperature for spermatogenesis and sperm storage throughout the Cenozoic at the lower plesiomorphic levels of body temperature that prevailed in ancestral mammals for at least 163million years. Evolutionary stasis may have been driven by reduced rates of germ-cell mutations at lower body temperatures. Following the extinction of the dinosaurs at the Cretaceous-Palaeogene boundary 65.5mya, immediate pulses in endothermy occurred associated with the dramatic radiation of the modern placental mammal orders. The fitness advantages of an optimum temperature of spermatogenesis outweighed the potential costs of testes externalization and paved the way for the evolution of the scrotum. The scrotum evolved within several hundred thousand years of the K-Pg extinction, probably associated initially with the evolution of cursoriality, and arguably facilitated mid- and late Cenozoic metabolic adaptations to factors such as climate, flight in bats and sociality in primates.