To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic ...characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.
The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been ...studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull's major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation. This article is part of the theme issue 'The mammalian skull: development, structure and function'.
The family Phyllostomidae is recognized as representing the most extensive radiation known in any mammalian family. Creating a Linnaean classification for this clade has been difficult and ...controversial. In two companion papers, we here propose a revised classification drawing on the strengths of genetic and morphological data and reflecting current ideas regarding phylogenetic relationships within this monophyletic clade. We recognize 11 subfamilies (Macrotinae, Micronycterinae, Desmodontinae, Phyllostominae, Glossophaginae, Lonchorhininae, Lonchophyllinae, Glyphonycterinae, Carolliinae, Rhinophyllinae, and Stenodermatinae), 12 tribes (Diphyllini, Desmodontini, Macrophyllini, Phyllostomini, Vampyrini, Glossophagnini, Brachyphyllini, Choeronycterini, Lonchophyllini, Hsunycterini, Sturnirini, and Stenodermatini), and nine subtribes (Brachyphyllina, Phyllonycterina, Anourina, Choeronycterina, Vampyressina, Enchisthenina, Ectophyllina, Artibeina, and Stenodermatina). The proposed arrangement avoids non-monophyletic associations, only keeping those detected based on analyses of DNA sequence data. We propose that a classification based on the strengths of the most complete morphological and genetic data sets will provide the most robust classification for multiple uses by science and society.
Mercury (Hg) is a persistent and widespread heavy metal with neurotoxic effects in wildlife. While bioaccumulation of Hg has historically been studied in aquatic food webs, terrestrial consumers can ...become contaminated with Hg when they feed on aquatic organisms (e.g., emergent aquatic insects, fish, and amphibians). However, the extent to which dietary connectivity to aquatic ecosystems can explain patterns of Hg bioaccumulation in terrestrial consumers has not been well studied. Bats (Order: Chiroptera) can serve as a model system for illuminating the trophic transfer of Hg given their high dietary diversity and foraging links to both aquatic and terrestrial food webs. Here we quantitatively characterize the dietary correlates of long-term exposure to Hg across a diverse local assemblage of bats in Belize and more globally across bat species from around the world with a comparative analysis of hair samples. Our data demonstrate considerable interspecific variation in hair total Hg concentrations in bats that span three orders of magnitude across species, ranging from 0.04 mg/kg in frugivorous bats (Artibeus spp.) to 145.27 mg/kg in the piscivorous Noctilio leporinus. Hg concentrations showed strong phylogenetic signal and were best explained by dietary connectivity of bat species to aquatic food webs. Our results highlight that phylogeny can be predictive of Hg concentrations through similarity in diet and how interspecific variation in feeding strategies influences chronic exposure to Hg and enables movement of contaminants from aquatic to terrestrial ecosystems.
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•Total mercury was determined in hair from 98 bats from 22 species in Belize.•Dietary guild was the best predictor of hair THg in Belizean bats.•Frugivores had lowest THg (μ = 0.04 mg/kg) while a single piscivore (Noctilio leporinus) showed highest THg (145.27 mg/kg).•Hair THg showed strong phylogenetic signal across 50 bat species from this study and the literature (Pagel's λ = 0.97).•Bat species that consumed more potentially aquatic prey (e.g., invertebrates, ectotherms, fish) showed the highest THg.
Background
The neotropical leaf‐nosed bats (Chiroptera, Phyllostomidae) are an ecologically diverse group of mammals with distinctive morphological adaptations associated with specialized modes of ...feeding. The dramatic skull shape changes between related species result from changes in the craniofacial development process, which brings into focus the nature of the underlying evolutionary developmental processes.
Results
In this study, we use three‐dimensional geometric morphometrics to describe, quantify, and compare morphological modifications unfolding during evolution and development of phyllostomid bats. We examine how changes in development of the cranium may contribute to the evolution of the bat craniofacial skeleton. Comparisons of ontogenetic trajectories to evolutionary trajectories reveal two separate evolutionary developmental growth processes contributing to modifications in skull morphogenesis: acceleration and hypermorphosis.
Conclusion
These findings are consistent with a role for peramorphosis, a form of heterochrony, in the evolution of bat dietary specialists.
Key Findings
The analyses comparing evolutionary and developmental patterns in morphology uncovered two distinct heterochronic processes, hypermorphosis and acceleration, in the evolution of fruit, nectar and vampire bats.
The results from our report present the first clear example of peramorphosis in morphologically and ecologically varied mammalian group, which provides a useful model for understanding the role and consequences of adaptive evolution and lays groundwork for further studies of its genetic mechanisms.
We anticipate that our study will stimulate attempts to quantitatively discover the signature of peramorphosis and terminal addition in other adaptive radiations.
Human activities create novel food resources that can alter wildlife–pathogen interactions. If resources amplify or dampen, pathogen transmission probably depends on both host ecology and pathogen ...biology, but studies that measure responses to provisioning across both scales are rare. We tested these relationships with a 4-year study of 369 common vampire bats across 10 sites in Peru and Belize that differ in the abundance of livestock, an important anthropogenic food source. We quantified innate and adaptive immunity from bats and assessed infection with two common bacteria. We predicted that abundant livestock could reduce starvation and foraging effort, allowing for greater investments in immunity. Bats from high-livestock sites had higher microbicidal activity and proportions of neutrophils but lower immunoglobulin G and proportions of lymphocytes, suggesting more investment in innate relative to adaptive immunity and either greater chronic stress or pathogen exposure. This relationship was most pronounced in reproductive bats, which were also more common in high-livestock sites, suggesting feedbacks between demographic correlates of provisioning and immunity. Infection with both Bartonella and haemoplasmas were correlated with similar immune profiles, and both pathogens tended to be less prevalent in high-livestock sites, although effects were weaker for haemoplasmas. These differing responses to provisioning might therefore reflect distinct transmission processes. Predicting how provisioning alters host–pathogen interactions requires considering how both within-host processes and transmission modes respond to resource shifts.
This article is part of the theme issue ‘Anthropogenic resource subsidies and host–parasite dynamics in wildlife’.
Bats are increasingly studied as model systems for longevity and as natural hosts for some virulent viruses. Yet the ability to characterize immune mechanisms of viral tolerance and to quantify ...infection dynamics in wild bats is often limited by small sample volumes and few species-specific reagents. Here, we demonstrate how proteomics can overcome these limitations by using data-independent acquisition-based shotgun proteomics to survey the serum proteome of 17 vampire bats (Desmodus rotundus) from Belize. Using just 2 μL of sample and relatively short separations of undepleted serum digests, we identified 361 proteins across 5 orders of magnitude. Levels of immunological proteins in vampire bat serum were then compared to human plasma via published databases. Of particular interest were antiviral and antibacterial components, circulating 20S proteasome complex and proteins involved in redox activity. Lastly, we used known virus proteomes to putatively identify Rh186 from Macacine herpesvirus 3 and ORF1a from Middle East respiratory syndrome-related coronavirus, indicating that mass spectrometry-based techniques show promise for pathogen detection. Overall, these results can be used to design targeted mass-spectrometry assays to quantify immunological markers and detect pathogens. More broadly, our findings also highlight the application of proteomics in advancing wildlife immunology and pathogen surveillance.
Bats are the only mammals capable of powered flight. One of the oldest bats known from a complete skeleton is Onychonycteris finneyi from the Early Eocene (Green River Formation, Wyoming, 52.5 Ma). ...Estimated to weigh approximately 40 g, Onychonycteris exhibits the most primitive combination of characters thus far known for bats. Here, we reconstructed the aerofoil of the two known specimens, calculated basic aerodynamic variables and compared them with those of extant bats and gliding mammals. Onychonycteris appears in the edges of the morphospace for bats, underscoring the primitive conformation of its flight apparatus. Low aerodynamic efficiency is inferred for this extinct species as compared to any extant bat. When we estimated aerofoil variables in a model of Onychonycteris excluding the handwing, it closely approached the morphospace of extant gliding mammals. Addition of a handwing to the model lacking this structure results in a 2.3-fold increase in aspect ratio and a 28% decrease in wing loading, thus greatly enhancing aerodynamics. In the context of these models, the rapid evolution of the chiropteran handwing via genetically mediated developmental changes appears to have been a key transformation in the hypothesized transition from gliding to flapping in early bats.
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