From teeth to pad: tooth loss and development of keratinous structures in sirenians.

Sirenians are a well-known example of morphological adaptation to a shallow-water grazing diet characterized by a modified feeding apparatus and orofacial morphology. Such adaptations were accompanied by an anterior tooth reduction associated with the development of keratinized pads, the evolution of which remains elusive. Among sirenians, the recently extinct Steller's sea cow represents a special case for being completely toothless. Here, we used µ-CT scans of sirenian crania to understand how motor-sensor systems associated with tooth innervation responded to innovations such as keratinized pads and continuous dental replacement. In addition, we surveyed nine genes associated with dental reduction for signatures of loss of function. Our results reveal how patterns of innervation changed with modifications of the dental formula, especially continuous replacement in manatees. Both our morphological and genomic data show that dental development was not completely lost in the edentulous Steller's sea cows. By tracing the phylogenetic history of tooth innervation, we illustrate the role of development in promoting the innervation of keratinized pads, similar to the secondary use of dental canals for innervating neomorphic keratinized structures in other tetrapod groups.

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales.

Ontogeny plays a key role in the evolution of organisms, as changes during the complex processes of development can allow for new traits to arise. Identifying changes in ontogenetic allometry-the relationship between skull shape and size during growth-can reveal the processes underlying major evolutionary transformations. Baleen whales (Mysticeti, Cetacea) underwent major morphological changes in transitioning from their ancestral raptorial feeding mode to the three specialized filter-feeding modes observed in extant taxa. Heterochronic processes have been implicated in the evolution of these feeding modes, and their associated specialized cranial morphologies, but their role has never been tested with quantitative data. Here, we quantified skull shapes ontogeny and reconstructed ancestral allometric trajectories using 3D geometric morphometrics and phylogenetic comparative methods on sample representing modern mysticetes diversity. Our results demonstrate that Mysticeti, while having a common developmental trajectory, present distinct cranial shapes from early in their ontogeny corresponding to their different feeding ecologies. Size is the main driver of shape disparity across mysticetes. Disparate heterochronic processes are evident in the evolution of the group: skim feeders present accelerated growth relative to the ancestral nodes, while Balaenopteridae have overall slower growth, or pedomorphosis. Gray whales are the only taxon with a relatively faster rate of growth in this group, which might be connected to its unique benthic feeding strategy. Reconstructed ancestral allometries and related skull shapes indicate that extinct taxa used less specialized filter-feeding modes, a finding broadly in line with the available fossil evidence.

Pedomorphosis in the ancestry of marsupial mammals.

Within mammals, different reproductive strategies (e.g., egg laying, live birth of extremely underdeveloped young, and live birth of well-developed young) have been linked to divergent evolutionary histories. How and when developmental variation across mammals arose is unclear. While egg laying is unquestionably considered the ancestral state for all mammals, many long-standing biases treat the extreme underdeveloped state of marsupial young as the ancestral state for therian mammals (clade including both marsupials and placentals), with the well-developed young of placentals often considered the derived mode of development. Here, we quantify mammalian cranial morphological development and estimate ancestral patterns of cranial shape development using geometric morphometric analysis of the largest comparative ontogenetic dataset of mammals to date (165 specimens, 22 species). We identify a conserved region of cranial morphospace for fetal specimens, after which cranial morphology diversified through ontogeny in a cone-shaped pattern. This cone-shaped pattern of development distinctively reflected the upper half of the developmental hourglass model. Moreover, cranial morphological variation was found to be significantly associated with the level of development (position on the altricial-precocial spectrum) exhibited at birth. Estimation of ancestral state allometry (size-related shape change) reconstructs marsupials as pedomorphic relative to the ancestral therian mammal. In contrast, the estimated allometries for the ancestral placental and ancestral therian were indistinguishable. Thus, from our results, we hypothesize that placental mammal cranial development most closely reflects that of the ancestral therian mammal, while marsupial cranial development represents a more derived mode of mammalian development, in stark contrast to many interpretations of mammalian evolution.

The ontogeny of asymmetry in echolocating whales.

Extreme asymmetry of the skull is one of the most distinctive traits that characterizes toothed whales (Odontoceti, Cetacea). The origin and function of cranial asymmetry are connected to the evolution of echolocation, the ability to use high-frequency sounds to navigate the surrounding environment. Although this novel phenotype must arise through changes in cranial development, the ontogeny of cetacean asymmetry has never been investigated. Here we use three-dimensional geometric morphometrics to quantify the changes in degree of asymmetry and skull shape during prenatal and postnatal ontogeny for five genera spanning odontocete diversity (oceanic dolphins, porpoises and beluga). Asymmetry in early ontogeny starts low and tracks phylogenetic relatedness of taxa. Distantly related taxa that share aspects of their ecology overwrite these initial differences via heterochronic shifts, ultimately converging on comparable high levels of skull asymmetry. Porpoises maintain low levels of asymmetry into maturity and present a decelerated rate of growth, probably retained from the ancestral condition. Ancestral state reconstruction of allometric trajectories demonstrates that both paedomorphism and peramorphism contribute to cranial shape diversity across odontocetes. This study provides a striking example of how divergent developmental pathways can produce convergent ecological adaptations, even for some of the most unusual phenotypes exhibited among vertebrates.

Museum genomics reveals the rapid decline and extinction of Australian rodents since European settlement.

Australia has the highest historically recorded rate of mammalian extinction in the world, with 34 terrestrial species declared extinct since European colonization in 1788. Among Australian mammals, rodents have been the most severely affected by these recent extinctions; however, given a sparse historical record, the scale and timing of their decline remain unresolved. Using museum specimens up to 184 y old, we generate genomic-scale data from across the entire assemblage of Australian hydromyine rodents (i.e., eight extinct species and their 42 living relatives). We reconstruct a phylogenomic tree for these species spanning ∼5.2 million years, revealing a cumulative total of 10 million years (>10%) of unique evolutionary history lost to extinction within the past ∼150 y. We find no evidence for reduced genetic diversity in extinct species just prior to or during decline, indicating that their extinction was extremely rapid. This suggests that populations of extinct Australian rodents were large prior to European colonization, and that genetic diversity does not necessarily protect species from catastrophic extinction. In addition, comparative analyses suggest that body size and biome interact to predict extinction and decline, with larger species more likely to go extinct. Finally, we taxonomically resurrect a species from extinction, Gould's mouse (Pseudomys gouldii Waterhouse, 1839), which survives as an island population in Shark Bay, Western Australia (currently classified as Pseudomys fieldi Waite, 1896). With unprecedented sampling across a radiation of extinct and living species, we unlock a previously inaccessible historical perspective on extinction in Australia. Our results highlight the capacity of collections-based research to inform conservation and management of persisting species.

Functional constraints during development limit jaw shape evolution in marsupials.

Differences in jaw function experienced through ontogeny can have striking consequences for evolutionary outcomes, as has been suggested for the major clades of mammals. By contrast to placentals, marsupial newborns have an accelerated development of the head and forelimbs, allowing them to crawl to the mother's teats to suckle within just a few weeks of conception. The different functional requirements that marsupial newborns experience in early postnatal development have been hypothesized to have constrained their morphological diversification relative to placentals. Here, we test whether marsupials have a lower ecomorphological diversity and rate of evolution in comparison with placentals, focusing specifically on their jaws. To do so, a geometric morphometric approach was used to characterize jaw shape for 151 living and extinct species of mammals spanning a wide phylogenetic, developmental and functional diversity. Our results demonstrate that jaw shape is significantly influenced by both reproductive mode and diet, with substantial ecomorphological convergence between metatherians and eutherians. However, metatherians have markedly lower disparity and rate of mandible shape evolution than observed for eutherians. Thus, despite their ecomorphological diversity and numerous convergences with eutherians, the evolution of the jaw in metatherians appears to be strongly constrained by their specialized reproductive biology.

New mitogenomic lineages in Papio baboons and their phylogeographic implications.

OBJECTIVES: Incomplete and/or biased sampling either on a taxonomic or geographic level can lead to delusive phylogenetic and phylogeographic inferences. However, a complete taxonomic and geographical sampling is often and for various reasons impossible, particularly for widespread taxa such as baboons (Papio spp.). Previous studies on baboon phylogeography identified several sampling gaps, some of which we fill by investigating additional material including samples from museum specimens. MATERIALS AND METHODS: We generated 10 new mitochondrial genomes either via conventional PCR and subsequent Sanger sequencing from two blood samples or via high-throughput shotgun sequencing from degraded DNA extracted from eight museum specimens. Phylogenetic relationships and divergence times among baboon lineages were determined using maximum-likelihood and Bayesian inferences. RESULTS: We identified new mitochondrial lineages in baboons from Central Africa (Chad, the Central African Republic), from the Mahale, and the Udzungwa Mountains (Tanzania), with the latter likely representing a case of mitochondrial capture from sympatric kipunjis (Rungwecebus kipunji). We also found that the mitochondrial clades of olive baboons found in Ivory Coast and Tanzania extend into Niger and the Democratic Republic of Congo, respectively. Moreover, an olive baboon from Sierra Leone carries a mitochondrial haplotype usually found in Guinea baboons, suggesting gene flow between these two species. DISCUSSION: The extension of the geographic sampling by including samples from areas difficult to visit or from populations that are most likely extirpated has improved the geographic and temporal resolution of the mitochondrial phylogeny of baboons considerably. Our study also shows the great value of museum material for genetic analyses even when DNA is highly degraded.

The genome sequence of the eastern grey squirrel, Sciurus carolinensis Gmelin, 1788.

We present a genome assembly from an individual male Sciurus carolinensis (the eastern grey squirrel; Vertebrata; Mammalia; Eutheria; Rodentia; Sciuridae). The genome sequence is 2.82 gigabases in span. The majority of the assembly (92.3%) is scaffolded into 21 chromosomal-level scaffolds, with both X and Y sex chromosomes assembled.

The genome sequence of the Eurasian red squirrel, Sciurus vulgaris Linnaeus 1758.

We present a genome assembly from an individual male Sciurus vulgaris (the Eurasian red squirrel; Vertebrata; Mammalia; Eutheria; Rodentia; Sciuridae). The genome sequence is 2.88 gigabases in span. The majority of the assembly is scaffolded into 21 chromosomal-level scaffolds, with both X and Y sex chromosomes assembled.

The genome sequence of the Eurasian river otter, Lutra lutra Linnaeus 1758.

We present a genome assembly from an individual male Lutra lutra (the Eurasian river otter; Vertebrata; Mammalia; Eutheria; Carnivora; Mustelidae). The genome sequence is 2.44 gigabases in span. The majority of the assembly is scaffolded into 20 chromosomal pseudomolecules, with both X and Y sex chromosomes assembled.

Sex biases in bird and mammal natural history collections.

Natural history specimens are widely used across ecology, evolutionary biology and conservation. Although biological sex may influence all of these areas, it is often overlooked in large-scale studies using museum specimens. If collections are biased towards one sex, studies may not be representative of the species. Here, we investigate sex ratios in over two million bird and mammal specimen records from five large international museums. We found a slight bias towards males in birds (40% females) and mammals (48% females), but this varied among orders. The proportion of female specimens has not significantly changed in 130 years, but has decreased in species with showy male traits like colourful plumage and horns. Body size had little effect. Male bias was strongest in name-bearing types; only 27% of bird and 39% of mammal types were female. These results imply that previous studies may be impacted by undetected male bias, and vigilance is required when using specimen data, collecting new specimens and designating types.