A symmoriiform chondrichthyan braincase and the origin of chimaeroid fishes.

Chimaeroid fishes (Holocephali) are one of the four principal divisions of modern gnathostomes (jawed vertebrates). Despite only 47 described living species, chimaeroids are the focus of resurgent interest as potential archives of genomic data and for the unique perspective they provide on chondrichthyan and gnathostome ancestral conditions. Chimaeroids are also noteworthy for their highly derived body plan. However, like other living groups with distinctive anatomies, fossils have been of limited use in unravelling their evolutionary origin, as the earliest recognized examples already exhibit many of the specializations present in modern forms. Here we report the results of a computed tomography analysis of Dwykaselachus, an enigmatic chondrichthyan braincase from the ~280 million year old Karoo sediments of South Africa. Externally, the braincase is that of a symmoriid shark and is by far the most complete uncrushed example yet discovered. Internally, the morphology exhibits otherwise characteristically chimaeroid specializations, including the otic labyrinth arrangement and the brain space configuration relative to exceptionally large orbits. These results have important implications for our view of modern chondrichthyan origins, add robust structure to the phylogeny of early crown group gnathostomes, reveal preconditions that suggest an initial morpho-functional basis for the derived chimaeroid cranium, and shed new light on the chondrichthyan response to the extinction at the end of the Devonian period.

Drivers of longitudinal telomere dynamics in a long-lived bat species, Myotis myotis.

Age-related telomere shortening is considered a hallmark of the ageing process. However, a recent cross-sectional ageing study of relative telomere length (rTL) in bats failed to detect a relationship between rTL and age in the long-lived genus Myotis (M. myotis and M. bechsteinii), suggesting some other factors are responsible for driving telomere dynamics in these species. Here, we test if longitudinal rTL data show signatures of age-associated telomere attrition in M. myotis and differentiate which intrinsic or extrinsic factors are likely to drive telomere length dynamics. Using quantitative polymerase chain reaction, rTL was measured in 504 samples from a marked population, from Brittany, France, captured between 2013 and 2016. These represent 174 individuals with an age range of 0 to 7+ years. We find no significant relationship between rTL and age (p = .762), but demonstrate that within-individual rTL is highly variable from year to year. To investigate the heritability of rTL, a population pedigree (n = 1744) was constructed from genotype data generated from a 16-microsatellite multiplex, designed from an initial, low-coverage, Illumina genome for M. myotis. Heritability was estimated in a Bayesian, mixed model framework, and showed that little of the observed variance in rTL is heritable (h2  = 0.01-0.06). Rather, correlations of first differences, correlating yearly changes in telomere length and weather variables, demonstrate that, during the spring transition, average temperature, minimum temperature, rainfall and windspeed correlate with changes in longitudinal telomere dynamics. As such, rTL may represent a useful biomarker to quantify the physiological impact of various environmental stressors in bats.

The Birth and Death of Olfactory Receptor Gene Families in Mammalian Niche Adaptation.

The olfactory receptor (OR) gene families, which govern mammalian olfaction, have undergone extensive expansion and contraction through duplication and pseudogenization. Previous studies have shown that broadly defined environmental adaptations (e.g., terrestrial vs. aquatic) are correlated with the number of functional and non-functional OR genes retained. However, to date, no study has examined species-specific gene duplications in multiple phylogenetically divergent mammals to elucidate OR evolution and adaptation. Here, we identify the OR gene families driving adaptation to different ecological niches by mapping the fate of species-specific gene duplications in the OR repertoire of 94 diverse mammalian taxa, using molecular phylogenomic methods. We analyze >70,000 OR gene sequences mined from whole genomes, generated from novel amplicon sequencing data, and collated with data from previous studies, comprising one of the largest OR studies to date. For the first time, we demonstrate statistically significant patterns of OR species-specific gene duplications associated with the presence of a functioning vomeronasal organ. With respect to dietary niche, we uncover a novel link between a large number of duplications in OR family 5/8/9 and herbivory. Our results also highlight differences between social and solitary niches, indicating that a greater OR repertoire expansion may be associated with a solitary lifestyle. This study demonstrates the utility of species-specific duplications in elucidating gene family evolution, revealing how the OR repertoire has undergone expansion and contraction with respect to a number of ecological adaptations in mammals.

Olfactory receptor repertoire size in dinosaurs.

The olfactory bulb (OB) ratio is the size of the OB relative to the cerebral hemisphere, and is used to estimate the proportion of the forebrain devoted to smell. In birds, OB ratio correlates with the number of olfactory receptor (OR) genes and therefore has been used as a proxy for olfactory acuity. By coupling OB ratios with known OR gene repertoires in birds, we infer minimum repertoire sizes for extinct taxa, including non-avian dinosaurs, using phylogenetic modelling, ancestral state reconstruction and comparative genomics. We highlight a shift in the scaling of OB ratio to body size along the lineage leading to modern birds, demonstrating variable OR repertoires present in different dinosaur and crown-bird lineages, with varying factors potentially influencing sensory evolution in theropods. We investigate the ancestral sensory space available to extinct taxa, highlighting potential adaptations to ecological niches. Through combining morphological and genomic data, we show that, while genetic information for extinct taxa is forever lost, it is potentially feasible to investigate evolutionary trajectories in extinct genomes.

An early chondrichthyan and the evolutionary assembly of a shark body plan.

Although relationships among the major groups of living gnathostomes are well established, the relatedness of early jawed vertebrates to modern clades is intensely debated. Here, we provide a new description of Gladbachus, a Middle Devonian (Givetian approx. 385-million-year-old) stem chondrichthyan from Germany, and one of the very few early chondrichthyans in which substantial portions of the endoskeleton are preserved. Tomographic and histological techniques reveal new details of the gill skeleton, hyoid arch and jaws, neurocranium, cartilage, scales and teeth. Despite many features resembling placoderm or osteichthyan conditions, phylogenetic analysis confirms Gladbachus as a stem chondrichthyan and corroborates hypotheses that all acanthodians are stem chondrichthyans. The unfamiliar character combination displayed by Gladbachus, alongside conditions observed in acanthodians, implies that pre-Devonian stem chondrichthyans are severely under-sampled and strongly supports indications from isolated scales that the gnathostome crown group originated at the latest by the early Silurian (approx. 440 Ma). Moreover, phylogenetic results highlight the likely convergent evolution of conventional chondrichthyan conditions among earliest members of this primary gnathostome division, while skeletal morphology points towards the likely suspension feeding habits of Gladbachus, suggesting a functional origin of the gill slit condition characteristic of the vast majority of living and fossil chondrichthyans.

Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes.

Acanthodians, an exclusively Palaeozoic group of fish, are central to a renewed debate on the origin of modern gnathostomes: jawed vertebrates comprising Chondrichthyes (sharks, rays and ratfish) and Osteichthyes (bony fishes and tetrapods). Acanthodian internal anatomy is primarily understood from Acanthodes bronni because it remains the only example preserved in substantial detail, central to which is an ostensibly osteichthyan braincase. For this reason, Acanthodes has become an indispensible component in early gnathostome phylogenies. Here we present a new description of the Acanthodes braincase, yielding new details of external and internal morphology, notably the regions surrounding and within the ear capsule and neurocranial roof. These data contribute to a new reconstruction that, unexpectedly, resembles early chondrichthyan crania. Principal coordinates analysis of a character-taxon matrix including these new data confirms this impression: Acanthodes is quantifiably closer to chondrichthyans than to osteichthyans. However, phylogenetic analysis places Acanthodes on the osteichthyan stem, as part of a well-resolved tree that also recovers acanthodians as stem chondrichthyans and stem gnathostomes. As such, perceived chondrichthyan features of the Acanthodes cranium represent shared primitive conditions for crown group gnathostomes. Moreover, this increasingly detailed picture of early gnathostome evolution highlights ongoing and profound anatomical reorganization of vertebrate crania after the origin of jaws but before the divergence of living clades.

Patterns of orofacial clefting in the facial morphology of bats: a possible naturally occurring model of cleft palate.

A normal feature of the facial anatomy of many species of bat is the presence of bony discontinuities or clefts, which bear a remarkable similarity to orofacial clefts that occur in humans as a congenital pathology. These clefts occur in two forms: a midline cleft between the two premaxillae (analogous to the rare midline craniofacial clefts in humans) and bilateral paramedian clefts between the premaxilla and the maxillae (analogous to the typical cleft lip and palate in humans). Here, we describe the distribution of orofacial clefting across major bat clades, exploring the relationship of the different patterns of clefting to feeding mode, development of the vomeronasal organ, development of the nasolacrimal duct and mode of emission of the echolocation call in different bat groups. We also present the results of detailed radiographic and soft tissue dissections of representative examples of the two types of cleft. The midline cleft has arisen independently multiple times in bat phylogeny, whereas the paramedian cleft has arisen once and is a synapomorphy uniting the Rhinolophidae and Hipposideridae. In all cases examined, the bony cleft is filled in by a robust fibrous membrane, continuous with the periosteum of the margins of the cleft. In the paramedian clefts, this membrane splits to enclose the premaxilla but forms a loose fold laterally between the premaxilla and maxilla, allowing the premaxilla and nose-leaf to pivot dorsoventrally in the sagittal plane under the action of facial muscles attached to the nasal cartilages. It is possible that this is a specific adaptation for echolocation and/or aerial insectivory. Given the shared embryological location of orofacial clefts in bats and humans, it is likely that aspects of the developmental control networks that produce cleft lip and palate in humans may also be implicated in the formation of these clefts as a normal feature in some bats. A better understanding of craniofacial development in bats with and without clefts may therefore suggest avenues for research into abnormal craniofacial development in humans.

Complex body size trends in the evolution of sloths (Xenarthra: Pilosa).

BACKGROUND: Extant sloths present an evolutionary conundrum in that the two living genera are superficially similar (small-bodied, folivorous, arboreal) but diverged from one another approximately 30 million years ago and are phylogenetically separated by a radiation of medium to massive, mainly ground-dwelling, taxa. Indeed, the species in the two living genera are among the smallest, and perhaps most unusual, of the 50+ known sloth species, and must have independently and convergently evolved small size and arboreality. In order to accurately reconstruct sloth evolution, it is critical to incorporate their extinct diversity in analyses. Here, we used a dataset of 57 species of living and fossil sloths to examine changes in body mass mean and variance through their evolution, employing a general time-variable model that allows for analysis of evolutionary trends in continuous characters within clades lacking fully-resolved phylogenies, such as sloths. RESULTS: Our analyses supported eight models, all of which partition sloths into multiple subgroups, suggesting distinct modes of body size evolution among the major sloth lineages. Model-averaged parameter values supported trended walks in most clades, with estimated rates of body mass change ranging as high as 126 kg/million years for the giant ground sloth clades Megatheriidae and Nothrotheriidae. Inclusion of living sloth species in the analyses weakened reconstructed rates for their respective groups, with estimated rates for Megalonychidae (large to giant ground sloths and the extant two-toed sloth) were four times higher when the extant genus Choloepus was excluded. CONCLUSIONS: Analyses based on extant taxa alone have the potential to oversimplify or misidentify macroevolutionary patterns. This study demonstrates the impact that integration of data from the fossil record can have on reconstructions of character evolution and establishes that body size evolution in sloths was complex, but dominated by trended walks towards the enormous sizes exhibited in some recently extinct forms.

A dynamic global equilibrium in carnivoran diversification over 20 million years.

The ecological and evolutionary processes leading to present-day biological diversity can be inferred by reconstructing the phylogeny of living organisms, and then modelling potential processes that could have produced this genealogy. A more direct approach is to estimate past processes from the fossil record. The Carnivora (Mammalia) has both substantial extant species richness and a rich fossil record. We compiled species-level data for over 10 000 fossil occurrences of nearly 1400 carnivoran species. Using this compilation, we estimated extinction, speciation and net diversification for carnivorans through the Neogene (22-2 Ma), while simultaneously modelling sampling probability. Our analyses show that caniforms (dogs, bears and relatives) have higher speciation and extinction rates than feliforms (cats, hyenas and relatives), but lower rates of net diversification. We also find that despite continual species turnover, net carnivoran diversification through the Neogene is surprisingly stable, suggesting a saturated adaptive zone, despite restructuring of the physical environment. This result is strikingly different from analyses of carnivoran diversification estimated from extant species alone. Two intervals show elevated diversification rates (13-12 Ma and 4-3 Ma), although the precise causal factors behind the two peaks in carnivoran diversification remain open questions.

First tooth-set outside the jaws in a vertebrate.

Holocephalans (ratfish, rabbitfish and chimaeras) figure with increasing prominence in studies of gnathostome evolutionary biology. Here, we provide the first complete description of the teeth and toothplates of one of the earliest known holocephalans, Chondrenchelys problematica, including the first unambiguous evidence of a gnathostome with an extra-mandibular dentition. We further demonstrate that holocephalan toothplate ontogeny differs fundamentally from all other extant gnathostome examples, and show how the conjunction of these teeth and toothplates challenges the monophyly of an extinct chondrichthyan clade, the Petalodontiformes. Chondrenchelys provides a novel perspective on the evolution of dentitions in shark-like fishes, expands the known repertoire of gnathostome dental morphologies and offers a glimpse of radically new chondrichthyan ecomorphs, now lost from the modern biota, following the end-Devonian extinctions.

Congruence of morphologically-defined genera with molecular phylogenies.

Morphologically-defined mammalian and molluscan genera (herein "morphogenera") are significantly more likely to be monophyletic relative to molecular phylogenies than random, under 3 different models of expected monophyly rates: approximately 63% of 425 surveyed morphogenera are monophyletic and 19% are polyphyletic, although certain groups appear to be problematic (e.g., nonmarine, unionoid bivalves). Compiled nonmonophyly rates are probably extreme values, because molecular analyses have focused on "problem" taxa, and molecular topologies (treated herein as error-free) contain contradictory groupings across analyses for 10% of molluscan morphogenera and 37% of mammalian morphogenera. Both body size and geographic range, 2 key macroevolutionary and macroecological variables, show significant rank correlations between values for morphogenera and molecularly-defined clades, even when strictly monophyletic morphogenera are excluded from analyses. Thus, although morphogenera can be imperfect reflections of phylogeny, large-scale statistical treatments of diversity dynamics or macroevolutionary variables in time and space are unlikely to be misleading.

Brain-size evolution and sociality in Carnivora.

Increased encephalization, or larger brain volume relative to body mass, is a repeated theme in vertebrate evolution. Here we present an extensive sampling of relative brain sizes in fossil and extant taxa in the mammalian order Carnivora (cats, dogs, bears, weasels, and their relatives). By using Akaike Information Criterion model selection and endocranial volume and body mass data for 289 species (including 125 fossil taxa), we document clade-specific evolutionary transformations in encephalization allometries. These evolutionary transformations include multiple independent encephalization increases and decreases in addition to a remarkably static basal Carnivora allometry that characterizes much of the suborder Feliformia and some taxa in the suborder Caniformia across much of their evolutionary history, emphasizing that complex processes shaped the modern distribution of encephalization across Carnivora. This analysis also permits critical evaluation of the social brain hypothesis (SBH), which predicts a close association between sociality and increased encephalization. Previous analyses based on living species alone appeared to support the SBH with respect to Carnivora, but those results are entirely dependent on data from modern Canidae (dogs). Incorporation of fossil data further reveals that no association exists between sociality and encephalization across Carnivora and that support for sociality as a causal agent of encephalization increase disappears for this clade.

Diversity dynamics of Miocene mammals in relation to the history of tectonism and climate.

Continental biodiversity gradients result not only from ecological processes, but also from evolutionary and geohistorical processes involving biotic turnover in landscape and climatic history over millions of years. Here, we investigate the evolutionary and historical contributions to the gradient of increasing species richness with topographic complexity. We analysed a dataset of 418 fossil rodent species from western North America spanning 25 to 5 Ma. We compared diversification histories between tectonically active (Intermontane West) and quiescent (Great Plains) regions. Although diversification histories differed between the two regions, species richness, origination rate and extinction rate per million years were not systematically different over the 20 Myr interval. In the tectonically active region, the greatest increase in originations coincided with a Middle Miocene episode of intensified tectonic activity and global warming. During subsequent global cooling, species richness declined in the montane region and increased on the Great Plains. These results suggest that interactions between tectonic activity and climate change stimulate diversification in mammals. The elevational diversity gradient characteristic of modern mammalian faunas was not a persistent feature over geologic time. Rather, the Miocene rodent record suggests that the elevational diversity gradient is a transient feature arising during particular episodes of Earth's history.

Does encephalization correlate with life history or metabolic rate in Carnivora?

A recent analysis of brain size evolution reconstructed the plesiomorphic brain-body size allometry for the mammalian order Carnivora, providing an important reference frame for comparative analyses of encephalization (brain volume scaled to body mass). I performed phylogenetically corrected regressions to remove the effects of body mass, calculating correlations between residual values of encephalization with basal metabolic rate (BMR) and six life-history variables (gestation time, neonatal mass, weaning time, weaning mass, litter size, litters per year). No significant correlations were recovered between encephalization and any life-history variable or BMR, arguing against hypotheses relating encephalization to maternal energetic investment. However, after correcting for clade-specific adaptations, I recovered significant correlations for several variables, and further analysis revealed a conserved carnivoran reproductive strategy, linking degree of encephalization to the well-documented mammalian life-history trade-off between neonatal mass and litter size. This strategy of fewer, larger offspring correlating with increased encephalization remains intact even after independent changes in encephalization allometries in the evolutionary history of this clade.

The evolution of orbit orientation and encephalization in the Carnivora (Mammalia).

Evolutionary change in encephalization within and across mammalian clades is well-studied, yet relatively few comparative analyses attempt to quantify the impact of evolutionary change in relative brain size on cranial morphology. Because of the proximity of the braincase to the orbits, and the inter-relationships among ecology, sensory systems and neuroanatomy, a relationship has been hypothesized between orbit orientation and encephalization for mammals. Here, we tested this hypothesis in 68 fossil and living species of the mammalian order Carnivora, comparing orbit orientation angles (convergence and frontation) to skull length and encephalization. No significant correlations were observed between skull length and orbit orientation when all taxa were analysed. Significant correlations were observed between encephalization and orbit orientation; however, these were restricted to the families Felidae and Canidae. Encephalization is positively correlated with frontation in both families and negatively correlated with convergence in canids. These results indicate that no universal relationship exists between encephalization and orbit orientation for Carnivora. Braincase expansion impacts orbit orientation in specific carnivoran clades, the nature of which is idiosyncratic to the clade itself.

High-performance suction feeding in an early elasmobranch.

High-performance suction feeding is often presented as a classic innovation of ray-finned fishes, likely contributing to their remarkable evolutionary success, whereas sharks, with seemingly less sophisticated jaws, are generally portrayed as morphologically conservative throughout their history. Here, using a combination of computational modeling, physical modeling, and quantitative three-dimensional motion simulation, we analyze the cranial skeleton of one of the earliest known stem elasmobranchs, Tristychius arcuatus from the Middle Mississippian of Scotland. The feeding apparatus is revealed as highly derived, capable of substantial oral expansion, and with clear potential for high-performance suction feeding some 50 million years before the earliest osteichthyan equivalent. This exceptional jaw performance is not apparent from standard measures of ecomorphospace using two-dimensional data. Tristychius signals the emergence of entirely new chondrichthyan ecomorphologies in the aftermath of the end-Devonian extinction and highlights sharks as significant innovators in the early radiation of the modern vertebrate biota.

The evolution of encephalization in caniform carnivorans.

A weighted-average model, which reliably estimates endocranial volume from three external measurements of the neurocranium of extant taxa in the mammalian order Carnivora, was tested for its applicability to fossil taxa by comparing model-estimated endocranial volumes to known endocast volumes. The model accurately reproduces endocast volumes for a wide array of fossil taxa across the crown radiation of the Carnivora, three stem carnivoramorphan taxa, and Pleistocene fossils of two extant species. Applying this model to fossil taxa without known endocast volumes expanded the sample of fossil taxa with estimated brain volumes in the carnivoran suborder Caniformia from 11 to 60 taxa. This then allowed a comprehensive assessment of the evolution of relative brain size across this clade. An allometry of brain volume to body mass was calculated on phylogenetically independent contrasts for the set of extant taxa, and from this, log-transformed encephalization quotients (logEQs) were calculated for all taxa, extant, and fossil. A series of Mann-Whitney tests demonstrated that the distributions of logEQs for taxa early in caniform evolutionary history possessed significantly lower median logEQs than extant taxa. Median logEQ showed a pronounced shift around the Miocene-Pliocene transition. Support tests, based on likelihood ratios, demonstrated that the variances of these distributions also were significantly lower than among modern taxa, but logEQ variance increased gradually through the history of the clade, not abruptly. Reconstructions of ancestral logEQs using weighted squared-change parsimony demonstrate that increased encephalization is observed across all major caniform clades (with the possible exception of skunks) and that these increases were achieved in parallel, although an "ancestor-descendant differencing" method could not rule out drift as a hypothesis. Peculiarities in the estimated logEQs for the extinct caniform family Amphicyonidae were also investigated; these unusual patterns are likely due to a unique allometry in scaling brain to body size in this single clade.

Mechanisms behind active trends in body size evolution of the Canidae (Carnivora: Mammalia).

Clade-level interactions can impart trends on observed characters. In this study, origination and extinction events were compiled for the three subfamilies of the Canidae (dogs): Hesperocyoninae, Borophaginae, and Caninae. These events were binned into 2-million-year time slices, and median body masses were calculated for each time slice. Originations and extinctions were classified as "large" or "small" relative to these median values. Likelihood ratios demonstrate that originations were significantly biased from random in four time slices, while extinctions were never significantly different from random. Two models were chosen by the Akaike Information Criterion to describe the evolutionary dynamics of canid body size. Both proposed a consistent, significant bias toward larger originations, punctuated by episodic "pulses" of increased bias toward larger originations and a Quaternary "pulse" favoring smaller originations, tracking the Quaternary diversification of foxlike canids. These pulses correspond in each subfamily to periods of rapid taxonomic diversification and the appearances of morphologies associated with hypercarnivorous diets. Together, the diversity data, the appearance of hypercarnivory, and the biases in originations document competitive interactions between Hesperocyoninae and Borophaginae and suggest that body size trends were driven, in part, by clade-level dynamics in the Canidae.

The Identification of a 1916 Irish Rebel: New Approach for Estimating Relatedness From Low Coverage Homozygous Genomes.

Thomas Kent was an Irish rebel who was executed by British forces in the aftermath of the Easter Rising armed insurrection of 1916 and buried in a shallow grave on Cork prison's grounds. In 2015, ninety-nine years after his death, a state funeral was offered to his living family to honor his role in the struggle for Irish independence. However, inaccuracies in record keeping did not allow the bodily remains that supposedly belonged to Kent to be identified with absolute certainty. Using a novel approach based on homozygous single nucleotide polymorphisms, we identified these remains to be those of Kent by comparing his genetic data to that of two known living relatives. As the DNA degradation found on Kent's DNA, characteristic of ancient DNA, rendered traditional methods of relatedness estimation unusable, we forced all loci homozygous, in a process we refer to as "forced homozygote approach". The results were confirmed using simulated data for different relatedness classes. We argue that this method provides a necessary alternative for relatedness estimations, not only in forensic analysis, but also in ancient DNA studies, where reduced amounts of genetic information can limit the application of traditional methods.