Publications by authors named "Roger Benson"

76 Publications

Beyond the beak: Brain size and allometry in avian craniofacial evolution.

J Anat 2021 Sep 23. Epub 2021 Sep 23.

Department of Earth Sciences, University of Oxford, Oxford, UK.

Birds exhibit an enormous variety of beak shapes. Such remarkable variation, however, has distracted research from other important aspects of their skull evolution, the nature of which has been little explored. Key aspects of avian skull variation appear to be qualitatively similar to those of mammals, encompassing variation in the degree of cranial vaulting, cranial base flexure, and the proportions and orientations of the occipital and facial regions. The evolution of these traits has been studied intensively in mammals under the Spatial Packing Hypothesis (SPH), an architectural constraint so-called because the general anatomical organization and development of such skull parts makes them evolve predictably in response to changes in relative brain size. Such SPH predictions account for the different appearances of skull configurations across species, either in having longer or shorter faces, and caudally or ventrally oriented occiputs, respectively. This pattern has been morphometrically and experimentally proven in mammals but has not been examined in birds or other tetrapods, and so its generality remains unknown. We explored the SPH in an interspecific sample of birds using three-dimensional geometric morphometrics. Our results show that the dominant trend of evolutionary variation in the skull of crown-group birds can be predicted by the SPH, involving concomitant changes in the face, the cranial vault and the basicranium, and with striking similarities to craniofacial variation among mammals. Although craniofacial variation is significantly affected by allometry, these allometric effects are independent of the influence of the SPH on skull morphology, as are any effects of volumetric encephalization. Our results, therefore, validate the hypothesis that a general architectural constraint underlies skull homoplasy evolution of cranial morphology among avian clades, and possibly between birds and mammals, but they downplay encephalization and allometry as the only factors involved.
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http://dx.doi.org/10.1111/joa.13555DOI Listing
September 2021

A reassessment of the enigmatic diapsid and the early history of Lepidosauromorpha.

Proc Biol Sci 2021 Aug 25;288(1957):20211084. Epub 2021 Aug 25.

Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OXI 3AN, UK.

Lepidosaurs include lizards, snakes, amphisbaenians and the tuatara, comprising a highly speciose evolutionary radiation with widely varying anatomical traits. Their stem-lineage originated by the late middle Permian 259 million years ago, but its early fossil record is poorly documented, obscuring the origins of key anatomical and functional traits of the group. , from the Early Triassic of South Africa, is an enigmatic fossil species with the potential to provide information on this. However, its anatomy and phylogenetic affinities remain highly uncertain, and have been debated since its discovery more than 100 years ago. We present microtomographic three-dimensional imaging of the cranial anatomy of that clarifies these uncertainties, providing strong evidence for lepidosauromorph affinities based on the structure of the temporal region and the implantation of marginal dentition. Phylogenetic analysis including these new data recovers as the earliest known stem-lepidosaur, within a long-lived group of early diverging lepidosauromorphs that persisted to at least the Middle Jurassic. Our results provide insights into cranial evolution on the lepidosaur stem-lineage, confirming that characteristics of pleurodont dental implantation evolved early on the lepidosaur stem-lineage. By contrast, key functional traits related to hearing (quadrate conch) and feeding (streptostyly) evolved later in the lepidosaur crown-group.
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http://dx.doi.org/10.1098/rspb.2021.1084DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8385343PMC
August 2021

The relationship between sternum variation and mode of locomotion in birds.

BMC Biol 2021 Aug 19;19(1):165. Epub 2021 Aug 19.

Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON, M5S 3B2, Canada.

Background: The origin of powered avian flight was a locomotor innovation that expanded the ecological potential of maniraptoran dinosaurs, leading to remarkable variation in modern birds (Neornithes). The avian sternum is the anchor for the major flight muscles and, despite varying widely in morphology, has not been extensively studied from evolutionary or functional perspectives. We quantify sternal variation across a broad phylogenetic scope of birds using 3D geometric morphometrics methods. Using this comprehensive dataset, we apply phylogenetically informed regression approaches to test hypotheses of sternum size allometry and the correlation of sternal shape with both size and locomotory capabilities, including flightlessness and the highly varying flight and swimming styles of Neornithes.

Results: We find evidence for isometry of sternal size relative to body mass and document significant allometry of sternal shape alongside important correlations with locomotory capability, reflecting the effects of both body shape and musculoskeletal variation. Among these, we show that a large sternum with a deep or cranially projected sternal keel is necessary for powered flight in modern birds, that deeper sternal keels are correlated with slower but stronger flight, robust caudal sternal borders are associated with faster flapping styles, and that narrower sterna are associated with running abilities. Correlations between shape and locomotion are significant but show weak explanatory power, indicating that although sternal shape is broadly associated with locomotory ecology, other unexplored factors are also important.

Conclusions: These results display the ecological importance of the avian sternum for flight and locomotion by providing a novel understanding of sternum form and function in Neornithes. Our study lays the groundwork for estimating the locomotory abilities of paravian dinosaurs, the ancestors to Neornithes, by highlighting the importance of this critical element for avian flight, and will be useful for future work on the origin of flight along the dinosaur-bird lineage.
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http://dx.doi.org/10.1186/s12915-021-01105-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8377870PMC
August 2021

Multiple paths to morphological diversification during the origin of amniotes.

Nat Ecol Evol 2021 Sep 26;5(9):1243-1249. Epub 2021 Jul 26.

Department of Earth Sciences, University of Oxford, Oxford, UK.

Early terrestrial vertebrates (amniotes) provide a classic example of diversification following adaptive zone invasion. The initial terrestrialization of vertebrates was closely followed by dietary diversification, as evidenced by a proliferation of craniomandibular and dental adaptations. However, morphological evolution of early amniotes has received limited study, in analyses with restricted taxonomic scope, leaving substantial questions about the dynamics of this important terrestrial radiation. We use novel analyses of discrete characters to quantify variation in evolutionary rates and constraints during diversification of the amniote feeding apparatus. We find evidence for an early burst, comprising high rates of anatomical change that decelerated through time, giving way to a background of saturated morphological evolution. Subsequent expansions of phenotypic diversity were not associated with increased evolutionary rates. Instead, variation in the mode of evolution became important, with groups representing independent origins of herbivory evolving distinctive, group-specific morphologies and thereby exploring novel character-state spaces. Our findings indicate the importance of plant-animal interactions in structuring the earliest radiation of amniotes and demonstrate the importance of variation in modes of phenotypic divergence during a major evolutionary radiation.
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http://dx.doi.org/10.1038/s41559-021-01516-xDOI Listing
September 2021

Fossilized cell structures identify an ancient origin for the teleost whole-genome duplication.

Proc Natl Acad Sci U S A 2021 Jul;118(30)

Department of Earth Sciences, University of Oxford, OX1 3AN Oxford, United Kingdom;

Teleost fishes comprise one-half of all vertebrate species and possess a duplicated genome. This whole-genome duplication (WGD) occurred on the teleost stem lineage in an ancient common ancestor of all living teleosts and is hypothesized as a trigger of their exceptional evolutionary radiation. Genomic and phylogenetic data indicate that WGD occurred in the Mesozoic after the divergence of teleosts from their closest living relatives but before the origin of the extant teleost groups. However, these approaches cannot pinpoint WGD among the many extinct groups that populate this 50- to 100-million-y lineage, preventing tests of the evolutionary effects of WGD. We infer patterns of genome size evolution in fossil stem-group teleosts using high-resolution synchrotron X-ray tomography to measure the bone cell volumes, which correlate with genome size in living species. Our findings indicate that WGD occurred very early on the teleost stem lineage and that all extinct stem-group teleosts known so far possessed duplicated genomes. WGD therefore predates both the origin of proposed key innovations of the teleost skeleton and the onset of substantial morphological diversification in the clade. Moreover, the early occurrence of WGD allowed considerable time for postduplication reorganization prior to the origin of the teleost crown group. This suggests at most an indirect link between WGD and evolutionary success, with broad implications for the relationship between genomic architecture and large-scale evolutionary patterns in the vertebrate Tree of Life.
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http://dx.doi.org/10.1073/pnas.2101780118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8325350PMC
July 2021

Patterns of skeletal integration in birds reveal that adaptation of element shapes enables coordinated evolution between anatomical modules.

Nat Ecol Evol 2021 Sep 19;5(9):1250-1258. Epub 2021 Jul 19.

Department of Earth Sciences, University of Oxford, Oxford, UK.

Birds show tremendous ecological disparity in spite of strong biomechanical constraints imposed by flight. Modular skeletal evolution is generally accepted to have facilitated this, with distinct body regions showing semi-independent evolutionary trajectories. However, this hypothesis has received little scrutiny. We analyse evolutionary modularity and ecomorphology using three-dimensional data from across the entire skeleton in a phylogenetically broad sample of extant birds. We find strongly modular evolution of skeletal element sizes within body regions (head, trunk, forelimb and hindlimb). However, element shapes show substantially less modularity, have stronger relationships to ecology, and provide evidence that ecological adaptation involves coordinated evolution of elements across different body regions. This complicates the straightforward paradigm in which modular evolution facilitated the ecological diversification of birds. Our findings suggest the potential for undetected patterns of morphological evolution in even well-studied groups, and advance the understanding of the interface between evolutionary integration and ecomorphology.
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http://dx.doi.org/10.1038/s41559-021-01509-wDOI Listing
September 2021

Serial disparity in the carnivoran backbone unveils a complex adaptive role in metameric evolution.

Commun Biol 2021 07 15;4(1):863. Epub 2021 Jul 15.

Department of Earth Sciences, University of Oxford, Oxford, UK.

Organisms comprise multiple interacting parts, but few quantitative studies have analysed multi-element systems, limiting understanding of phenotypic evolution. We investigate how disparity of vertebral morphology varies along the axial column of mammalian carnivores - a chain of 27 subunits - and the extent to which morphological variation have been structured by evolutionary constraints and locomotory adaptation. We find that lumbars and posterior thoracics exhibit high individual disparity but low serial differentiation. They are pervasively recruited into locomotory functions and exhibit relaxed evolutionary constraint. More anterior vertebrae also show signals of locomotory adaptation, but nevertheless have low individual disparity and constrained patterns of evolution, characterised by low-dimensional shape changes. Our findings demonstrate the importance of the thoracolumbar region as an innovation enabling evolutionary versatility of mammalian locomotion. Moreover, they underscore the complexity of phenotypic macroevolution of multi-element systems and that the strength of ecomorphological signal does not have a predictable influence on macroevolutionary outcomes.
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http://dx.doi.org/10.1038/s42003-021-02346-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8282787PMC
July 2021

Ecological and biogeographic drivers of biodiversity cannot be resolved using clade age-richness data.

Nat Commun 2021 05 19;12(1):2945. Epub 2021 May 19.

Department of Earth Sciences, University of Oxford, Oxford, OX1 3AN, UK.

Estimates of evolutionary diversification rates - speciation and extinction - have been used extensively to explain global biodiversity patterns. Many studies have analyzed diversification rates derived from just two pieces of information: a clade's age and its extant species richness. This "age-richness rate" (ARR) estimator provides a convenient shortcut for comparative studies, but makes strong assumptions about the dynamics of species richness through time. Here we demonstrate that use of the ARR estimator in comparative studies is problematic on both theoretical and empirical grounds. We prove mathematically that ARR estimates are non-identifiable: there is no information in the data for a single clade that can distinguish a process with positive net diversification from one where net diversification is zero. Using paleontological time series, we demonstrate that the ARR estimator has no predictive ability for real datasets. These pathologies arise because the ARR inference procedure yields "point estimates" that have been computed under a saturated statistical model with zero degrees of freedom. Although ARR estimates remain useful in some contexts, they should be avoided for comparative studies of diversification and species richness.
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http://dx.doi.org/10.1038/s41467-021-23307-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8134473PMC
May 2021

Mammaliaform extinctions as a driver of the morphological radiation of Cenozoic mammals.

Curr Biol 2021 Jul 17;31(13):2955-2963.e4. Epub 2021 May 17.

Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK.

Adaptive radiations are hypothesized as a generating mechanism for much of the morphological diversity of extant species. The Cenozoic radiation of placental mammals, the foundational example of this concept, gave rise to much of the morphological disparity of extant mammals, and is generally attributed to relaxed evolutionary constraints following the extinction of non-avian dinosaurs. However, study of this and other radiations has focused on variation in evolutionary rates, leaving the extent to which relaxation of constraints enabled the origin of novel phenotypes less well characterized. We evaluate constraints on morphological evolution among mammaliaforms (mammals and their closest relatives) using a new method that quantifies the capacity of evolutionary change to generate phenotypic novelty. We find that Mesozoic crown-group therians, which include the ancestors of placental mammals, were significantly more constrained than other mammaliaforms. Relaxation of these constraints occurred in the mid-Paleocene, post-dating the extinction of non-avian dinosaurs at the K/Pg boundary, instead coinciding with important environmental shifts and with declining ecomorphological diversity in non-theriimorph mammaliaforms. This relaxation occurred even in small-bodied Cenozoic mammals weighing <100 g, which are unlikely to have competed with dinosaurs. Instead, our findings support a more complex model whereby Mesozoic crown therian evolution was in part constrained by co-occurrence with disparate mammaliaforms, as well as by the presence of dinosaurs, within-lineage incumbency effects, and environmental factors. Our results demonstrate that variation in evolutionary constraints can occur independently of variation in evolutionary rate, and that both make important contributions to the understanding of adaptive radiations.
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http://dx.doi.org/10.1016/j.cub.2021.04.044DOI Listing
July 2021

Evolution of vision and hearing modalities in theropod dinosaurs.

Science 2021 05;372(6542):610-613

Evolutionary Studies Institute, University of the Witwatersrand, 1 Jan Smuts Avenue, Johannesburg 2000, South Africa.

Owls and nightbirds are nocturnal hunters of active prey that combine visual and hearing adaptations to overcome limits on sensory performance in low light. Such sensory innovations are unknown in nonavialan theropod dinosaurs and are poorly characterized on the line that leads to birds. We investigate morphofunctional proxies of vision and hearing in living and extinct theropods and demonstrate deep evolutionary divergences of sensory modalities. Nocturnal predation evolved early in the nonavialan lineage Alvarezsauroidea, signaled by extreme low-light vision and increases in hearing sensitivity. The Late Cretaceous alvarezsauroid had even further specialized hearing acuity, rivaling that of today's barn owl. This combination of sensory adaptations evolved independently in dinosaurs long before the modern bird radiation and provides a notable example of convergence between dinosaurs and mammals.
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http://dx.doi.org/10.1126/science.abe7941DOI Listing
May 2021

Deep evolutionary diversification of semicircular canals in archosaurs.

Curr Biol 2021 Jun 29;31(12):2520-2529.e6. Epub 2021 Apr 29.

Department of Geosciences, Virginia Tech, 926 West Campus Drive, Blacksburg, VA 24061, USA. Electronic address:

Living archosaurs (birds and crocodylians) have disparate locomotor strategies that evolved since their divergence ∼250 mya. Little is known about the early evolution of the sensory structures that are coupled with these changes, mostly due to limited sampling of early fossils on key stem lineages. In particular, the morphology of the semicircular canals (SCCs) of the endosseous labyrinth has a long-hypothesized relationship with locomotion. Here, we analyze SCC shapes and sizes of living and extinct archosaurs encompassing diverse locomotor habits, including bipedal, semi-aquatic, and flying taxa. We test form-function hypotheses of the SCCs and chronicle their evolution during deep archosaurian divergences. We find that SCC shape is statistically associated with both flight and bipedalism. However, this shape variation is small and is more likely explained by changes in braincase geometry than by locomotor changes. We demonstrate high disparity of both shape and size among stem-archosaurs and a deep divergence of SCC morphologies at the bird-crocodylian split. Stem-crocodylians exhibit diverse morphologies, including aspects also present in birds and distinct from other reptiles. Therefore, extant crocodylian SCC morphologies do not reflect retention of a "primitive" reptilian condition. Key aspects of bird SCC morphology that hitherto were interpreted as flight related, including large SCC size and enhanced sensitivity, appeared early on the bird stem-lineage in non-flying dinosaur precursors. Taken together, our results indicate a deep divergence of SCC traits at the bird-crocodylian split and that living archosaurs evolved from an early radiation with high sensory diversity. VIDEO ABSTRACT.
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http://dx.doi.org/10.1016/j.cub.2021.03.086DOI Listing
June 2021

Evidence from South Africa for a protracted end-Permian extinction on land.

Proc Natl Acad Sci U S A 2021 Apr;118(17)

Negaunee Integrative Research Center, Field Museum of Natural History, Chicago, IL 60605.

Earth's largest biotic crisis occurred during the Permo-Triassic Transition (PTT). On land, this event witnessed a turnover from synapsid- to archosauromorph-dominated assemblages and a restructuring of terrestrial ecosystems. However, understanding extinction patterns has been limited by a lack of high-precision fossil occurrence data to resolve events on submillion-year timescales. We analyzed a unique database of 588 fossil tetrapod specimens from South Africa's Karoo Basin, spanning ∼4 My, and 13 stratigraphic bin intervals averaging 300,000 y each. Using sample-standardized methods, we characterized faunal assemblage dynamics during the PTT. High regional extinction rates occurred through a protracted interval of ∼1 Ma, initially co-occurring with low origination rates. This resulted in declining diversity up to the acme of extinction near the - Assemblage Zone boundary. Regional origination rates increased abruptly above this boundary, co-occurring with high extinction rates to drive rapid turnover and an assemblage of short-lived species symptomatic of ecosystem instability. The "disaster taxon" shows a long-term trend of increasing abundance initiated in the latest Permian. comprised 54% of all specimens by the onset of mass extinction and 70% in the extinction aftermath. This early abundance suggests its expansion was facilitated by environmental changes rather than by ecological opportunity following the extinctions of other species as commonly assumed for disaster taxa. Our findings conservatively place the Karoo extinction interval closer in time, but not coeval with, the more rapid marine event and reveal key differences between the PTT extinctions on land and in the oceans.
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http://dx.doi.org/10.1073/pnas.2017045118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8092562PMC
April 2021

Craniofacial development illuminates the evolution of nightbirds (Strisores).

Proc Biol Sci 2021 04 14;288(1948):20210181. Epub 2021 Apr 14.

School of Earth Sciences, University of Bristol, Life Sciences Building, Bristol, UK.

Evolutionary variation in ontogeny played a central role in the origin of the avian skull. However, its influence in subsequent bird evolution is largely unexplored. We assess the links between ontogenetic and evolutionary variation of skull morphology in Strisores (nightbirds). Nightbirds span an exceptional range of ecologies, sizes, life-history traits and craniofacial morphologies constituting an ideal test for evo-devo hypotheses of avian craniofacial evolution. These morphologies include superficially 'juvenile-like' broad, flat skulls with short rostra and large orbits in swifts, nightjars and allied lineages, and the elongate, narrow rostra and globular skulls of hummingbirds. Here, we show that nightbird skulls undergo large ontogenetic shape changes that differ strongly from widespread avian patterns. While the superficially juvenile-like skull morphology of many adult nightbirds results from convergent evolution, rather than paedomorphosis, the divergent cranial morphology of hummingbirds originates from an evolutionary reversal to a more typical avian ontogenetic trajectory combined with accelerated ontogenetic shape change. Our findings underscore the evolutionary lability of cranial growth and development in birds, and the underappreciated role of this aspect of phenotypic variability in the macroevolutionary diversification of the amniote skull.
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http://dx.doi.org/10.1098/rspb.2021.0181DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8059503PMC
April 2021

Evolutionary versatility of the avian neck.

Proc Biol Sci 2021 03 3;288(1946):20203150. Epub 2021 Mar 3.

Department of Musculoskeletal & Ageing Science, University of Liverpool, William Henry Duncan Building, 6 West Derby Street, Liverpool, L7 8TX, UK.

Bird necks display unparalleled levels of morphological diversity compared to other vertebrates, yet it is unclear what factors have structured this variation. Using three-dimensional geometric morphometrics and multivariate statistics, we show that the avian cervical column is a hierarchical morpho-functional appendage, with varying magnitudes of ecologically driven osteological variation at different scales of organization. Contrary to expectations given the widely varying ecological functions of necks in different species, we find that regional modularity of the avian neck is highly conserved, with an overall structural blueprint that is significantly altered only by the most mechanically demanding ecological functions. Nevertheless, the morphologies of vertebrae within subregions of the neck show more prominent signals of adaptation to ecological pressures. We also find that both neck length allometry and the nature of neck elongation in birds are different from other vertebrates. In contrast with mammals, neck length scales isometrically with head mass and, contrary to previous work, we show that neck elongation in birds is achieved predominantly by increasing vertebral lengths rather than counts. Birds therefore possess a cervical spine that may be unique in its versatility among extant vertebrates, one that, since the origin of flight, has adapted to function as a surrogate forelimb in varied ecological niches.
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http://dx.doi.org/10.1098/rspb.2020.3150DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7934994PMC
March 2021

Enigmatic dinosaur precursors bridge the gap to the origin of Pterosauria.

Nature 2020 12 9;588(7838):445-449. Epub 2020 Dec 9.

Departamento de Biologia, Universidade de São Paulo, Ribeirão Preto, Brazil.

Pterosaurs were the first vertebrates to evolve powered flight and comprised one of the main evolutionary radiations in terrestrial ecosystems of the Mesozoic era (approximately 252-66 million years ago), but their origin has remained an unresolved enigma in palaeontology since the nineteenth century. These flying reptiles have been hypothesized to be the close relatives of a wide variety of reptilian clades, including dinosaur relatives, and there is still a major morphological gap between those forms and the oldest, unambiguous pterosaurs from the Upper Triassic series. Here, using recent discoveries of well-preserved cranial remains, microcomputed tomography scans of fragile skull bones (jaws, skull roofs and braincases) and reliably associated postcrania, we demonstrate that lagerpetids-a group of cursorial, non-volant dinosaur precursors-are the sister group of pterosaurs, sharing numerous synapomorphies across the entire skeleton. This finding substantially shortens the temporal and morphological gap between the oldest pterosaurs and their closest relatives and simultaneously strengthens the evidence that pterosaurs belong to the avian line of archosaurs. Neuroanatomical features related to the enhanced sensory abilities of pterosaurs are already present in lagerpetids, which indicates that these features evolved before flight. Our evidence illuminates the first steps of the assembly of the pterosaur body plan, whose conquest of aerial space represents a remarkable morphofunctional innovation in vertebrate evolution.
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http://dx.doi.org/10.1038/s41586-020-3011-4DOI Listing
December 2020

Morphological divergence in giant fossil dormice.

Proc Biol Sci 2020 11 4;287(1938):20202085. Epub 2020 Nov 4.

Hull York Medical School, University of York, York, UK.

Insular gigantism-evolutionary increases in body size from small-bodied mainland ancestors-is a conceptually significant, but poorly studied, evolutionary phenomenon. Gigantism is widespread on Mediterranean islands, particularly among fossil and extant dormice. These include an extant giant population of on Formentera, the giant Balearic genus † and the exceptionally large † of Pleistocene Sicily. We quantified patterns of cranial and mandibular shape and their relationships to head size (allometry) among mainland and insular dormouse populations, asking to what extent the morphology of island giants is explained by allometry. We find that gigantism in dormice is not simply an extrapolation of the allometric trajectory of their mainland relatives. Instead, a large portion of their distinctive cranial and mandibular morphology resulted from the population- or species-specific evolutionary shape changes. Our findings suggest that body size increases in insular giant dormice were accompanied by the evolutionary divergence of feeding adaptations. This complements other evidence of ecological divergence in these taxa, which span predominantly faunivorous to herbivorous diets. Our findings suggest that insular gigantism involves context-dependent phenotypic modifications, underscoring the highly distinctive nature of island faunas.
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http://dx.doi.org/10.1098/rspb.2020.2085DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7735280PMC
November 2020

The macroevolutionary landscape of short-necked plesiosaurians.

Sci Rep 2020 10 2;10(1):16434. Epub 2020 Oct 2.

Department of Earth Sciences, University of Oxford, South Parks road, Oxford, OX1 3AN, UK.

Throughout their evolution, tetrapods have repeatedly colonised a series of ecological niches in marine ecosystems, producing textbook examples of convergent evolution. However, this evolutionary phenomenon has typically been assessed qualitatively and in broad-brush frameworks that imply simplistic macroevolutionary landscapes. We establish a protocol to visualize the density of trait space occupancy and thoroughly test for the existence of macroevolutionary landscapes. We apply this protocol to a new phenotypic dataset describing the morphology of short-necked plesiosaurians, a major component of the Mesozoic marine food webs (ca. 201 to 66 Mya). Plesiosaurians evolved this body plan multiple times during their 135-million-year history, making them an ideal test case for the existence of macroevolutionary landscapes. We find ample evidence for a bimodal craniodental macroevolutionary landscape separating latirostrines from longirostrine taxa, providing the first phylogenetically-explicit quantitative assessment of trophic diversity in extinct marine reptiles. This bimodal pattern was established as early as the Middle Jurassic and was maintained in evolutionary patterns of short-necked plesiosaurians until a Late Cretaceous (Turonian) collapse to a unimodal landscape comprising longirostrine forms with novel morphologies. This study highlights the potential of severe environmental perturbations to profoundly alter the macroevolutionary dynamics of animals occupying the top of food chains.
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http://dx.doi.org/10.1038/s41598-020-73413-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7532190PMC
October 2020

The origin of tetrapod herbivory: effects on local plant diversity.

Proc Biol Sci 2020 06 10;287(1928):20200124. Epub 2020 Jun 10.

Department of Earth Sciences, University of Oxford, South Parks Road, Oxford, UK.

The origin of herbivory in the Carboniferous was a landmark event in the evolution of terrestrial ecosystems, increasing ecological diversity in animals but also giving them greater influence on the evolution of land plants. We evaluate the effect of early vertebrate herbivory on plant evolution by comparing local species richness of plant palaeofloras with that of vertebrate herbivores and herbivore body size. Vertebrate herbivores became diverse and achieved a much greater range of body sizes across the Carboniferous-Permian transition interval. This coincides with an abrupt reduction in local plant richness that persists throughout the Permian. Time-series regression analysis supports a negative relationship of plant richness with herbivore richness but a positive relationship of plant richness with minimum herbivore body size. This is consistent with studies of present-day ecosystems in which increased diversity of smaller, more selective herbivores places greater predation pressures on plants, while a prevalence of larger bodied, less selective herbivores reduces the dominance of a few highly tolerant plant species, thereby promoting greater local richness. The diversification of herbivores across the Carboniferous-Permian boundary, along with the appearance of smaller, more selective herbivores like bolosaurid parareptiles, constrained plant diversity throughout the Permian. These findings demonstrate that the establishment of widespread vertebrate herbivory has structured plant communities since the late Palaeozoic, as expected from examination of modern ecosystems, and illustrates the potential for fossil datasets in testing palaeoecological hypotheses.
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http://dx.doi.org/10.1098/rspb.2020.0124DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7341937PMC
June 2020

The apparent exponential radiation of Phanerozoic land vertebrates is an artefact of spatial sampling biases.

Proc Biol Sci 2020 04 8;287(1924):20200372. Epub 2020 Apr 8.

School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK.

There is no consensus about how terrestrial biodiversity was assembled through deep time, and in particular whether it has risen exponentially over the Phanerozoic. Using a database of 60 859 fossil occurrences, we show that the spatial extent of the worldwide terrestrial tetrapod fossil record itself expands exponentially through the Phanerozoic. Changes in spatial sampling explain up to 67% of the change in known fossil species counts, and these changes are decoupled from variation in habitable land area that existed through time. Spatial sampling therefore represents a real and profound sampling bias that cannot be explained as redundancy. To address this bias, we estimate terrestrial tetrapod diversity for palaeogeographical regions of approximately equal size. We find that regional-scale diversity was constrained over timespans of tens to hundreds of millions of years, and similar patterns are recovered for major subgroups, such as dinosaurs, mammals and squamates. Although the Cretaceous/Palaeogene mass extinction catalysed an abrupt two- to three-fold increase in regional diversity 66 million years ago, no further increases occurred, and recent levels of regional diversity do not exceed those of the Palaeogene. These results parallel those recovered in analyses of local community-level richness. Taken together, our findings strongly contradict past studies that suggested unbounded diversity increases at local and regional scales over the last 100 million years.
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http://dx.doi.org/10.1098/rspb.2020.0372DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7209054PMC
April 2020

Three-dimensional characterization of osteocyte volumes at multiple scales, and its relationship with bone biology and genome evolution in ray-finned fishes.

J Evol Biol 2020 06 20;33(6):808-830. Epub 2020 Mar 20.

European Synchrotron Radiation Facility, Grenoble, France.

Osteocytes, cells embedded within the bone mineral matrix, inform on key aspects of vertebrate biology. In particular, a relationship between volumes of the osteocytes and bone growth and/or genome size has been proposed for several tetrapod lineages. However, the variation in osteocyte volume across different scales is poorly characterized and mostly relies on incomplete, two-dimensional information. In this study, we characterize the variation of osteocyte volumes in ray-finned fishes (Actinopterygii), a clade including more than half of modern vertebrate species in which osteocyte biology is poorly known. We use X-ray synchrotron micro-computed tomography (SRµCT) to achieve a three-dimensional visualization of osteocyte lacunae and direct measurement of their size (volumes). Our specimen sample is designed to characterize variation in osteocyte lacuna morphology at three scales: within a bone, among the bones of one individual and among species. At the intra-bone scale, we find that osteocyte lacunae vary noticeably in size between zones of organized and woven bone (being up to six times larger in woven bone), and across cyclical bone deposition. This is probably explained by differences in bone deposition rate, with larger osteocyte lacunae contained in bone that deposits faster. Osteocyte lacuna volumes vary 3.5-fold among the bones of an individual, and this cannot readily be explained by variation in bone growth rate or other currently observable factors. Finally, we find that genome size provides the best explanation of variation in osteocyte lacuna volume among species: actinopterygian taxa with larger genomes (polyploid taxa in particular) have larger osteocyte lacunae (with a ninefold variation in median osteocyte volume being measured). Our findings corroborate previous two-dimensional studies in tetrapods that also observed similar patterns of intra-individual variation and found a correlation with genome size. This opens new perspectives for further studies on bone evolution, physiology and palaeogenomics in actinopterygians, and vertebrates as a whole.
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http://dx.doi.org/10.1111/jeb.13612DOI Listing
June 2020

Developmental Constraints Do Not Influence Long-Term Phenotypic Evolution of Marsupial Forelimbs as Revealed by Interspecific Disparity and Integration Patterns.

Am Nat 2020 03 17;195(3):547-560. Epub 2020 Jan 17.

Marsupials show a smaller range of forelimb ecomorphologies than placental mammals, and it is hypothesized that this results from macroevolutionary constraints imposed by the specialized reproductive biology of marsupials. Specifically, the accelerated development of the marsupial forelimb allows neonates to crawl to the mother's pouch but may constrain adult morphology. This hypothesis makes three main predictions: (i) that marsupial forelimbs should show less interspecific disparity than their hindlimbs, (ii) that morphological integration within the marsupial forelimb is stronger than integration between limbs, and (iii) that these patterns should be strongest in diprotodontians, which undergo the most rigorous crawls as neonates. We use a three-dimensional geometric morphometric data set of limb bones for 51 marsupial species to test these predictions. We find that (i) marsupial forelimbs and hindlimbs show similar disparities, (ii) no clear differences in integration exist either within or between limbs, and (iii) the same patterns occur in diprotodontians as in other marsupials, even correcting for lineage age. Therefore, there is currently little evidence that the developmental biology of marsupials has constrained their macroevolutionary patterns. It is possible that functional selection can overcome the effects of developmental constraint on macroevolutionary timescales. Our findings suggest that the role of developmental constraints in explaining the limited phenotypic variability of marsupials (compared with that of placentals) should be reconsidered.
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http://dx.doi.org/10.1086/707194DOI Listing
March 2020

A new possible megalosauroid theropod from the Middle Jurassic Xintiangou Formation of Chongqing, People's Republic of China and its implication for early tetanuran evolution.

Sci Rep 2020 01 10;10(1):139. Epub 2020 Jan 10.

Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, 100044, China.

Tetanurae is a special group of theropod dinosaurs that originated by the late Early Jurassic. It includes several early-diverging groups of generally large-bodied predators (megalosauroids, allosauroids, tyrannosauroid coelurosaurs) as well as morphologically disparate small-bodied coelurosaurs, including birds. Aspects of the evolutionary history of tetanurans remain contested, including the topology of their deep phylogenetic divergences (among Megalosauroidea, Allosauroidea and Coelurosauria). We report a new theropod, Yunyangosaurus puanensis gen. et sp. nov., based on a fragmentary specimen recovered from the Middle Jurassic Xintiangou Formation of Chongqing, southwestern China. It shares several features uniquely with some megalosauroids (the clade of megalosaurids + spinosaurids + piatnitzkysaurids), such as prominent rims around the anterior articular surfaces of cervical centra and bifurcated anterior dorsal neural spines (present in piatnitzkysaurids). Nevertheless, it also shows several features that are rare or absent among megalosauroids and more crownward tetanurans, including prominent spinopostyzgopophyseal laminae (also present in non-tetanurans and metriacanthosaurid allosauroids), flat anterior articular surfaces of the cervical centra (also present in piatnitzkysaurids and some earlier-diverging tetanurans), and the presence of a posterior pneumatic foramen or fossa (absent in most tetanurans, but sporadically present in some cervical vertebrae of piatnitzkysaurids). Yunyangosaurus therefore presents a combination of derived and apparently primitive character states that are not seen in other theropods. This suggests that patterns of morphological evolution associated with deep tetanuran divergences were more complex than currently recognized, with implications for understanding the character evolution in theropods.
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http://dx.doi.org/10.1038/s41598-019-56959-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6954265PMC
January 2020

Evolution: The Two Faces of Plant-Eating Dinosaurs.

Curr Biol 2020 01;30(1):R14-R16

Department of Earth Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK.

Plant-eating dinosaurs evolved varied feeding strategies. A new study demonstrates convergent evolution of their skulls and teeth towards two distinct functional optima, one resembling advanced mammalian herbivory and the other echoing herbivory in birds and other reptiles.
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http://dx.doi.org/10.1016/j.cub.2019.11.035DOI Listing
January 2020

The phylogeny of early amniotes and the affinities of Parareptilia and Varanopidae.

Nat Ecol Evol 2020 01 23;4(1):57-65. Epub 2019 Dec 23.

Department of Earth Sciences, University of Oxford, Oxford, UK.

Amniotes include mammals, reptiles and birds, representing 75% of extant vertebrate species on land. They originated around 318 million years ago in the early Late Carboniferous and their early fossil record is central to understanding the expansion of vertebrates in terrestrial ecosystems. We present a phylogenetic hypothesis that challenges the widely accepted consensus about early amniote evolution, based on parsimony analysis and Bayesian inference of a new morphological dataset. We find a reduced membership of the mammalian stem lineage, which excludes varanopids. This implies that evolutionary turnover of the mammalian stem lineage during the Early-Middle Permian transition (273 million years ago) was more abrupt than has previously been recognized. We also find that Parareptilia are nested within Diapsida. This suggests that temporal fenestration, a key structural innovation with important functional implications, evolved fewer times than generally thought, but showed highly variable morphology among early reptiles after its initial origin. Our phylogeny also addresses controversies over the affinities of mesosaurids, the earliest known aquatic amniotes, which we recover as early diverging parareptiles.
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http://dx.doi.org/10.1038/s41559-019-1047-3DOI Listing
January 2020

The multi-peak adaptive landscape of crocodylomorph body size evolution.

BMC Evol Biol 2019 08 7;19(1):167. Epub 2019 Aug 7.

School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, UK.

Background: Little is known about the long-term patterns of body size evolution in Crocodylomorpha, the > 200-million-year-old group that includes living crocodylians and their extinct relatives. Extant crocodylians are mostly large-bodied (3-7 m) predators. However, extinct crocodylomorphs exhibit a wider range of phenotypes, and many of the earliest taxa were much smaller (< 1.2 m). This suggests a pattern of size increase through time that could be caused by multi-lineage evolutionary trends of size increase or by selective extinction of small-bodied species. Here, we characterise patterns of crocodylomorph body size evolution using a model fitting-approach (with cranial measurements serving as proxies). We also estimate body size disparity through time and quantitatively test hypotheses of biotic and abiotic factors as potential drivers of crocodylomorph body size evolution.

Results: Crocodylomorphs reached an early peak in body size disparity during the Late Jurassic, and underwent an essentially continual decline since then. A multi-peak Ornstein-Uhlenbeck model outperforms all other evolutionary models fitted to our data (including both uniform and non-uniform), indicating that the macroevolutionary dynamics of crocodylomorph body size are better described within the concept of an adaptive landscape, with most body size variation emerging after shifts to new macroevolutionary regimes (analogous to adaptive zones). We did not find support for a consistent evolutionary trend towards larger sizes among lineages (i.e., Cope's rule), or strong correlations of body size with climate. Instead, the intermediate to large body sizes of some crocodylomorphs are better explained by group-specific adaptations. In particular, the evolution of a more aquatic lifestyle (especially marine) correlates with increases in average body size, though not without exceptions.

Conclusions: Shifts between macroevolutionary regimes provide a better explanation of crocodylomorph body size evolution on large phylogenetic and temporal scales, suggesting a central role for lineage-specific adaptations rather than climatic forcing. Shifts leading to larger body sizes occurred in most aquatic and semi-aquatic groups. This, combined with extinctions of groups occupying smaller body size regimes (particularly during the Late Cretaceous and Cenozoic), gave rise to the upward-shifted body size distribution of extant crocodylomorphs compared to their smaller-bodied terrestrial ancestors.
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http://dx.doi.org/10.1186/s12862-019-1466-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6686447PMC
August 2019

Comparative analysis of the shape and size of the middle ear cavity of turtles reveals no correlation with habitat ecology.

J Anat 2019 12 2;235(6):1078-1097. Epub 2019 Aug 2.

Department of Earth Sciences, University of Oxford, Oxford, UK.

The middle ear of turtles differs from other reptiles in being separated into two distinct compartments. Several ideas have been proposed as to why the middle ear is compartmentalized in turtles, most suggesting a relationship with underwater hearing. Extant turtle species span fully marine to strictly terrestrial habitats, and ecomorphological hypotheses of turtle hearing predict that this should correlate with variation in the structure of the middle ear due to differences in the fluid properties of water and air. We investigate the shape and size of the air-filled middle ear cavity of 56 extant turtles using 3D data and phylogenetic comparative analysis to test for correlations between habitat preferences and the shape and size of the middle ear cavity. Only weak correlations are found between middle ear cavity size and ecology, with aquatic taxa having proportionally smaller cavity volumes. The middle ear cavity of turtles exhibits high shape diversity among species, but we found no relationship between this shape variation and ecology. Surprisingly, the estimated acoustic transformer ratio, a key functional parameter of impedance-matching ears in vertebrates, also shows no relation to habitat preferences (aquatic/terrestrial) in turtles. We suggest that middle ear cavity shape may be controlled by factors unrelated to hearing, such as the spatial demands of surrounding cranial structures. A review of the fossil record suggests that the modern turtle ear evolved during the Early to Middle Jurassic in stem turtles broadly adapted to freshwater and terrestrial settings. This, combined with our finding that evolutionary transitions between habitats caused only weak evolutionary changes in middle ear structure, suggests that tympanic hearing in turtles evolved as a compromise between subaerial and underwater hearing.
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http://dx.doi.org/10.1111/joa.13071DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6875938PMC
December 2019

Evolution: Much on the Menu for Ancient Crocs.

Curr Biol 2019 07;29(14):R683-R685

Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794-8434, USA.

Crocodylians are carnivores, but their extinct relatives had wider-ranging diets. A new study shows that herbivory evolved often in these animals, and that their teeth rivalled those of mammals in terms of complexity.
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http://dx.doi.org/10.1016/j.cub.2019.06.004DOI Listing
July 2019

Anatomy of (Protostegidae) and marine adaptation during the early evolution of chelonioids.

PeerJ 2019 1;7:e6811. Epub 2019 May 1.

Department of Earth Sciences, University of Oxford, Oxford, UK.

Knowledge of the early evolution of sea turtles (Chelonioidea) has been limited by conflicting phylogenetic hypotheses resulting from sparse taxon sampling and a superficial understanding of the morphology of key taxa. This limits our understanding of evolutionary adaptation to marine life in turtles, and in amniotes more broadly. One problematic group are the protostegids, Early-Late Cretaceous marine turtles that have been hypothesised to be either stem-cryptodires, stem-chelonioids, or crown-chelonioids. Different phylogenetic hypotheses for protostegids suggest different answers to key questions, including (1) the number of transitions to marine life in turtles, (2) the age of the chelonioid crown-group, and (3) patterns of skeletal evolution during marine adaptation. We present a detailed anatomical study of one of the earliest protostegids, from the early Late Cretaceous of Europe, using high-resolution μCT. We synonymise all previously named European species and document the variation seen among them. A phylogeny of turtles with increased chelonioid taxon sampling and revised postcranial characters is provided, recovering protostegids as stem-chelonioids. Our results imply a mid Early Cretaceous origin of total-group chelonioids and an early Late Cretaceous age for crown-chelonioids, which may inform molecular clock analyses in future. Specialisations of the chelonioid flipper evolved in a stepwise-fashion, with innovations clustered into pulses at the origin of total-group chelonioids, and subsequently among dermochelyids, crown-cheloniids, and gigantic protostegids from the Late Cretaceous.
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http://dx.doi.org/10.7717/peerj.6811DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6500378PMC
May 2019

Patterns of mammalian jaw ecomorphological disparity during the Mesozoic/Cenozoic transition.

Proc Biol Sci 2019 05;286(1902):20190347

1 Department of Earth Sciences, University of Oxford , Oxford OX1 3AN , UK.

The radiation of mammals after the Cretaceous/Palaeogene (K/Pg) boundary was a major event in the evolution of terrestrial ecosystems. Multiple studies point to increases in maximum body size and body size disparity, but patterns of disparity for other traits are less clear owing to a focus on different indices and subclades. We conducted an inclusive comparison of jaw functional disparity from the Early Jurassic-latest Eocene, using six mechanically relevant mandibular ratios for 256 species representing all major groups. Jaw functional disparity across all mammals was low throughout much of the Mesozoic and remained low across the K/Pg boundary. Nevertheless, the K/Pg boundary was characterized by a pronounced pattern of turnover and replacement, entailing a substantial reduction of non-therian and stem-therian disparity, alongside a marked increase in that of therians. Total mammal disparity exceeded its Mesozoic maximum for the first time during the Eocene, when therian mammals began exploring previously unoccupied regions of function space. This delay in the rise of jaw functional disparity until the Eocene probably reflects the duration of evolutionary recovery after the K/Pg mass extinction event. This contrasts with the more rapid expansion of maximum body size, which occurred in the Palaeocene.
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http://dx.doi.org/10.1098/rspb.2019.0347DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6532522PMC
May 2019
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