Search bioRxiv⌕ Search

Biology subjects

Weisbecker, V.

Publications and source records attributed to Weisbecker, V..

16 recordsLinked to original sources

Species richness and trait diversity show parallel island-biogeographic patterns across Australian islands

Island biogeography is the theoretical and empirically validated expectation that an islands biodiversity is ultimately limited by its size and isolation, with larger and less isolated (from mainland communities) islands supporting greater diversity. Island biogeography is generally applied to simple metrics of diversity such as species richness (number of different species); however, fewer studies have used traits to measure biodiversity. An organisms traits -- e.g., body mass, age at sexual maturity, trophic level -- can be used to measure biodiversity and understand how ecological communities function. We quantified species richness for birds, mammals, reptiles, and amphibians, and functional diversity for birds and mammals (for which sufficient trait data were available), and tested whether this diversity can be predicted using the theory of island biogeography. We identified 9,103 Australian islands, of which 1,661 had at least one (native and/or non-native) non-marine species present according to the Atlas of Living Australia. As expected, tetrapod species richness (S) increased with island area (A) (z = 0.299 {+/-} 0.012) following a typical power-law relationship (i.e., S = cAz, where z = 0.2-0.4), but was not predicted by distance from mainland -- consistent with the pattern observed on other recently (< 10,000 years) isolated continental islands. We found that trait richness increased at the same rate with island area as species richness for mammals, but for birds, trait richness increased more slowly than species richness. Trait turnover increased modestly with inter-island distance, whereas trait nestedness was unrelated to distance. Trait richness increased strongly with species richness in both birds and mammals, and island area and isolation explained no additional variation in functional richness after accounting for species richness. These results indicate that island geography influences functional diversity primarily through species accumulation, rather than through direct effects on occupied trait space. Overall, the trait space of smaller islands tended to be nested within that of larger, nearby islands; the main differences among similar-sized islands are due to turnover (change in species/trait combinations among assemblages), and the effects are more pronounced in mammals compared to birds. We also found evidence for an asymptotic relationship between trait and species turnover in both birds and mammals, suggesting close coupling between taxonomic and functional turnover, with some saturation of trait turnover at high species turnover. Large islands that are simultaneously more isolated might offer conservation advantages by reducing the influence of threatening processes on the mainland if distance limits access of people and invasive species.

ecology↗

Sizing up phylogenetic testing in geometric morphometrics: A case study of allometry

AbstractAccounting for phylogenetic relatedness in the analysis of shape has become a common practice, deemed necessary to factor in the non-independence between species because of common ancestry. However, when adjusting error distributions to account for relatedness, the phylogenetic-generalised-least-squares (PGLS) test can obscure an important component of variation called conservative trait correlation (CTC). This is the amount of variation in a response variable that is both attributable to a predictor variable and phylogenetically structured. If CTC represents a large amount of correlated variation, true biological associations with strong phylogenetic signal (from unrepeated evolutionary events for example) might not be supported using a PGLS. We demonstrate this effect using geometric morphometric shape analysis on 370 crania from the speciose Australian rock- wallabies (genus Petrogale). In this clade, well-recognised allometric patterns such as scaling of the braincase (Hallers rule) and snout length (craniofacial evolutionary allometry) are supported using ordinary least squares (OLS) regression, but not PGLS, indicating that important between-species shape variation is lost. We then apply two methods capable of quantifying aspects of the missing variation: variation partitioning (VARPART), which estimates the proportion of variation shared between the predictor and phylogeny, and multi- response phylogenetic mixed models (MR-PMM), which identify the strength of correlation within the phylogenetic component of trait variance. Both methods show that CTC dominates the allometric shape variation in our sample, highlighting its importance in assessing phylogenetically informed models. We suggest approaches that can consider CTC become more widely used to better understand morphology and its predictors.

evolutionary biology↗

Cracking the case: Differential adaptations to hard biting dominate cranial shape in rat-kangaroos (Potoroidae: Bettongia) with divergent diets.

Functional adaptation in the mammalian jaw is often best predicted by the hardest bites an animal makes. Therefore, even when closely related species have otherwise divergent diets, a shared biomechanically challenging resource should be reflected in similar adaptations to jaw biomechanics. We assessed this in two species of rat-kangaroos, whose otherwise divergent diets include the extremely tough-shelled seeds of Santalum spp. (sandalwood and/or quandong). We used geometric morphometrics to analyse cranial shape of 161 bettongs (Bettongia spp.), including all four extant species. We identified adaptations to higher bite forces in both species that crack open Santalum seeds. However, B. lesueur had shorter facial proportions, indicating higher mechanical advantage, while B. penicillata had a premolar morphology that likely focussed bites to a specific, reinforced position on the jaw. This represents an example of many-to-one mapping at the genus level. We also found differences in a subsample of captive northern bettongs compared to wild conspecifics, suggesting some role of phenotypic plasticity in shaping adult skulls. The large olfactory tracts of B. penicillata, that support search for underground fungi, might have constrained its cranium to retain longer proportions. Fungal abundance could potentially be an important consideration in identifying translocation sites for this species.

developmental biology↗

Sorting the mob: using geometric morphometrics and machine learning to differentiate kangaroo postcrania for zooarchaeological applications

Taxonomic identification of bone is one of the building blocks of zooarchaeological research into human foraging behaviour. However, it can prove difficult in regions, such as Australia, that have biodiverse taxa that are difficult to differentiate using bone morphology. One such case are the kangaroos and wallabies (macropods), one of the most speciose groups of marsupials whose remains are frequently recovered from Australian archaeological sites. Despite their clear importance to Indigenous economies, little research has been undertaken on how to reliably differentiate the postcranial remains of extant macropods. Here we address this gap by applying three-dimensional geometric morphometrics to describe how the astragalus and calcaneus differs between several large macropod genera. We describe taxonomically diagnostic anatomical attributes between genera and identify the size related (allometric) shape variation that could be mistaken for taxonomic differences. We then compare several machine learning models to demonstrate how these can be applied to geometric morphometric data to statistically classify unknown specimens from palaeozoological contexts with a high degree of accuracy. Our results show that non-linear methods of supervised machine learning outperform classical discriminant function analysis when used on our geometric morphometric data. Statistical classification of palaeozoological specimens has the potential to be a valuable tool, where differentiating skeletal remains of closely related taxa continues to prove challenging.

paleontology↗

Ozboneviz: An Australian Precedent in FAIR 3D Imagery and Extended Biodiversity Collections

Billions of specimens are in biodiversity collections worldwide, and this infrastructure is crucial for research on Earths natural history. Three-dimensional (3D) imagery of specimens is an increasingly important part of the Digital Extended Specimen network of metadata. Open access, high fidelity 3D imagery of biodiversity specimens improves researcher efficiency, equity and increases public engagement with collections. We introduce Ozboneviz, an open access collection of FAIR (Findable, Accessible, Interoperable, Reusable) 3D imagery aiming to enhance research capacity in Australasian vertebrate skeletal morphology. Ozboneviz is an Australian test case demonstrating the feasibility of creating multi-institutional, FAIR 3D biodiversity imagery collections. We outline project design, challenges, and use by the international research community. We then discuss the urgent need for investment in infrastructure and curatorial support to progress the digitisation of Australian biodiversity collections in a way that maximises stakeholder benefit and facilitates 3D data discoverability and retrieval.

zoology↗

Avian telencephalon and cerebellum volumes can be accurately estimated from digital brain endocasts

For studies of the evolution of vertebrate brain anatomy and potentially associated behaviours, reconstructions of digital brain endocasts from computed tomography scans have revolutionised our capacity to collect neuroanatomical data. However, measurements from digital endocasts must be validated as reflecting actual brain anatomy, which is difficult because the collection of soft tissue information through histology is laborious and time consuming. In birds, the reliability of digital endocast measurements as volume proxies for the two largest brain regions - the telencephalon and cerebellum - remains to be validated despite their use as proxies e.g. of cognitive performance or flight ability. We here use the largest dataset of histology and digital endocasts to date, including 136 species from 25 avian orders, to compare digital endocast surface area measurements with actual brain volumes of the telencephalon, cerebellum, and whole-brain endocast. Using linear and phylogenetically informed regression analyses, we demonstrate that endocast surfaces are strongly correlated with their brain volume counterparts for both absolute and relative size. This provides empirical support for using endocast-derived cerebellar and telencephalic surface areas in existing and future studies of living and extinct birds, with potential to expand to the dinosaur-bird transition in the future.

animal behavior and cognition↗

Testing hypotheses of skull function with comparative finite element analysis: three methods reveal contrasting results

Comparative finite element analysis often involves standardising aspects of the models to test equivalent loading scenarios across species. However, in the context of feeding biomechanics of the vertebrate skull, what is considered "equivalent" can depend on the hypothesis. We use 13 skulls from diverse group of marsupial bettongs and potoroos (Potoroidae) to demonstrate that that scaling muscle forces to standardise unique aspects of biting mechanics can produce contrasting results of comparative stress or strain that are differentially suited to test specific kinds of hypotheses. We propose three categories of hypotheses for skull biting mechanics which each involve a unique method of muscle scaling: those comparing (1) the skulls efficiency in distributing input muscle forces, via standardising input muscle force to size, (2) morphological biting adaptation through standardising mechanical advantage to simulate size-independent, equivalent bites, and (3) feeding ecology affected by size, such as niche partitioning, via standardising bite reaction force. SUMMARY STATEMENTCommon approaches for scaling muscle forces in skull finite element models might not always offer reliable results for all hypotheses. We provide a framework for selecting the appropriate method.

evolutionary biology↗

Facing the facts: Adaptive trade-offs along body size ranges determine mammalian craniofacial scaling

The mammalian cranium (skull without lower jaw) is representative of mammalian diversity and is thus of particular interest to mammalian biologists across disciplines. One widely retrieved pattern accompanying mammalian cranial diversification is referred to as "craniofacial evolutionary allometry" (CREA). This posits that "adults of larger species, in a group of closely related mammals, tend to have relatively longer faces and smaller braincases". However, no process has been officially suggested to explain this pattern, there are many exceptions, and its predictions potentially conflict with well-established biomechanical principles. Understanding the mechanisms behind CREA and causes for deviations from the pattern therefore has tremendous potential to explain allometry and diversification of the mammalian cranium. Here, we propose an amended framework to characterise the CREA pattern more clearly, in that "longer faces" can arise through several kinds of evolutionary change, including elongation of the rostrum, retraction of the jaw muscles, or a more narrow or shallow skull, which all result in a generalised gracilisation of the facial skeleton with increased size. We define a standardised workflow to test for the presence of the pattern, using allometric shape predictions derived from geometric morphometrics analysis, and apply this to 22 mammalian families including marsupials, rabbits, rodents, bats, carnivores, antelope, and whales. Our results show that increasing facial gracility with size is common, but not necessarily as ubiquitous as previously suggested. To address the mechanistic basis for this variation, we then review cranial adaptations for harder biting. These dictate that a more gracile cranium in larger species must represent a sacrifice in the ability to produce or withstand harder bites, relative to size. This leads us to propose that facial gracilisation in larger species is often a product of bite force allometry and phylogenetic niche conservatism, where more closely related species tend to exhibit more similar feeding ecology and biting behaviours and, therefore, absolute (size-independent) bite force requirements. Since larger species can produce the same absolute bite forces as smaller species with less effort, we propose that relaxed bite force demands can permit facial gracility in response to bone optimisation and alternative selection pressures. Thus, mammalian facial scaling represents an adaptive by-product of the shifting importance of selective pressures occurring with increased size. A reverse pattern of facial "shortening" can accordingly also be found, and is retrieved in several cases here, where larger species incorporate novel feeding behaviours involving greater bite forces. We discuss multiple exceptions to a bite force-mediated influence on facial length across mammals which lead us to argue that ecomorphological specialisation of the cranium is likely to be the primary driver of facial scaling patterns, with developmental and/or phylogenetic constraints a secondary factor. A potential for larger species to have a wider range of cranial functions when less constrained by biomechanical demands might also explain why selection for larger sizes seems to be prevalent in some mammalian clades. The interplay between adaptation and constraint across size ranges thus presents an interesting consideration for a mechanistically grounded investigation of mammalian cranial allometry.

evolutionary biology↗

Using 3D geometric morphometrics to aid taxonomic and ecological understanding of a recent speciation event within a small Australian marsupial (genus Antechinus)

Taxonomic distinction of species forms the foundation of biodiversity assessments and conservation priorities. However, traditional morphological and/or genetics-based taxonomic assessments frequently miss the opportunity of elaborating on the ecological and functional context of species diversification. Here, we used 3D geometric morphometrics of the cranium to improve taxonomic differentiation and add eco-morphological characterisation of a young cryptic divergence within the marsupial carnivorous genus Antechinus. Specifically, we used 168 museum specimens to characterise the recently proposed clades A. stuartii "south", A. stuartii "north" and A. subtropicus. Beyond slight differences attributable to overall size (and therefore not necessarily diagnostic), we also found clear allometry-independent shape variation. This allowed us to define new, easily measured diagnostic traits in the palate, which differentiate the three clades. Contrary to previous suggestions, we found no support for a latitudinal gradient as causing the differentiation between the clades. However, skull shape co-varied with temperature and precipitation seasonality, suggesting that the clades may be adapted to environmental variables that are likely to be impacted by climate change. Our study demonstrates the use of 3D geometric morphometrics to improve taxonomic diagnosis of cryptic mammalian species, while providing perspectives on the adaptive origins and potential future threats of mammalian diversity.

zoology↗

Testing hypotheses of marsupial brain size variation using phylogenetic multiple imputations and a Bayesian comparative framework

Considerable controversy exists about which hypotheses and variables best explain mammalian brain size variation. We use a new, high-coverage dataset of marsupial brain and body sizes, and the first phylogenetically imputed full datasets of 16 predictor variables, to model the prevalent hypotheses explaining brain size evolution using phylogenetically corrected Bayesian generalised linear mixed-effects modelling. Despite this comprehensive analysis, litter size emerges as the only significant predictor. Marsupials differ from the more frequently studied placentals in displaying much lower diversity of reproductive traits, which are known to interact extensively with many behavioural and ecological predictors of brain size. Our results therefore suggest that studies of relative brain size evolution in placental mammals may require targeted co-analysis or adjustment of reproductive parameters like litter size, weaning age, or gestation length. This supports suggestions that significant associations between behavioural or ecological variables with relative brain size may be due to a confounding influence of the extensive reproductive diversity of placental mammals.

evolutionary biology↗

Global elongation and high shape flexibility as an evolutionary hypothesis of accommodating mammalian brains into skulls

Little is known about how the large brains of mammals are accommodated into the dazzling diversity of their skulls. It has been suggested that brain shape is influenced by relative brain size, that it evolves or develops according to extrinsic or intrinsic mechanical constraints, and that its shape can provide insights into its proportions and function. Here, we characterise the shape variation among 84 marsupial cranial endocasts of 57 species including fossils, using 3D geometric morphometrics and virtual dissections. Statistical shape analysis revealed four main patterns: over half of endocast shape variation ranges between elongate and straight to globular and inclined; little allometric variation with respect to centroid size, and none for relative volume; no association between locomotion and endocast shape; limited association between endocast shape and previously published histological cortex volumes. Fossil species tend to have smaller cerebral hemispheres. We find divergent endocast shapes in closely related species and within species, and diverse morphologies superimposed over the main variation. An evolutionarily and individually malleable brain with a fundamental tendency to arrange into a spectrum of elongate-to-globular shapes - possibly mostly independent of brain function - may explain the accommodation of brains within the enormous diversity of mammalian skull form.

evolutionary biology↗

Relative demographic susceptibility does not explain the extinction chronology of Sahul's megafauna

The causes of Sahuls megafauna extinctions remain uncertain, although multiple, interacting factors were likely responsible. To test hypotheses regarding plausible ecological mechanisms underlying these extinctions, we constructed the first stochastic, age-structured models for 13 extinct megafauna species from five functional/taxonomic groups, as well as 8 extant species within these groups for comparison. Perturbing specific demographic rates individually, we tested which species were more demographically susceptible to extinction, and then compared these relative sensitivities to the fossil-derived extinction chronology. Here we show that the macropodiformes were the most resilient to extinction, followed by carnivores, monotremes, vombatiform herbivores, and large birds. Five of the eight extant species were as or more susceptible than were the extinct species. There was no clear relationship between extinction susceptibility and the extinction chronology for any perturbation scenario, but body mass and generation length explained much of the variation in relative risk. Our models reveal that the actual mechanisms leading to extinction were unlikely related to variation in demographic susceptibility per se, but were driven instead by finer-scale variation in climate change and/or human prey choice and relative hunting success.

ecology↗

Australian rodents reveal conserved Cranial Evolutionary Allometry across 10 million years of murid evolution

Among vertebrates, placental mammals are particularly variable in the covariance between their cranial shapes and body size (allometry), with the notable exception of rodents. Australian murid rodents present an opportunity to assess the cause of this anomaly because they radiated on an ecologically diverse continent unique for lacking other terrestrial placentals. Here we used 3D geometric morphometrics to quantify species-level and evolutionary allometries in 38 species (317 crania) from all Australian murid genera. We ask if ecological opportunity resulted in greater allometric diversity; conversely, we test if intrinsic constraints and/or stabilizing selection conserved allometry. To increase confidence in species-level allometric slopes, we introduce a new phylogeny-based method of bootstrapping and randomly resampling across the whole sample. We found exceedingly conserved allometry across the 10 million year split between Mus and the clade containing Australian murids. Cranial shapes followed craniofacial evolutionary allometry (CREA) patterns, with larger species having relatively longer snouts and smaller braincases. CREA is consistent with both intrinsic constraints and stabilizing selection hypotheses for conserved allometry. However, large-bodied frugivores evolved faster, while carnivorous specialists showed skull modifications known to conflict with masticatory efficiency. These results suggest a strong role of stabilizing selection on the masticatory apparatus of murid rodents.

evolutionary biology↗

Shifting spaces: which disparity or dissimilarity metrics best summarise occupancy in multidimensional spaces?

O_LIMultidimensional analysis of traits are now a common toolkit in ecology and evolution and are based on trait-spaces in which each dimension summarise the observed trait combination (a morphospace or an ecospace). Observations of interest will typically occupy a subset of this trait-space, and researchers will apply one or more metrics to quantify the way in which organisms \"inhabit\" that trait-space. In macroevolution and ecology these metrics are referred to as disparity or dissimilarity metrics and can be generalised as space occupancy metrics. Researchers use these metrics to investigate how space occupancy changes through time, in relation to other groups of organisms, and in response to global environmental changes, such as global warming events or mass extinctions. However, the mathematical and biological meaning of most space occupancy metrics is vague with the majority of widely-used metrics lacking formal description.\nC_LIO_LIHere we propose a broad classification of space occupancy metrics into three categories that capture changes in volume, density, or position. We analyse the behaviour of 25 metrics to study changes in trait-space volume, density and position on a series of simulated and empirical datasets.\nC_LIO_LIWe find no one metric describes all of trait-space but that some metrics are better at capturing certain aspects compared to other approaches and that their performance depends on both the trait-space and the hypothesis analysed. However, our results confirm the three broad categories (volume, density and position) and allow to relate changes in any of these categories to biological phenomena.\nC_LIO_LISince the choice of space occupancy metric should be specific to the data and question at had, we introduced moms, a user-friendly tool based on a graphical interface that allows users to both visualise and measure changes space occupancy for any metric in simulated or imported trait-spaces. Users are also provided with tools to transform their data in space (e.g. contraction, displacement, etc.). This tool is designed to help researchers choose the right space occupancy metrics, given the properties of their trait-space and their biological question.\nC_LI

evolutionary biology↗

Primate hippocampus size and organisation are predicted by sociality but not diet

The hippocampus is well known for its roles in spatial navigation and memory, but it is organized into regions that have different connections and functional specializations. Notably, the region CA2 has a role in social and not spatial cognition, as is the case for the regions CA1 and CA3 that surround it. Here we investigated the evolution of the hippocampus in terms of its size and organization in relation to the evolution of social and ecological variables in primates, namely home range, diet and different measures of group size. We found that the volumes within the whole cornu ammonis coevolve with group size, while only the volume of CA1 and subiculum can also be predicted by home range. On the other hand, diet, expressed as a shift from folivory toward frugivory, was shown to not be related to hippocampal volume. Interestingly, CA2 was shown to exhibit phylogenetic signal only against certain measures of group size but not with ecological factors. We also found that sex differences in the hippocampus are related to body size sex dimorphism. This is in line with reports of sex differences in hippocampal volume in non-primates that are related to social structure and sex differences in behaviour. Our findings support the notion that in primates, the hippocampus is a mosaic structure evolving in line with social pressures, where certain subsections evolve in line with spatial ability too.

evolutionary biology↗

Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

BackgroundWithin-species skull shape variation of marsupial mammals is widely considered low and strongly size-dependent (allometric), possibly due to developmental constraints arising from the altricial birth of marsupials. However, species whose skulls are impacted by strong muscular stresses - particularly those produced through mastication of tough food items - may not display such intrinsic patterns very clearly because of the known plastic response of bone to muscle activity of the individual. In such cases, shape variation should not be dominated by allometry; ordination of shape in a geometric morphometric context through principal component analysis (PCA) should reveal main variation in areas under masticatory stress (incisor region/zygomatic arches/mandibular ramus); but this main variation should emerge from high individual variability and thus have low eigenvalues.\n\nResultsWe assessed the evidence for high individual variation through 3D geometric morphometric shape analysis of crania and mandibles of thre species of grazing-specialized wombats, whose diet of tough grasses puts considerable strain on their masticatory system. As expected, we found little allometry and low Principal Component 1 (PC1) eigenvalues within crania and mandibles of all three species. Also as expected, the main variation was in the muzzle, zygomatic arches, and masticatory muscle attachments of the mandibular ramus. We then implemented a new test to ask if the landmark variation reflected on PC1 was reflected in individuals with opposite PC1 scores and with opposite shapes in Procrustes space. This showed that correspondence between individual and ordinated shape variation was limited, indicating high levels of individual variability in the masticatory apparatus.\n\nDiscussionOur results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern. Rather, they support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials (and possibly other mammals) with high masticatory stresses, making it difficult to understand the degree to which intrinsic constraint act on shape variation at the within-species level. We conclude that studies that link micro- and macroevolutionary patterns of shape variation might benefit from a focus on species with low-impact mastication, such as carnivorous or frugivorous species.

evolutionary biology↗