Population genomic diversity and structure in the golden bandicoot: a history of isolation, extirpation, and conservation.

Using genetic information to develop and implement conservation programs is vital for maintaining biodiversity and ecosystem resilience. Evaluation of the genetic variability within and among remnant populations can inform management of both natural and translocated populations to maximise species' adaptive potential, mitigate negative impacts of inbreeding, and subsequently minimise risk of extinction. Here we use reduced representation sequencing to undertake a genetic assessment of the golden bandicoot (Isoodon auratus), a threatened marsupial endemic to Australia. The currently recognised taxon consists of three subspecies distributed among multiple natural and translocated populations. After confirming the genetic distinctiveness of I. auratus from two closely related taxa, I. fusciventer and I. macrourus, we identified four genetic clusters within I. auratus. These clusters exhibited substantial genetic differentiation (pairwise FST values ranging from 0.18 to 0.65, pairwise DXY ranging from 0.1 to 0.168), reflecting long-term isolation of some populations on offshore islands and the influence of genetic drift. Mainland natural populations in the Kimberley region had the highest genetic diversity and the largest contribution to overall allelic and gene diversity compared to both natural and translocated island populations. A population translocated to Guluwuru Island in the Northern Territory had the lowest genetic diversity. Our data suggest that island populations can appear genetically unique due to genetic drift and this needs to be taken into account when considering genetic diversity in conservation efforts to maintain overall genetic diversity of the species. We effectively demonstrate how genomic information can guide practical conservation planning, especially when declining species are represented by multiple isolated populations.

All-a-glow: spectral characteristics confirm widespread fluorescence for mammals.

Mammalian fluorescence has been reported from numerous species of monotreme, marsupial and placental mammal. However, it is unknown how widespread this phenomenon is among mammals, it is unclear for many species if these observations of 'glowing' are true fluorescence and the biological function of fluorescence remains undetermined. We examined a wide range of mammal species held in a museum collection for the presence of apparent fluorescence using UV light, and then analysed a subset of preserved and non-preserved specimens by fluorescent spectroscopy at three different excitation wavelengths to assess whether the observations were fluorescence or optical scatter, and the impact of specimen preservation. We also evaluated if fluorescence was related to biological traits. We found that fluorescence is widespread in mammalian taxa; we identified examples of the phenomena among 125 species representing all 27 living mammalian orders and 79 families. For a number of model species, there was no evidence of a corresponding shift in the emission spectra when the wavelength of excitation was shifted, suggesting that observations of 'glowing' mammals were indeed fluorescence. Preservation method impacted the intensity of fluorescence. Fluorescence was most common and most intense among nocturnal species and those with terrestrial, arboreal and fossorial habits, with more of their body being more fluorescent. It remains unclear if fluorescence has any specific biological role for mammals. It appears to be a ubiquitous property of unpigmented fur and skin but may function to make these areas appear brighter and therefore enhance visual signalling, especially for nocturnal species.

Linking life history to landscape for threatened species conservation in a multiuse region.

Landscape-scale conservation that considers metapopulation dynamics will be essential for preventing declines of species facing multiple threats to their survival. Toward this end, we developed a novel approach that combines occurrence records, spatial-environmental data, and genetic information to model habitat, connectivity, and patterns of genetic structure and link spatial attributes to underlying ecological mechanisms. Using the threatened northern quoll (Dasyurus hallucatus) as a case study, we applied this approach to address the need for conservation decision-making tools that promote resilient metapopulations of this threatened species in the Pilbara, Western Australia, a multiuse landscape that is a hotspot for biodiversity and mining. Habitat and connectivity were predicted by different landscape characteristics. Whereas habitat suitability was overwhelmingly driven by terrain ruggedness, dispersal was facilitated by proximity to watercourses. Although there is limited evidence for major physical barriers in the Pilbara, areas with high silt and clay content (i.e., alluvial and hardpan plains) showed high resistance to dispersal. Climate subtlety shaped distributions and patterns of genetic turnover, suggesting the potential for local adaptation. By understanding these spatial-environmental associations and linking them to life-history and metapopulation dynamics, we highlight opportunities to provide targeted species management. To support this, we have created habitat, connectivity, and genetic uniqueness maps for conservation decision-making in the region. These tools have the potential to provide a more holistic approach to conservation in multiuse landscapes globally.

La conservación a nivel del paisaje que incluye las dinámicas metapoblacionales será esencial para prevenir la declinación de especies con múltiples amenazas a su supervivencia. Enfocados en este fin, desarrollamos una estrategia novedosa que combina los registros presenciales, datos espacio-ambientales e información genética para modelar la conectividad de hábitat y los patrones de estructura genética y conectar los atributos espaciales con los mecanismos ecológicos subyacentes. Usamos al cuol del norte (Dasyurus hallucatus) como estudio de caso para aplicar esta estrategia y abordar la necesidad de herramientas de decisión en la conservación que promuevan metapoblaciones resilientes de esta especie en la Pilbara de Australia Occidental, un paisaje multiusos que es un punto caliente para la biodiversidad y la minería. Diferentes características del paisaje pronosticaron la conectividad y el hábitat. Mientras que la escabrosidad del terreno causó enormemente la idoneidad del hábitat, la dispersión estuvo propiciada por la proximidad a los cauces. Aunque hay evidencias limitadas de barreras físicas importantes en la Pilbara, las áreas con un contenido elevado de limo y arcilla (es decir, planicies aluviales y de alio) mostraron una gran resistencia a la dispersión. La matización climática determinó la distribución y los patrones del recambio genético, lo que sugiere un potencial para la adaptación local. Si entendemos estas asociaciones espacio-ambientales y las conectamos con las dinámicas metapoblacionales y de historia de vida, podemos resaltar las oportunidades para proporcionar un manejo focalizado de la especie. Para respaldar esto hemos creado mapas de hábitat, conectividad y singularidad genética para las decisiones de conservación en la región. Estas herramientas tienen el potencial de proporcionar una estrategia más holística para la conservación en los paisajes multiusos de todo el mundo.

Hiding in plain sight: two new species of diminutive marsupial (Dasyuridae: Planigale) from the Pilbara, Australia.

Many of Australias smaller marsupial species have been taxonomically described in just the past 50 years, and the Dasyuridae, a speciose family of carnivores, is known to harbour many cryptic taxa. Evidence from molecular studies is being increasingly utilised to help revise species boundaries and focus taxonomic efforts, and research over the past two decades has identified several undescribed genetic lineages within the dasyurid genus Planigale. Here, we describe two new species, Planigale kendricki sp. nov. (formerly known as Planigale 1) and P. tealei sp. nov. (formerly known as Planigale sp. Mt Tom Price). The two new species have broadly overlapping distributions in the Pilbara region of Western Australia. The new species are genetically distinct from each other and from all other members of the genus, at both mitochondrial and nuclear loci, and morphologically, in both external and craniodental characters. The new species are found in regional sympatry within the Pilbara but occupy different habitat types at local scales. This work makes a start at resolving the cryptic diversity within Planigale at a time when small mammals are continuing to decline throughout Australia.

Keeping an ear out: size relationship of the tympanic bullae and pinnae in bandicoots and bilbies (Marsupialia: Peramelemorphia).

Bandicoots and bilbies (Order Peramelemorphia) occupy a broad range of habitats across Australia and New Guinea, from open, arid deserts to dense forests. This once diverse group has been particularly vulnerable to habitat loss and introduced eutherian predators, and numerous species extinctions and range retractions have occurred. Understanding reasons for this loss requires greater understanding of their biology. Morphology of the pinnae and tympanic bullae varies markedly among species. As hearing is important for both predator avoidance and prey location, the variability in ear morphology could reflect specialization and adaptation to specific environments, and therefore be of conservation relevance. We measured 798 museum specimens representing 29 species of Peramelemorphia. Controlling for phylogenetic relatedness and head length, pinna surface area was weakly negatively correlated with average precipitation (rainfall being our surrogate measure of vegetation productivity/complexity), and there were no environmental correlates with effective diameter (pinna width). Controlling for phylogenetic relatedness and skull length, tympanic bulla volume was negatively correlated with precipitation. Species that inhabited drier habitats, which would be open and allow sound to carry further with less obstruction, had relatively larger pinnae and tympanic bullae. In contrast, species from higher rainfall habitats, where sounds would be attenuated and diffused by dense vegetation, had the smallest pinnae and bullae, suggesting that low-frequency hearing is not as important in these habitats. Associations with temperature did not reach statistical significance. These findings highlight linkages between hearing traits and habitat that can inform conservation and management strategies for threatened species.

Species identification of Australian marsupials using collagen fingerprinting.

The study of faunal remains from archaeological sites is often complicated by the presence of large numbers of highly fragmented, morphologically unidentifiable bones. In Australia, this is the combined result of harsh preservation conditions and frequent scavenging by marsupial carnivores. The collagen fingerprinting method known as zooarchaeology by mass spectrometry (ZooMS) offers a means to address these challenges and improve identification rates of fragmented bones. Here, we present novel ZooMS peptide markers for 24 extant marsupial and monotreme species that allow for genus-level distinctions between these species. We demonstrate the utility of these new peptide markers by using them to taxonomically identify bone fragments from a nineteenth-century colonial-era pearlshell fishery at Bandicoot Bay, Barrow Island. The suite of peptide biomarkers presented in this study, which focus on a range of ecologically and culturally important species, have the potential to significantly amplify the zooarchaeological and paleontological record of Australia.

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 characterize the shape variation among 84 marsupial cranial endocasts of 57 species including fossils, using three-dimensional geometric morphometrics and virtual dissections. Statistical shape analysis revealed four main patterns: over half of endocast shape variation ranges from 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.

Review of the methods used for calculating physiological cross-sectional area (PCSA) for ecological questions.

This review examines literature that used physiological cross-sectional area (PCSA) as a representative measure of an individual muscle's maximal isometric force production. PCSA is used to understand the muscle architecture and how a trade-off between muscle force and muscle contractile velocity reflect adaptations of the musculoskeletal system as a reflection of functional demands. Over the decades, methods have been developed to measure muscle volume, fascicle lengths, and pennation angle to calculate PCSA. The advantages and limitations of these methods (especially the inclusion/elimination of pennation angle) are discussed frequently; however, these method descriptions are scattered throughout the literature. Here, we reviewed and summarised the different approaches to collecting and recording muscle architectural properties to subsequently calculate PCSA. By critically discussing the advantages and limitations of each methodology, we aim to provide readers with an overview of repeatable methods to assess muscle architecture. This review may serve as a guide to facilitate readers searching for the appropriate techniques to calculate PCSA and measure muscle architecture to be applied in ecomorphology research. RESEARCH HIGHLIGHTS: Discuss the theories behind PCSA in a synthesised review to inform researchers about PCSA methodology.

Hidden in plain sight: reassessment of the pig-footed bandicoot, Chaeropus ecaudatus (Peramelemorphia, Chaeropodidae), with a description of a new species from central australia, and use of the fossil record to trace its past distribution.

The Pig-footed Bandicoot, Chaeropus ecaudatus, an extinct arid-adapted bandicoot, was named in 1838 based on a specimen without a tail from the Murray River in New South Wales. Two additional species were later named, C. castanotis and C. occidentalis, which have since been synonymised with C. ecaudatus. Taxonomic research on the genus is rather difficult because of the limited material available for study. Aside from the types of C. castanotis and C. occidentalis housed at the Natural History Museum in London, and the type of C. ecaudatus at the Australian Museum in Sydney, there are fewer than 30 other modern specimens in other collections scattered around the world. Examining skeletal and dental characters for several specimens, and using a combination of traditional morphology, morphometrics, palaeontology and molecular phylogenetics, we have identified two distinct species, C. ecaudatus and C. yirratji sp. nov., with C. ecaudatus having two distinct subspecies, C. e. ecaudatus and C. e. occidentalis. We use palaeontological data to reconstruct the pre-European distribution of the two species, and review the ecological information known about these extinct taxa.

Covariation between forelimb muscle anatomy and bone shape in an Australian scratch-digging marsupial: Comparison of morphometric methods.

The close association between muscle and bone is broadly intuitive; however, details of the covariation between the two has not been comprehensively studied. Without quantitative understanding of how muscle anatomy influences bone shape, it is difficult to draw conclusions of the significance of many morphological traits of the skeleton. In this study, we investigated these relationships in the Quenda (Isoodon fusciventer), a scratch-digging marsupial. We quantified the relationships between forelimb muscle anatomy and bone shape for animals representing a range of body masses (124-1,952 g) using two-block partial least square analyses. Muscle anatomy was quantified as muscle mass and physiological cross-sectional area (PCSA), and we used two morphometric methods to characterize bone shape: seven indices of linear bone proportions, and landmarks analysis. Bone shape was significantly correlated with body mass, reflecting allometric bone growth. Of the seven bone indices, only shoulder moment index (SMI) and ulna robustness index (URI) showed a significant covariation with muscle anatomy. Stronger relationships between muscle anatomy and forelimb bone shape were found using the landmark coordinates: muscle mass and PCSA were correlated with the geometric shape of the scapula, humerus, and third metacarpal, but to a lesser extent with shape of the ulna. Overall, our data show that landmark coordinates are more sensitive than bone indices to capturing shape changes evident throughout ontogeny, and is therefore a more appropriate method to investigate covariation with forelimb muscle anatomy. Single-species studies investigating ontogeny require refined methods to accurately develop understanding of the important relationships between muscle force generation and bone shape remodeling. Landmark analyses provide such a method.

Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer).

Many mammals dig, either during foraging to access subsurface food resources, or in creating burrows for shelter. Digging requires large forces produced by muscles and transmitted to the soil via the skeletal system; thus fossorial mammals tend to have characteristic modifications of the musculoskeletal system that reflect their digging ability. Bandicoots (Marsupialia: Peramelidae) scratch-dig mainly to source food, searching for subterranean food items including invertebrates, seeds, and fungi. They have musculoskeletal features for digging, including shortened, robust forelimb bones, large muscles, and enlarged muscle attachment areas. Here, we compared changes in the ontogenetic development of muscles associated with digging in the Quenda (Isoodon fusciventer). We measured muscle mass (m m ), pennation angle, and fiber length (FL) to calculate physiological cross-sectional area (PCSA; a proxy of maximum isometric force) as well as estimate the maximum isometric force (Fmax) for 34 individuals ranging in body size from 124 to 2,390 g. Males grow larger than females in this bandicoot species, however, we found negligible sex differences in mass-specific m m , PCSA or FL for our sample. Majority of the forelimb muscles PCSA showed a positive allometric relationship with total body mass, while m m and FL in the majority of forelimb muscles showed isometry. Mechanical similarity was tested, and two thirds of forelimb muscles maximum isometric forces (Fmax) scaled with isometry; therefore the forelimb is primarily mechanical similar throughout ontogeny. PCSA showed a significant difference between scaling slopes between main movers in the power stroke, and main movers of the recovery stroke of scratch-digging. This suggests that some forelimb muscles grow with positive allometry, specially these associated with the power stroke of digging. Intraspecific variation in PCSA is rarely considered in the literature, and thus this is an important study quantifying changes in muscle architectural properties with growth in a mammalian model of scratch-digging.

Total evidence analysis of the phylogenetic relationships of bandicoots and bilbies (Marsupialia: Peramelemorphia): reassessment of two species and description of a new species.

The phylogenetic relationships of bandicoots and bilbies have been somewhat problematic, with conflicting results between morphological work and molecular data. This conflict makes it difficult to assess the taxonomic status of species and subspecies within this order, and also prevents accurate evolutionary assessments. Here, we present a new total evidence analysis, combining the latest cranio-dental morphological matrix containing both modern and fossil taxa, with molecular data from GenBank. Several subspecies were scored in the morphological dataset to match the molecular data available. Both parsimony and Bayesian analyses were performed, giving similar topologies except for the position of four fossil taxa. Total evidence dating places the peramelemorphian crown origin close to the Oligocene/Miocene boundary, and the radiations of most modern genera beginning in the Late Miocene or Early Pliocene. Our results show that some species and subspecies require taxonomic reassessment, and are revised here. We also describe a new, extinct species from the Nullarbor region. This suggests that the number of recently extinct peramelemorphian species is likely to further increase.

Correction to 'Oldest fossil remains of the enigmatic pig-footed bandicoot show rapid herbivorous evolution'.

[This corrects the article DOI: 10.1098/rsos.160089.].

Oldest fossil remains of the enigmatic pig-footed bandicoot show rapid herbivorous evolution.

The pig-footed bandicoot, Chaeropus ecaudatus, is one of the most enigmatic Australian marsupials, which went extinct in the late 1950s probably as a result of European colonization. It is unusual in being the only marsupial to have evolved reduction of digits on both fore and hind feet, with the forefeet being pig-like (two toes) and the hind feet being horse-like (one toe). According to molecular phylogenetic analyses, Chaeropus diverged from other bandicoots (Peramelidae), and the bilbies (Thylacomyidae) by the mid-Late Oligocene. This is considerably earlier than suggested by the fossil record, with the current oldest specimens being Late Pleistocene in age. Here, I report the oldest fossils of Chaeropus, representing a new species, Chaeropus baynesi from the Late Pliocene to Early Pleistocene (2.47-2.92 Ma) Fisherman's Cliff Local Fauna, Moorna Formation, New South Wales, Australia, and extending the fossil record of the genus and family by at least 2 million years. Chaeropus baynesi is less high crowned than C. ecaudatus and lacks lateral blade development on lower molars, suggesting that it was unlikely to be grazing. This suggests that Chaeropus must have adapted rapidly to the drying conditions and changes in environments, and would have become a grazer in a very short period of time.

Investigating dental variation in Perameles nasuta Geoffroy, 1804, with morphological evidence to raise P. nasuta pallescens Thomas, 1923 to species rank.

The long-nosed bandicoot, Perameles nasuta Geoffroy, 1804, found on the east coast of Australia, has two subspecies, P. n. nasuta Geoffroy, 1804 and P. n. pallescens Thomas, 1923. Until recently, this distinction has remained untested by either morphological or molecular studies. Based on a recently published but limited molecular study, two publications have recommended that P. pallescens be treated as a species distinct from P. nasuta. Here, the morphological distinction between P. pallescens and P. nasuta is tested by examination of museum specimens from throughout the combined species range, using both qualitative and quantitative techniques. No external features and very few cranial features were found to separate the two subspecies. However, dental morphology and measurements are effective at distinguishing two geographically distinct populations; while a complex pattern of clinal vs non-clinal trends in cranial size suggest a genetic disjunction that corresponds with the dentally-defined geographic groups. These findings support the raising of P. pallescens to species level. In terms of dental features, P. pallescens was found to be most similar to the fossil P. sobbei. The morphological phylogeny recovered P. pallescens as sister to P. nasuta, when no fossil Perameles taxa were included, probably as a result of little cranial differentiation between them. When fossil Perameles were included, the relationships between species of Perameles were unresolved, probably as a result of P. sobbei lacking cranial remains.

A new species of the basal "kangaroo" Balbaroo and a re-evaluation of stem macropodiform interrelationships.

Exceptionally well-preserved skulls and postcranial elements of a new species of the plesiomorphic stem macropodiform Balbaroo have been recovered from middle Miocene freshwater limestone deposits in the Riversleigh World Heritage Area of northwestern Queensland, Australia. This constitutes the richest intraspecific sample for any currently known basal "kangaroo", and, along with additional material referred to Balbaroo fangaroo, provides new insights into structural variability within the most prolific archaic macropodiform clade--Balbaridae. Qualitative and metric evaluations of taxonomic boundaries demonstrate that the previously distinct species Nambaroo bullockensis is a junior synonym of B. camfieldensis. Furthermore, coupled Maximum Parsimony and Bayesian phylogenetic analyses reveal that our new Balbaroo remains represent the most derived member of the Balbaroo lineage, and are closely related to the middle Miocene B. camfieldensis, which like most named balbarid species is identifiable only from isolated jaws. The postcranial elements of Balbaroo concur with earlier finds of the stratigraphically oldest balbarid skeleton, Nambaroo gillespieae, and suggest that quadrupedal progression was a primary gait mode as opposed to bipedal saltation. All Balbaroo spp. have low-crowned bilophodont molars, which are typical for browsing herbivores inhabiting the densely forested environments envisaged for middle Miocene northeastern Australia.

Vertebrate palaeontology of Australasia into the twenty-first century.

The 13th Conference on Australasian Vertebrate Evolution Palaeontology and Systematics (CAVEPS) took place in Perth, Western Australia, from 27 to 30 April 2011. This biennial meeting was jointly hosted by Curtin University, the Western Australian Museum, Murdoch University and the University of Western Australia. Researchers from diverse disciplines addressed many aspects of vertebrate evolution, including functional morphology, phylogeny, ecology and extinctions. New additions to the fossil record were reported, especially from hitherto under-represented ages and clades. Yet, application of new techniques in palaeobiological analyses dominated, such as dental microwear and geochronology, and technological advances, including computed tomography and ancient biomolecules. This signals a shift towards increased emphasis in interpreting broader evolutionary patterns and processes. Nonetheless, further field exploration for new fossils and systematic descriptions will continue to shape our understanding of vertebrate evolution in this little-studied, but most unusual, part of the globe.