Manganese Exacerbates Seasonal Health Declines in a Suicidally Breeding Mammal.

Reproductive costs must be balanced with survival to maximize lifetime reproductive rates; however, some organisms invest in a single, suicidal bout of breeding known as semelparity. The northern quoll (Dasyurus hallucatus) is an endangered marsupial in which males, but not females, are semelparous. Northern quolls living near mining sites on Groote Eylandt, Northern Territory, Australia, accumulate manganese (Mn) in their brains, testes, and hair, and elevated Mn impacts motor performance. Whether Mn is associated with other health declines is yet unknown. In the present study we show that male and female northern quolls with higher Mn accumulation had a 20% reduction in immune function and a trend toward reduced cortisol concentrations in hair. The telomere lengths of male quolls did not change pre- to postbreeding, but those with higher Mn levels had longer telomeres; in contrast, the telomeres of females shortened during the breeding season but recovered between the first year and second year of breeding. In addition, the telomeres of quolls that were recaptured declined at significantly higher rates in quolls with higher Mn between prebreeding, breeding, and/or postbreeding seasons. Future research should determine whether changes in cortisol, immune function, or telomere length affect reproductive output or survival-particularly for semelparous males. Environ Toxicol Chem 2024;43:74-86. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Potential for host-symbiont communication via neurotransmitters and neuromodulators in an aneural animal, the marine sponge Amphimedon queenslandica.

Interkingdom signalling within a holobiont allows host and symbionts to communicate and to regulate each other's physiological and developmental states. Here we show that a suite of signalling molecules that function as neurotransmitters and neuromodulators in most animals with nervous systems, specifically dopamine and trace amines, are produced exclusively by the bacterial symbionts of the demosponge Amphimedon queenslandica. Although sponges do not possess a nervous system, A. queenslandica expresses rhodopsin class G-protein-coupled receptors that are structurally similar to dopamine and trace amine receptors. When sponge larvae, which express these receptors, are exposed to agonists and antagonists of bilaterian dopamine and trace amine receptors, we observe marked changes in larval phototactic swimming behaviour, consistent with the sponge being competent to recognise and respond to symbiont-derived trace amine signals. These results indicate that monoamines synthesised by bacterial symbionts may be able to influence the physiology of the host sponge.

Is Mushy Tuna Syndrome a Growing Problem for the Tuna Industry?

Reducing food loss and waste is crucial for a sustainable global food system and an efficient use of natural resources. Fast-growing tuna provides a key contribution to global nutrition targets; however, reports suggest that an appreciable proportion of the catch is lost from its value chain due to flesh quality issues, one of which is Mushy Tuna Syndrome (MTS). MTS-affected tuna flesh becomes soft and pasty, unfit for canning or human consumption, resulting in high wastage of partially processed material. We investigated the prevalence of MTS globally by surveying the tuna industry using a questionnaire. Of the responses from 32 companies across 14 nations, 97% acknowledged MTS as an issue that predominantly affects skipjack (Katsuwonus pelamis) tuna. The cost of rejects reported by participants from 2017 to 2019 varied greatly, from less than 1000 USD per year to over 1 million USD. The median cost was over 60,000 USD and the average rejection rate was 1.8%. The occurrence of MTS was noted to be seasonal, mainly in the summer months. More than half of the respondents who experience MTS reported an increasing trend of occurrence. Industry perceptions suggest MTS causes are associated with environmental, physiological, and biological factors. The survey results highlight that MTS is prevalent in the industry and demonstrate the need to identify amelioration strategies for the fishers and processors to minimise loss and maximise resource efficiency.

The relative performance of geometric morphometrics and linear-based methods in the taxonomic resolution of a mammalian species complex.

Morphology-based taxonomic research frequently applies linear morphometrics (LMM) in skulls to quantify species distinctions. The choice of which measurements to collect generally relies on the expertise of the investigators or a set of standard measurements, but this practice may ignore less obvious or common discriminatory characteristics. In addition, taxonomic analyses often ignore the potential for subgroups of an otherwise cohesive population to differ in shape purely due to size differences (or allometry). Geometric morphometrics (GMM) is more complicated as an acquisition technique but can offer a more holistic characterization of shape and provides a rigorous toolkit for accounting for allometry. In this study, we used linear discriminant analysis (LDA) to assess the discriminatory performance of four published LMM protocols and a 3D GMM dataset for three clades of antechinus known to differ subtly in shape. We assessed discrimination of raw data (which are frequently used by taxonomists); data with isometry (i.e., overall size) removed; and data after allometric correction (i.e., with nonuniform effects of size removed). When we visualized the principal component analysis (PCA) plots, we found that group discrimination among raw data was high for LMM. However, LMM datasets may inflate PC variance accounted in the first two PCs, relative to GMM. GMM discriminated groups better after isometry and allometry were removed in both PCA and LDA. Although LMM can be a powerful tool to discriminate taxonomic groups, we show that there is substantial risk that this discrimination comes from variation in size, rather than shape. This suggests that taxonomic measurement protocols might benefit from GMM-based pilot studies, because this offers the option of differentiating allometric and nonallometric shape differences between species, which can then inform on the development of the easier-to-apply LMM protocols.

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 generalized 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 a 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.

Skull shape of a widely distributed, endangered marsupial reveals little evidence of local adaptation between fragmented populations.

The biogeographic distribution of diversity among populations of threatened mammalian species is generally investigated using population genetics. However, intraspecific phenotypic diversity is rarely assessed beyond taxonomy-focused linear measurements or qualitative descriptions. Here, we use a technique widely used in the evolutionary sciences-geometric morphometrics-to characterize shape diversity in the skull of an endangered marsupial, the northern quoll, across its 5,000 km distribution range along Northern Australia. Skull shape is a proxy for feeding, behavior, and phenotypic differentiation, allowing us to ask whether populations can be distinguished and whether patterns of variation indicate adaptability to changing environmental conditions. We analyzed skull shape in 101 individuals across four mainland populations and several islands. We assessed the contribution of population, size, sex, rainfall, temperature, and geography to skull shape variation using principal component analysis, Procrustes ANOVA, and variation partitioning analyses. The populations harbor similar amounts of broadly overlapping skull shape variation, with relatively low geographic effects. Size predicted skull shape best, coinciding with braincase size variation and differences in zygomatic arches. Size-adjusted differences in populations explained less variation with far smaller effect sizes, relating to changes in the insertion areas of masticatory muscles, as well as the upper muzzle and incisor region. Climatic and geographic variables contributed little. Strikingly, the vast majority of shape variation-76%-remained unexplained. Our results suggest a uniform intraspecific scope for shape variation, possibly due to allometric constraints or phenotypic plasticity beyond the relatively strong allometric effect. The lack of local adaptation indicates that cross-breeding between populations will not reduce local morphological skull (and probably general musculoskeletal) adaptation because none exists. However, the potential for heritable morphological variation (e.g., specialization to local diets) seems exceedingly limited. We conclude that 3D geometric morphometrics can provide a comprehensive, statistically rigorous phenomic contribution to genetic-based conservation studies.

Skin hydrophobicity as an adaptation for self-cleaning in geckos.

Hydrophobicity is common in plants and animals, typically caused by high relief microtexture functioning to keep the surface clean. Although the occurrence and physical causes of hydrophobicity are well understood, ecological factors promoting its evolution are unclear. Geckos have highly hydrophobic integuments. We predicted that, because the ground is dirty and filled with pathogens, high hydrophobicity should coevolve with terrestrial microhabitat use. Advancing contact-angle (ACA) measurements of water droplets were used to quantify hydrophobicity in 24 species of Australian gecko. We reconstructed the evolution of ACA values, in relation to microhabitat use of geckos. To determine the best set of structural characteristics associated with the evolution of hydrophobicity, we used linear models fitted using phylogenetic generalized least squares (PGLS), and then model averaging based on AICc values. All species were highly hydrophobic (ACA > 132.72°), but terrestrial species had significantly higher ACA values than arboreal ones. The evolution of longer spinules and smaller scales was correlated with high hydrophobicity. These results suggest that hydrophobicity has coevolved with terrestrial microhabitat use in Australian geckos via selection for long spinules and small scales, likely to keep their skin clean and prevent fouling and disease.

Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

Beyond Brownian Motion and the Ornstein-Uhlenbeck Process: Stochastic Diffusion Models for the Evolution of Quantitative Characters.

Gaussian processes, such as Brownian motion and the Ornstein-Uhlenbeck process, have been popular models for the evolution of quantitative traits and are widely used in phylogenetic comparative methods. However, they have drawbacks that limit their utility. Here we describe new, non-Gaussian stochastic differential equation (diffusion) models of quantitative trait evolution. We present general methods for deriving new diffusion models and develop new software for fitting non-Gaussian evolutionary models to trait data. The theory of stochastic processes provides a mathematical framework for understanding the properties of current and future phylogenetic comparative methods. Attention to the mathematical details of models of trait evolution and diversification may help avoid some pitfalls when using stochastic processes to model macroevolution.

Ecological associations among epidermal microstructure and scale characteristics of Australian geckos (Squamata: Carphodactylidae and Diplodactylidae).

A first step in examining factors influencing trait evolution is demonstrating associations between traits and environmental factors. Scale microstructure is a well-studied feature of squamate reptiles (Squamata), including geckos, but few studies examine ecology the of microstructures, and those focus mainly on toe pads. In this study, the ecomorphology of cutaneous microstructures on the dorsum was described for eight Australian species of carphodactylid (Squamata: Carphodactylidae) and 19 diplodactylid (Squamata: Diplodactylidae) geckos. We examined scale dimensions, spinule and cutaneous sensilla (CS) morphology, using scanning electron microscopy, and described associations of these traits with microhabitat selection (arboreal, saxicoline or terrestrial) and relative humidity of each species' habitat (xeric, mesic or humid). We used a phylogenetic flexible discriminant analysis (pFDA) to describe relationships among all traits and then a modeling approach to examine each trait individually. Our analysis showed that terrestrial species tended to have long spinules and CS with more bristles, saxicoline species larger diameter CS and arboreal species tended to have large granule scales and small intergranule scales. There was high overlap in cutaneous microstructural morphology among species from xeric and mesic environments, whereas species from humid environments had large diameter CS and few bristles. Significant associations between epidermal morphology and environmental humidity and habitat suggest that epidermal microstructures have evolved in response to environmental variables. In summary, long spinules, which aid self-cleaning in terrestrial geckos, are consistent with greater exposure to dirt and debris in this habitat. Long spinules were not clearly correlated to environmental humidity. Finally, more complex CS (larger diameter with more bristles) may facilitate better perception of environmental variation in geckos living in drier habitats.