article-journal

Captivity alters behaviour but not seasonal brain size change in semi-naturally housed shrews
Captivity, frequently used in animal research, can profoundly alter brain size, cognitive abilities and activity levels. Critically, persistent exposure to stressors in captive environments can lead to chronic stress and subsequently to a range of health issues. However, the direct implications of captivity on research outcomes have not been thoroughly investigated. We examined the effects of captivity on the common shrew, Sorex araneus, a species that exhibits a profound seasonal reversible change in brain and body size. We compared wild shrews during summer and winter to assess seasonal changes in brain size and behaviour and then contrasted these findings with shrews kept in captivity for six months. Using repeated in vivo magnitic resonance imaging, we determined that the extent of seasonal brain size change was not affected by the semi-natural captive conditions. However, captivity led to increased activity levels and reduced learning motivation in the shrews, indicative of chronic stress. These results suggest that even semi-natural conditions can significantly alter the outcome of studies and these effects need to be quantified before experimentation.
Bat genomes illuminate adaptations to viral tolerance and disease resistance
Zoonoses are infectious diseases transmitted from animals to humans. Compared to other mammalian orders, bats are suggested to harbor more zoonotic viruses(Olival et al. 2017). Infections in bats are largely asymptomatic(Schlottau et al. 2020; Guito et al. 2021), suggesting limited tissue-damaging inflammation and immunopathology. To investigate the genomic basis of disease resistance, the Bat1K project generated reference-quality genomes of ten bat species, including potential viral reservoirs. A systematic analysis covering 115 mammalian genomes revealed that signatures of selection in immune genes are more prevalent in bats compared with other mammalian orders. We found an excess of immune gene adaptations in the ancestral chiropteran branch and in many descending bat lineages, highlighting viral entry and detection factors, and regulators of antiviral and inflammatory responses. ISG15, an antiviral gene contributing to hyperinflammation during COVID-19(Perng and Lenschow 2018; Munnur et al. 2021), exhibits key residue changes in rhinolophid and hipposiderid bats. Cellular infection experiments show species-specific antiviral differences and an essential role offor protein conjugation in antiviral function of bat ISG15, separate from its role in secretion and inflammation in humans. Furthermore, in contrast to human ISG15, ISG15 of most rhinolophid and hipposiderid bats has strong anti-SARS-CoV-2 activity. Our work reveals molecular mechanisms contributing to viral tolerance and disease resistance in bats.
Frugivore traits predict plant-frugivore interactions using generalized joint attribute modeling
Under an adaptive hypothesis, the reciprocal influence between mutualistic plants and frugivores is expected to result in dispersal syndromes comprising both frugivore and plant traits that structure fruit consumption. How frugivore traits and within-species variation contribute to structuring dispersal syndromes is, however, often ignored. To address both gaps, we analyze traits for the mutualistic ecological network comprising Carollia bats that feed on and disperse Piper seeds. We used generalized joint attribute modeling (GJAM), a Bayesian modeling approach that simultaneously accounts for multiple sources of variance across trait types. In support of the adaptive hypothesis and indicating niche partitioning among Carollia bats, we find differential consumption of a suite of Piper species influenced by bat traits such as body size; however, Piper morphological traits had no effect on bat consumption. Slow evolutionary rates, dispersal by other vertebrates, and unexamined fruit traits, such as Piper chemical bouquets, may explain the lack of association between bat Piper consumption and fruit morphological traits. We have identified a potential asymmetric influence of frugivore traits on plant-frugivore interactions, providing a template for future trait analyses of plant-animal networks. As intraspecific trait variation is rarely included in studies on trait matching, this paper contributes to closing that important knowledge gap.
Gene expression comparisons between captive and wild shrew brains reveal captivity effects
Compared with their free-ranging counterparts, wild animals in captivity experience different conditions with lasting physiological and behavioural effects. Although shifts in gene expression are expected to occur upstream of these phenotypes, we found no previous gene expression comparisons of captive versus free-ranging mammals. We assessed gene expression profiles of three brain regions (cortex, olfactory bulb and hippocampus) of wild shrews (Sorex araneus) compared with shrews kept in captivity for two months and undertook sample dropout to examine robustness given limited sample sizes. Consistent with captivity effects, we found hundreds of differentially expressed genes in all three brain regions, 104 overlapping across all three, that enriched pathways associated with neurodegenerative disease, oxidative phosphorylation and genes encoding ribosomal proteins. In the shrew, transcriptomic changes detected under captivity resemble responses in several human pathologies, including major depressive disorder and neurodegeneration. While interpretations of individual genes are tempered by small sample sizes, we propose captivity influences brain gene expression and function and can confound analyses of natural processes in wild individuals under captive conditions.
Newly assembled pocket gopher genomes can facilitate conservation management of biodiversity
Texas exhibits one of the richest levels of pocket gopher diversity in the United States. Three genera (Cratogeomys, Geomys, and Thomomys) and 11 species are found in Texas. It is not surprising given the diversity of the Texas landscape (ecoregions, life zones, substrates, and vegetation) that these species are further subdivided into 29 subspecies in Texas alone. Pocket gopher distributions are determined by availability of suitable soil types and therefore often occur in small, isolated populations. For some taxa, limited distribution and ultimately small deme sizes result in populations that may require attention from a regulatory and management perspective. For many Texas pocket gopher subspecies, insufficient information exists to make sound recommendations relative to conservation status and needs despite decades of research collecting and evaluating data based on morphometrics, distributions and habitat preferences, karyotypes, allozymes, and mitochondrial DNA. As such, there is precedent for elevating pocket gopher subspecies to species after evaluation of available data, as well as subsuming subspecies into a broader taxonomic group. We used genomic techniques to identify genetically defined operational taxonomic units (OTUs) of pocket gophers to improve knowledge and understanding of pocket gopher distributions within the state. Using tens of thousands of single nucleotide polymorphisms, we determined the number of OTUs in each genus to be 5 for Thomomys bottae subspecies, 8 for Geomys species, and 5 for Cratogeomys castanops subspecies in Texas. In general, these data agree with current taxonomic hypotheses regarding Geomys and C. castanops; however, many T. bottae groups present similar genetic patterns that do not merit subspecies status based on these data, suggesting a more conservative classification of T. bottae in Texas and southeastern New Mexico that could facilitate conservation efforts, should they be necessary.
Seasonal and comparative evidence of adaptive gene expression in mammalian brain size plasticity
Contrasting almost all other mammalian wintering strategies, Eurasian common shrews, Sorex araneus, endure winter by shrinking their brain, skull, and most organs, only to then regrow to breeding size the following spring. How such tiny mammals achieve this unique brain size plasticity while maintaining activity through the winter remains unknown. To discover potential adaptations underlying this trait, we analyzed seasonal differential gene expression in the shrew hypothalamus, a brain region that both regulates metabolic homeostasis and drastically changes size, and compared hypothalamus gene expression across species. We discovered seasonal variation in suites of genes involved in energy homeostasis and apoptosis, shrew-specific upregulation of genes involved in the development of the hypothalamic blood-brain barrier and calcium signaling, as well as overlapping seasonal and comparative gene expression divergence in genes implicated in the development and progression of human neurological and metabolic disorders, including CCDC22. With high metabolic rates and facing harsh winter conditions, S. araneus have evolved both adaptive and plastic mechanisms to sense and regulate their energy budget. Many of these changes mirrored those identified in human neurological and metabolic disease, highlighting the interactions between metabolic homeostasis, brain size plasticity, and longevity.
Discovery and biological confirmation of a highly divergent Tacaribe virus in metatranscriptomic data from neotropical bats
First isolated from neotropical fruit bats in Trinidad in 1956, Tacaribe virus (TCRV) has rarely been detected since. We searched for New World arenavirus reads in roughly 5.7 million sequencing runs available on public databases using Serratus. We recovered a complete genome of a divergent TCRV in metatranscriptomic data derived from heart and eye tissue of an adult male Jamaican fruit-eating bat sampled in the Dominican Republic, 2014. In total, 2,733 reads were mapped resulting in mean coverages of 7.4-fold for the L and 10.2-fold for the S segment. Re-testing original bat specimens showed the highest viral loads in liver tissue (245 copies/mg). Sanger sequencing of PCR amplicons from liver confirmed correctness of and completed the genome recovered from metatranscriptomic data, revealing conserved arenavirus genomic organization, length, intergenic regions, and genome termini. The newly found TCRV strain tentatively named DOM2014 clustered in a basal sister relationship to all other known TCRV strains with which it shared between 83.3%–86.0% genomic and 91.8%–93.7% translated amino acid sequence identity across protein-coding regions. DOM2014 showed a conserved glycine, proline, proline, threonine (GPPT) nucleopro­ tein motif, which is essential for TCRV interferon β antagonism. Our data confirm the association of TCRV with the bat genus Artibeus put into question by lethal experi­ mental infections and scarce bat-derived TCRV genomic data. Broad genetic diversity and geographic spread require assessments of TCRV strain-associated pathogenicity, particularly for DOM2014 as a highly divergent TCRV strain. Confirmation of genomic database findings by testing original specimens provides robustness to our findings and supports the usefulness of metatranscriptomic studies.
Neotropics as a Cradle for Adaptive Radiations
Neotropical ecosystems are renowned for numerous examples of adaptive radiation in both plants and animals resulting in high levels of biodiversity and endemism. However, we still lack a comprehensive review of the abiotic and biotic factors that contribute to these adaptive radiations. To fill this gap, we delve into the geological history of the region, including the role of tectonic events such as the Andean uplift, the formation of the Isthmus of Panama, and the emergence of the Guiana and Brazilian Shields. We also explore the role of ecological opportunities created by the emergence of new habitats, as well as the role of key innovations, such as novel feeding strategies or reproductive mechanisms. We discuss different examples of adaptive radiation, including classic ones like Darwin’s finches and Anolis lizards, and more recent ones like bromeliads and lupines. Finally, we propose new examples of adaptive radiations mediated by ecological interactions in their geological context. By doing so, we provide insights into the complex interplay of factors that contributed to the remarkable diversity of life in the Neotropics and highlight the importance of this region in understanding the origins of biodiversity.
Cochlea development shapes bat sensory system evolution
Sensory organs must develop alongside the skull within which they are largely encased, and this relationship can manifest as the skull constraining the organs, organs constraining the skull, or organs constraining one another in relative size. How this interplay between sensory organs and the developing skull plays out during the evolution of sensory diversity; however, remains unknown. Here, we examine the developmental sequence of the cochlea, the organ responsible for hearing and echolocation, in species with distinct diet and echolocation types within the ecologically diverse bat super-family Nocti- lionoidea. We found the size and shape of the cochlea largely correlates with skull size, with exceptions of Pteronotus parnellii, whose high duty cycle echo- location (nearly constant emission of sound pulses during their echolocation process allowing for detailed information gathering, also called constant fre- quency echolocation) corresponds to a larger cochlear and basal turn, and Monophyllus redmani, a small-bodied nectarivorous bat, for which interactions with other sensory organs restrict cochlea size. Our findings support the exis- tence of developmental constraints, suggesting that both developmental and anatomical factors may act synergistically during the development of sensory systems in noctilionoid bats.