Bats possess extraordinary adaptations, including flight, echolocation, extreme longevity and unique immunity. High-quality genomes are crucial for understanding the molecular basis and evolution of these traits. Here we incorporated long-read sequencing and state-of-the-art scaffolding protocols 1 to generate, to our knowledge, the first reference-quality genomes of six bat species (Rhinolophus ferrumequinum, Rousettus aegyptiacus, Phyllostomus discolor, Myotis myotis, Pipistrellus kuhlii and Molossus molossus). We integrated gene projections from our 'Tool to infer Orthologs from Genome Alignments' (TOGA) software with de novo and homology gene predictions as well as short-and long-read transcriptomics to generate highly complete gene annotations. To resolve the phylogenetic position of bats within Laurasiatheria, we applied several phylogenetic methods to comprehensive sets of orthologous protein-coding and noncoding regions of the genome, and identified a basal origin for bats within Scrotifera. Our genome-wide screens revealed positive selection on hearing-related genes in the ancestral branch of bats, which is indicative of laryngeal echolocation being an ancestral trait in this clade. We found selection and loss of immunity-related genes (including pro-inflammatory NF-κB regulators) and expansions of anti-viral APOBEC3 genes, which highlights molecular mechanisms that may contribute to the exceptional immunity of bats. Genomic integrations of diverse viruses provide a genomic record of historical tolerance to viral infection in bats. Finally, we found and experimentally validated bat-specific variation in microRNAs, which may regulate bat-specific gene-expression programs. Our reference-quality bat genomes provide the resources required to uncover and validate the genomic basis of adaptations of bats, and stimulate new avenues of research that are directly relevant to human health and disease 1. With more than 1,400 species identified to date 2 , bats (Chiroptera) account for about 20% of all extant mammal species. Bats are found around the world and successfully occupy diverse ecological niches 1. Their global success is attributed to an extraordinary suite of adaptations 1 including powered flight, laryngeal echolocation, vocal learning, exceptional longevity and a unique immune system that probably enables bats to better tolerate viruses that are lethal to other mammals (such as severe acute respiratory syndrome-related coronavirus, Middle East respiratory syndrome-related coronavirus and Ebola virus) 3. Bats therefore represent important model systems for the study of
Group foraging has been suggested as an important factor for the evolution of sociality. However, visual cues are predominantly used to gain information about group members' foraging success in diurnally foraging animals such as birds, where group foraging has been studied most intensively. By contrast, nocturnal animals, such as bats, would have to rely on other cues or signals to coordinate foraging. We investigated the role of echolocation calls as inadvertently produced cues for social foraging in the insectivorous bat Noctilio albiventris. Females of this species live in small groups, forage over water bodies for swarming insects and have an extremely short daily activity period. We predicted and confirmed that (i) free-ranging bats are attracted by playbacks of echolocation calls produced during prey capture, and that (ii) bats of the same social unit forage together to benefit from passive information transfer via the change in group members' echolocation calls upon finding prey. Network analysis of high-resolution automated radio telemetry confirmed that group members flew within the predicted maximum hearing distance 94G6 per cent of the time. Thus, echolocation calls also serve as intraspecific communication cues. Sociality appears to allow for more effective group foraging strategies via eavesdropping on acoustical cues of group members in nocturnal mammals.
Many serious emerging zoonotic infections have recently arisen from bats, including Ebola, Marburg, SARS-coronavirus, Hendra, Nipah, and a number of rabies and rabies-related viruses, consistent with the overall observation that wildlife are an important source of emerging zoonoses for the human population. Mechanisms underlying the recognized association between ecosystem health and human health remain poorly understood and responding appropriately to the ecological, social and economic conditions that facilitate disease emergence and transmission represents a substantial societal challenge. In the context of disease emergence from wildlife, wildlife and habitat should be conserved, which in turn will preserve vital ecosystem structure and function, which has broader implications for human wellbeing and environmental sustainability, while simultaneously minimizing the spillover of pathogens from wild animals into human beings. In this review, we propose a novel framework for the holistic and interdisciplinary investigation of zoonotic disease emergence and its drivers, using the spillover of bat pathogens as a case study. This study has been developed to gain a detailed interdisciplinary understanding, and it combines cutting-edge perspectives from both natural and social sciences, linked to policy impacts on public health, land use and conservation.
Variation in relative brain size is commonly interpreted as the result of selection on neuronal capacity. However, this approach ignores that relative brain size is also linked to another highly adaptive variable: body size. Considering that one-way tradeoff mechanisms are unlikely to provide satisfactory evolutionary explanations, we introduce an analytical framework that describes and quantifies all possible evolutionary scenarios between two traits. To investigate the effects of body mass changes on the interpretation of relative brain size evolution, we analyze three mammalian orders that are expected to be subject to different selective pressures on body size due to differences in locomotor adaptation: bats (powered flight), primates (primarily arboreal), and carnivorans (primarily terrestrial). We quantify rates of brain and body mass changes along individual branches of phylogenetic trees using an adaptive peak model of evolution. We find that the magnitude and variance of the level of integration of brain and body mass rates, and the subsequent relative influence of either brain or body size evolution on the brainbody relationship, differ significantly between orders and subgroups within orders. Importantly, we find that variation in brain-body relationships was driven primarily by variability in body mass. Our approach allows a more detailed interpretation of correlated trait evolution and variation in the underlying evolutionary pathways. Results demonstrate that a principal focus on interpreting relative brain size evolution as selection on neuronal capacity confounds the effects of body mass changes, thereby hiding important aspects that may contribute to explaining animal diversity.L arge brains and advanced cognitive abilities distinguish modern humans from other species, including our closest primate relatives. Consequently, brain size evolution has attracted the attention of generations of scientists (1). However, the human brain is not the largest in absolute mass or volume, but only under consideration of our rather moderate body mass (2-4). Increased "intelligence" is generally attributed to a deviation from a taxonspecific allometric relationship between brain and body (1, 5-7) (Fig. 1). The main interest of studies in the past has thus been to understand which selective forces led to an increase in brain size relative to body size (8)(9)(10)(11)(12)(13)(14).Although the relationship between encephalization and intelligence is intuitive, it is not void of contention (5,6,15). Recent research on measures of "general intelligence" in primates has, for example, found more robust correlations with total brain mass than with encephalization (15). The complex relationship between brain mass, body mass, and intelligence has thus been the subject of considerable debate (5, 6, 16), partly because allometric slopes are taxon-specific (17-19). Regardless of these issues, deviations from the general allometric brain-body relationship continue to be commonly interpreted as a result of ecological, behavior...
Animals are exposed to many conflicting ecological pressures, and the effect of one may often obscure that of another. A likely example of this is the so-called ''lunar phobia'' or reduced activity of bats during full moon. The main reason for lunar phobia was thought to be that bats adjust their activity to avoid predators. However, bats can be prey, but many are carnivorous and therefore predators themselves. Thus, they are likely to be influenced by prey availability as well as predation risk. We investigated the activity patterns of the perchhunting Lophostoma silvicolum and one of its main types of prey, katydids, to assess the influence of the former during different phases of the lunar cycle on a gleaning insectivorous bat. To avoid sampling bias, we used sound recordings and two different capture methods for the katydids, as well as video monitoring and radiotelemetry for the bats. Both, bats and katydids were significantly more active during the dark periods associated with new moon compared to bright periods around the full moon. We conclude that foraging activity of L. silvicolum is probably influenced by prey availability to a large extent and argue that generally the causes of lunar phobia are species-specific.
Bats are the only flying mammals and have well developed navigation abilities for 3D-space. Even bats with comparatively small home ranges cover much larger territories than rodents, and long-distance migration by some species is unique among small mammals. Adult proliferation of neurons, i.e., adult neurogenesis, in the dentate gyrus of rodents is thought to play an important role in spatial memory and learning, as indicated by lesion studies and recordings of neurons active during spatial behavior. Assuming a role of adult neurogenesis in hippocampal function, one might expect high levels of adult neurogenesis in bats, particularly among fruit- and nectar-eating bats in need of excellent spatial working memory. The dentate gyrus of 12 tropical bat species was examined immunohistochemically, using multiple antibodies against proteins specific for proliferating cells (Ki-67, MCM2), and migrating and differentiating neurons (Doublecortin, NeuroD). Our data show a complete lack of hippocampal neurogenesis in nine of the species (Glossophaga soricina, Carollia perspicillata, Phyllostomus discolor, Nycteris macrotis, Nycteris thebaica, Hipposideros cyclops, Neoromicia rendalli, Pipistrellus guineensis, and Scotophilus leucogaster), while it was present at low levels in three species (Chaerephon pumila, Mops condylurus and Hipposideros caffer). Although not all antigens were recognized in all species, proliferation activity in the subventricular zone and rostral migratory stream was found in all species, confirming the appropriateness of our methods for detecting neurogenesis. The small variation of adult hippocampal neurogenesis within our sample of bats showed no indication of a correlation with phylogenetic relationship, foraging strategy, type of hunting habitat or diet. Our data indicate that the widely accepted notion of adult neurogenesis supporting spatial abilities needs to be considered carefully. Given their astonishing longevity, certain bat species may be useful subjects to compare adult neurogenesis with other long-living species, such as monkeys and humans, showing low rates of adult hippocampal neurogenesis.
Summary1. Radiotelemetry and satellite-based telemetry approaches are essential to describe the behaviour and biology of animals. This is especially true for bats, whose small size and cryptic lifestyles make them challenging to study. However, only a handful of studies have evaluated how transmitter mass and the attachment method affect bat behaviour or health, and none have assessed the development of technical methods in the field. 2. We review the past 50 years of bat tracking studies to determine how devices have been attached, how guidelines have been followed or changed, and whether any health or fitness impacts from these transmitters can be determined. 3. Half of the nearly 300 studies available used devices heavier than the recommended 5% of body mass with minimal justification. Devices were typically glued directly to the backs of small bats and remained attached for 9 days. This is far shorter than battery life span of most devices. Little information is available regarding the overall impact of attaching transmitters on the health, survival and reproductive success of bats, and there has been little development in attachment methods since the first tracking studies. 4. We consequently developed a collar for small bats with a degradable weak link and tested it on several species. The collar worked successfully on three of four species. This allows longer habituation and tracking times while ensuring that the device drops off after the battery expires. 5. Future studies will need to invest more effort in assessing potential long-term effects of tracking. They also need to build upon previous knowledge to find the best attachment method, size and shape for their study species to effectively improve wildlife tracking.
Vertebrate brains are organized in modules which process information from sensory inputs selectively. Therefore they are probably under different evolutionary pressures. We investigated the impact of environmental influences on specific brain centres in bats. We showed in a phylogenetically independent contrast analysis that the wing area of a species corrected for body size correlated with estimates of habitat complexity. We subsequently compared wing area, as an indirect measure of habitat complexity, with the size of regions associated with hearing, olfaction and spatial memory, while controlling for phylogeny and body mass. The inferior colliculi, the largest sub-cortical auditory centre, showed a strong positive correlation with wing area in echolocating bats. The size of the main olfactory bulb did not increase with wing area, suggesting that the need for olfaction may not increase during the localization of food and orientation in denser habitat. As expected, a larger wing area was linked to a larger hippocampus in all bats. Our results suggest that morphological adaptations related to flight and neuronal capabilities as reflected by the sizes of brain regions coevolved under similar ecological pressures. Thus, habitat complexity presumably influenced and shaped sensory abilities in this mammalian order independently of each other.
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