Sound amplification by means of a horn-like roosting structure in Spix's disc-winged bat

While sound is a signal modality widely used by many animals, it is very susceptible to attenuation, hampering effective long-distance communication. A strategy to minimize sound attenuation that has been historically used by humans is to use acoustic horns; to date, no other animal is known to use a similar structure to increase sound intensity. Here, we describe how the use of a roosting structure that resembles an acoustic horn (the tapered tubes that form when new leaves of plants such as Heliconia or Calathea species start to unfurl) increases sound amplification of the incoming and outgoing social calls used by Spix''s disc-winged bat (Thyroptera tricolor) to locate roosts and group members. Our results indicate that incoming calls are significantly amplified as a result of sound waves being increasingly compressed as they move into the narrow end of the leaf. Outgoing calls were faintly amplified, probably as a result of increased sound directionality. Both types of call, however, experienced significant sound distortion, which might explain the patterns of signal recognition previously observed in behavioural experiments. Our study provides the first evidence of the potential role that a roost can play in facilitating acoustic communication in bats.     

Human‐modified habitats change patterns of population genetic structure and group relatedness in Peter's tent‐roosting bats

Although coloniality is widespread among mammals, it is still not clear what factors influence composition of social groups. As animals need to adapt to multiple habitat and environmental conditions throughout their range, variation in group composition should be influenced by adaptive adjustment to different ecological factors. Relevant to anthropogenic disturbance, increased habitat modification by humans can alter species’ presence, density, and population structure. Therefore, it is important to understand the consequences of changes to landscape composition, in particular how habitat modification affects social structure of group‐forming organisms. Here, we combine information on roosting associations with genetic structure of Peter's tent‐roosting bats, Uroderma bilobatum to address how different habitat characteristics at different scales affect structure of social groups. By dividing analyses by age and sex, we determined that genetic structure was greater for adult females than adult males or offspring. Habitat variables explained 80% of the variation in group relatedness (mainly influenced by female relatedness) with roost characteristics contributing the most explained variation. This suggests that females using roosts of specific characteristics exhibit higher relatedness and seem to be philopatric. These females mate with more males than do more labile female groups. Results describe ecological and microevolutionary processes, which affect relatedness and social structure; findings are highly relevant to species distributions in both natural and human‐modified environments.     

Can mite parasitism affect the condition of bat hosts? Implications for the social structure of colonial bats

Ectoparasitism may be recognized as one of the main costs of coloniality, but little is known about how it affects the fitness and social structure of bats, the most gregarious of mammals. We studied these issues using the colonial bat Miniopterus schreibersii and its haematophagous parasitic mite Spinturnix psi as a model. Body condition is an important indicator of individual fitness that is potentially affected by ectoparasitism. Thus, we measured host body condition and mite loads in a total of 969 bats throughout the annual cycle. Mites were rare while hosts hibernated, increased in abundance in spring and peaked during nursing season of bats, when they were particularly abundant on lactating females and young bats. This strong seasonal variation in mite loads is related to the reproductive cycle of mites, which in turn appears to be synchronized with the reproductive cycle of their hosts. Mite loads and the condition of bats were negatively correlated, and information available suggests that this may be due to an effect of parasitism, although other possible causes for this trend cannot be excluded. However, a negative correlation was only observed during the bat's nursing season, when mites were most abundant, and heavily parasitized bats lost about 10% of their weight. Mite parasitism did not seem to be a significant disadvantage of coloniality, except in nurseries, where it might impose some costs. However, as females and young usually aggregate in these colonies, we presume that for them such costs are probably offset by advantages of group living. Adult males, however, are usually absent from nurseries, which may be a strategy to minimize mite parasitism. Overall, the results suggest that ectoparasitism may play a role in determining the social structure of M. schreibersii and of many other temperate bats that have similar life cycles and ectoparasitic loads.     

Contrasted patterns of mitochondrial and nuclear structure among nursery colonies of the bat Myotis myotis

Thirteen nursery colonies of Myotis myotis were sampled in central Europe to investigate the dispersal behaviour of this bat species. Mitochondrial DNA sequences of 260 bats reveal the occurrence of three evolutionary lineages that have probably originated in distinct glacial refugia and meet in a contact zone near the Alps. Moreover, the strong haplotypic segregation (Φ_ST=0.540) suggests that breeding females are philopatric. Contrastingly, the low population structure at 15 microsatellite loci (F_ST=0.022), suggests the homogenizing effect of nuclear gene flow. The different perspectives given by these two markers are consistent with strong male‐biased dispersal. As a result of female philopatry, the local haplotypic variability seems to be largely influenced by historical processes of colonization. Conversely, the homogeneity of nuclear variability within roosts that are located north of the Alps seems to mainly reflect contemporary gene flow. Finally, despite the fact that females are faithful to their natal colony, movements of both males and females occur outside the breeding period. Mitochondrial survey of individuals sampled exclusively in nurseries may thus poorly reflect the metapopulation dynamics of this species.     

Tent selection, roosting ecology and social organization of the tent-making bat, Ectophylla alba, in Costa Rica

Small groups of the tent-making bat, Ectophylla alba , were found roosting in Heliconia (Musaceae) tents in old secondary-growth forest in north-eastern Costa Rica. The choice of specific Heliconia leaves for tents was predicted on the basis of leaf size and age. Additionally, tents in shrubs, saplings and epiphytic plants were found scattered throughout both primary- and secondary-growth forest. Tents were used either as night feeding roosts or as day-roosts for as long as 45 days. Groups of bats remained together when they moved to newly cut tents. After parturition, tent groups divided into all-male colonies and maternity colonies with females, non-volant young and a single adult male.     

Island biogeography of bats in Baja California, Mexico: patterns of bat species richness in a near-shore archipelago

Aim We studied the relationship between the size and isolation of islands and bat species richness in a near‐shore archipelago to determine whether communities of vagile mammals conform to predictions of island biogeography theory. We compared patterns of species richness in two subarchipelagos to determine whether area per se or differences in habitat diversity explain variations in bat species richness. Location Islands in the Gulf of California and adjacent coastal habitats on the Baja California peninsula in northwest Mexico. Methods Presence–absence surveys for bats were conducted on 32 islands in the Gulf of California using acoustic and mist‐net surveys. We sampled for bats in coastal habitats of four regions of the Baja peninsula to characterize the source pool of potential colonizing species. We fitted a semi‐log model of species richness and multiple linear regression and used Akaike information criterion model selection to assess the possible influence of log₁₀ area, isolation, and island group (two subarchipelagos) on the species richness of bats. We compared the species richness of bats on islands with greater vegetation densities in the southern gulf (n = 20) with that on drier islands with less vegetation in the northern gulf (n = 12) to investigate the relationship between habitat diversity and the species richness of bats. Results Twelve species of bats were detected on islands in the Gulf of California, and 15 species were detected in coastal habitats on the Baja peninsula. Bat species richness was related to both area and isolation of islands, and was higher in the southern subarchipelago, which has denser vegetation. Log₁₀ area was positively related to bat species richness, which increased by one species for every 5.4‐fold increase in island area. On average, richness declined by one species per 6.25 km increase in isolation from the Baja peninsula. Main conclusions Our results demonstrate that patterns of bat species richness in a near‐shore archipelago are consistent with patterns predicted by the equilibrium theory of island biogeography. Despite their vagility, bats may be more sensitive to moderate levels of isolation than previously expected in near‐shore archipelagos. Differences in vegetation and habitat xericity appear to be associated with richness of bat communities in this desert ecosystem. Although observed patterns of species richness were consistent with those predicted by the equilibrium theory, similar relationships between species richness and size and isolation of islands may arise from patch‐use decision making by individuals (optimal foraging strategies).     

Migration and dispersal patterns of bats and their influence on genetic structure

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A tale of two genomes: contrasting patterns of phylogeographic structure in a widely distributed bat

One of the most widely distributed bats in the New World, the big brown bat (Eptesicus fuscus) exhibits well-documented geographic variation in morphology and life history traits, suggesting the potential for significant phylogeographic structure as well as adaptive differentiation among populations. In a pattern broadly consistent with morphologically defined subspecies, we found deeply divergent mitochondrial lineages restricted to different geographic regions. In contrast, sequence data from two nuclear loci suggest a general lack of regional genetic structure except for peripheral populations in the Caribbean and Mexico/South America. Coalescent analyses suggest that the striking difference in population structure between genomes cannot be attributed solely to different rates of lineage sorting, but is likely due to male-mediated gene flow homogenizing nuclear genetic diversity across most of the continental range. Despite this ongoing gene flow, selection has apparently been effective in producing and maintaining adaptive differentiation among populations, while strong female site fidelity, maintained over the course of millions of years, has produced remarkably deep divergence among geographically isolated matrilines. Our results highlight the importance of evaluating multiple genetic markers for a more complete understanding of population structure and history.     

The three-dimensional structure and X-ray sequence reveal that trichomaglin is a novel S-like ribonuclease

Trichomaglin is a protein isolated from root tuber of the plant Maganlin (Trichosanthes Lepiniate, Cucurbitaceae). The crystal structure of trichomaglin has been determined by multiple-isomorphous replacement and refined at 2.2 A resolution. The X-ray sequence was established, based on electron density combined with the experimentally determined N-terminal sequence, and the sequence information derived from mass spectroscopic analysis. X-ray sequence-based homolog search and the three-dimensional structure reveal that trichomaglin is a novel S-like RNase, which was confirmed by biological assay. Trichomaglin molecule contains an additional beta sheet in the HV(b) region, compared with the known plant RNase structures. Fourteen cystein residues form seven disulfide bridges, more than those in the other known structures of S- and S-like RNases. His43 and His105 are expected to be the catalytic acid and base, respectively. Four hydrosulfate ions are bound in the active site pocket, three of them mimicking the substrate binding sites.     

A multiple peak adaptive landscape based on feeding strategies and roosting ecology shaped the evolution of cranial covariance structure and morphological differentiation in phyllostomid bats

We explored the evolution of morphological integration in the most noteworthy example of adaptive radiation in mammals, the New World leaf‐nosed bats, using a massive dataset and by combining phylogenetic comparative methods and quantitative genetic approaches. We demonstrated that the phenotypic covariance structure remained conserved on a broader phylogenetic scale but also showed a substantial divergence between interclade comparisons. Most of the phylogenetic structure in the integration space can be explained by splits at the beginning of the diversification of major clades. Our results provide evidence for a multiple peak adaptive landscape in the evolution of cranial covariance structure and morphological differentiation, based upon diet and roosting ecology. In this scenario, the successful radiation of phyllostomid bats was triggered by the diversification of dietary and roosting strategies, and the invasion of these new adaptive zones lead to changes in phenotypic covariance structure and average morphology. Our results suggest that intense natural selection preceded the invasion of these new adaptive zones and played a fundamental role in shaping cranial covariance structure and morphological differentiation in this hyperdiverse clade of mammals. Finally, our study demonstrates the power of combining comparative methods and quantitative genetic approaches when investigating the evolution of complex morphologies.     

Population genetic structure of serotine bats (Eptesicus serotinus) across Europe and implications for the potential spread of bat rabies (European bat lyssavirus EBLV-1)

Understanding of the movements of species at multiple scales is essential to appreciate patterns of population connectivity and in some cases, the potential for pathogen transmission. The serotine bat (Eptesicus serotinus) is a common and widely distributed species in Europe where it frequently harbours European bat lyssavirus type 1 (EBLV-1), a virus causing rabies and transmissible to humans. In the United Kingdom, it is rare, with a distribution restricted to south of the country and so far the virus has never been found there. We investigated the genetic structure and gene flow of E. serotinus across the England and continental Europe. Greater genetic structuring was found in England compared with continental Europe. Nuclear data suggest a single population on the continent, although further work with more intensive sampling is required to confirm this, while mitochondrial sequences indicate an east–west substructure. In contrast, three distinct populations were found in England using microsatellite markers, and mitochondrial diversity was very low. Evidence of nuclear admixture indicated strong male-mediated gene flow among populations. Differences in connectivity could contribute to the high viral prevalence on the continent in contrast with the United Kingdom. Although the English Channel was previously thought to restrict gene flow, our data indicate relatively frequent movement from the continent to England highlighting the potential for movement of EBLV-1 into the United Kingdom.     

Cytoplasmic and nuclear markers reveal contrasting patterns of spatial genetic structure in a natural Ipomopsis hybrid zone

Spatial variation in natural selection may play an important role in determining the genetic structure of hybridizing populations. Previous studies have found that F1 hybrids between naturally hybridizing Ipomopsis aggregata and Ipomopsis tenuituba in central Colorado differ in fitness depending on both genotype and environment: hybrids had higher survival when I. aggregata was the maternal parent, except in the centre of the hybrid zone where both hybrid types had high survival. Here, we developed both maternally (cpDNA PCR-RFLP) and biparentally inherited (nuclear AFLP) species-diagnostic markers to characterize the spatial genetic structure of the natural Ipomopsis hybrid zone, and tested the prediction that the majority of natural hybrids have I. aggregata cytoplasm, except in areas near the centre of the hybrid zone. Analyses of 352 individuals from across the hybrid zone indicate that cytoplasmic gene flow is bidirectional, but contrary to expectation, most plants in the hybrid zone have I. tenuituba cytoplasm. This cytotype distribution is consistent with a hybrid zone in historical transition, with I. aggregata nuclear genes advancing into the contact zone. Further, nuclear data show a much more gradual cline than cpDNA markers that is consistent with morphological patterns across the hybrid populations. A mixture of environment- and pollinator-mediated selection may contribute to the current genetic structure of this hybrid system.     

Acoustic characterization of bats from Malta: setting a baseline for monitoring and conservation of bat populations

Bioacoustic research has made several advancements in developing systems to record extensive acoustic data and classify bat echolocation calls to species level using automated classifiers. These systems are useful as echolocation calls give valuable information on bat behaviour and ecology and hence are widely used for research and conservation of bat populations. Despite the challenges associated with automated classifiers, due to the interspecific differences in call characteristics of bat species found in the Maltese Islands, the use of a quantitative and automated approach is investigated. The sound analysis pipeline involved the use of an algorithm to clean sound files from background noise and measure temporal and spectral parameters of bat echolocation calls. These parameters were then fed to a trained and validated artificial neural network using a bat call library built from reference bat calls from Malta. The automatic classifier achieved an overall correct classification rate of 98%. This high correct classification rate for reliable species identification may have benefitted from the absence of typically problematic species, such as species in the genus Myotis, in the analyses. This study’s results pave the way for efficient and reliable bat acoustic surveys in Malta in aid of necessary monitoring and conservation by providing an updated bat species list and their echolocation characteristics.     

The context of social learning: association patterns in a captive flock of brown-headed cowbirds

Much work on social learning has involved behaviour transmission between pairs of individuals, but recently the need to examine the social context in which learning occurs has been recognized. Previous studies using small numbers of animals have shown social influence on the behavioural development of juvenile male brown-headed cowbirds, Molothrus ater. Here we looked at the larger social context that forms the framework for such influence in more natural settings. We allowed a captive group of over 70 cowbirds, comprising adult and juvenile males and females, to associate freely in a large complex of connected aviaries. Highly organized social assortment emerged in the group, with individuals associating with others based on similarity in age and sex. Juvenile males that associated more with adult males had higher courtship success. Juvenile males that associated more with females sang less over the year. These results indicate that the social context of social learning for juvenile males is not just random association with all other birds in the social group, but is a selective and structured pattern of interaction. Differences in navigating this social structure correlated with courtship success and vocalization, behaviour known to be affected by social learning. Studies such as this, using large groups with free assortment of individuals, are the first step towards understanding the effects of the larger social context surrounding social learning.     

Global patterns reveal strong population structure in Haemonchus contortus, a nematode parasite of domesticated ruminants

We have examined the global population genetic structure of Haemonchus contortus. The genetic variability was studied using both amplified fragment length polymorphism (AFLP) and nad4 sequences of the mitochondrial genome. To examine the performance and information content of the two different marker systems, comparative assessment of population genetic diversity was undertaken in 19 isolates of H. contortus, a parasitic nematode of small ruminants. A total of 150 individual adult worms representing 14 countries from all inhabited continents were analysed. Altogether 1,429 informative AFLP markers were generated using four different primer combinations. Also, the genetic variation was high, which agrees with results from previous AFLP studies of nematode parasites of livestock. The genetic structure was high, indicating limited gene flow between the different isolates and populations from each continent mostly formed monophyletic groups in the phylogenetic analysis. However, for isolates representing Australia, Greece and one laboratory strain that originated from South Africa (WRS), there was no clear genetic relationship between the isolates and the distance between their geographical origins. Basically the same pattern was observed for the mitochondrial marker, although the phylogenetic analysis was less resolved than for AFLP. In contrast with previous findings on the population genetic structure of H. contortus, the calculation of population structure gave high values (Nst=0.59). The strong structure was present also for the four Swedish isolates (Nst=0.16) representing a small geographical area.