Genome-wide data reveal cryptic diversity and genetic introgression in an Oriental cynopterine fruit bat radiation.

BACKGROUND: The Oriental fruit bat genus Cynopterus, with several geographically overlapping species, presents an interesting case study to evaluate the evolutionary significance of coexistence versus isolation. We examined the morphological and genetic variability of congeneric fruit bats Cynopterus sphinx and C. brachyotis using 405 samples from two natural contact zones and 17 allopatric locations in the Indian subcontinent; and investigated the population differentiation patterns, evolutionary history, and the possibility of cryptic diversity in this species pair. RESULTS: Analysis of microsatellites, cytochrome b gene sequences, and restriction digestion based genome-wide data revealed that C. sphinx and C. brachyotis do not hybridize in contact zones. However, cytochrome b gene sequences and genome-wide SNP data helped uncover a cryptic, hitherto unrecognized cynopterine lineage in northeastern India coexisting with C. sphinx. Further analyses of shared variation of SNPs using Patterson's D statistics suggest introgression between this lineage and C. sphinx. Multivariate analyses of morphology using genetically classified grouping confirmed substantial morphological overlap between C. sphinx and C. brachyotis, specifically in the high elevation contact zones in southern India. CONCLUSION: Our results uncover novel diversity and detect a pattern of genetic introgression in a cryptic radiation of bats, demonstrating the complicated nature of lineage diversification in this poorly understood taxonomic group. Our results highlight the importance of genome-wide data to study evolutionary processes of morphologically similar species pairs. Our approach represents a significant step forward in evolutionary research on young radiations of non-model species that may retain the ability of interspecific gene flow.

Auditory pre-experience modulates classification of affect intensity: evidence for the evaluation of call salience by a non-human mammal, the bat Megaderma lyra.

INTRODUCTION: Immediate responses towards emotional utterances in humans are determined by the acoustic structure and perceived relevance, i.e. salience, of the stimuli, and are controlled via a central feedback taking into account acoustic pre-experience. The present study explores whether the evaluation of stimulus salience in the acoustic communication of emotions is specifically human or has precursors in mammals. We created different pre-experiences by habituating bats (Megaderma lyra) to stimuli based on aggression, and response, calls from high or low intensity level agonistic interactions, respectively. Then we presented a test stimulus of opposite affect intensity of the same call type. We compared the modulation of response behaviour by affect intensity between the reciprocal experiments. RESULTS: For aggression call stimuli, the bats responded to the dishabituation stimuli independent of affect intensity, emphasising the attention-grabbing function of this call type. For response call stimuli, the bats responded to a high affect intensity test stimulus after experiencing stimuli of low affect intensity, but transferred habituation to a low affect intensity test stimulus after experiencing stimuli of high affect intensity. This transfer of habituation was not due to over-habituation as the bats responded to a frequency-shifted control stimulus. A direct comparison confirmed the asymmetric response behaviour in the reciprocal experiments. CONCLUSIONS: Thus, the present study provides not only evidence for a discrimination of affect intensity, but also for an evaluation of stimulus salience, suggesting that basic assessment mechanisms involved in the perception of emotion are an ancestral trait in mammals.

Perception of individuality in bat vocal communication: discrimination between, or recognition of, interaction partners?

Different cognitive processes underlying voice identity perception in humans may have precursors in mammals. A perception of vocal signatures may govern individualised interactions in bats, which comprise species living in complex social structures and are nocturnal, fast-moving mammals. This paper investigates to what extent bats recognise, and discriminate between, individual voices and discusses acoustic features relevant for accomplishing these tasks. In spontaneous presentation and habituation-dishabituation experiments, we investigated how Megaderma lyra perceives and evaluates stimuli consisting of contact call series with individual-specific signatures from either social partners or unknown individuals. Spontaneous presentations of contact call stimuli from social partners or unknown individuals elicited strong, but comparable reactions. In the habituation-dishabituation experiments, bats dishabituated significantly to any new stimulus. However, reactions were less pronounced to a novel stimulus from the bat used for habituation than to stimuli from other bats, irrespective of familiarity, which provides evidence for identity discrimination. A model separately assessing the dissimilarity of stimuli in syllable frequencies, syllable durations and inter-call intervals relative to learned memory templates accounted for the behaviour of the bats. With respect to identity recognition, the spontaneous presentation experiments were not conclusive. However, the habituation-dishabituation experiments suggested that the bats recognised voices of social partners as the reaction to a re-habituation stimulus differed after a dishabituation stimulus from a social partner and an unknown bat.

Home ranges, directionality and the influence of moon phases on the movement ecology of Indian flying fox males in southern India.

Flying foxes of the genus Pteropus are amongst the largest fruit bats and potential long-range pollinators and seed dispersers in the paleotropics. Pteropus giganteus (currently P. medius) is the only flying fox that is distributed throughout the Indian mainland, including in urban and rural areas. Using GPS telemetry, we mapped the home ranges and examined flight patterns in P. giganteus males across moon phases in a semi-urban landscape in southern India. Home range differed between the tracked males (n=4), likely due to differences in their experience in the landscape. We found that nightly time spent outside the roost, distance commuted and the number of sites visited by tracked individuals did not differ significantly between moon phases. In 61% of total tracked nights across bats, the first foraging site was within 45˚ of the emergence direction. At the colony-level, scan-based observations showed emergence flights were mostly in the northeast (27%), west (22%) and southwest (19%) directions that could potentially be related to the distribution of foraging resources. The movement ecology of fruit bats in relation to the pollination and seed dispersal services they provide requires to be investigated in future studies. This article has an associated First Person interview with the first author of the paper.

Promiscuous mating in the harem-roosting fruit bat, Cynopterus sphinx.

Observations on mating behaviours and strategies guide our understanding of mating systems and variance in reproductive success. However, the presence of cryptic strategies often results in situations where social mating system is not reflective of genetic mating system. We present such a study of the genetic mating system of a harem-forming bat Cynopterus sphinx where harems may not be true indicators of male reproductive success. This temporal study using data from six seasons on paternity reveals that social harem assemblages do not play a role in the mating system, and variance in male reproductive success is lower than expected assuming polygynous mating. Further, simulations reveal that the genetic mating system is statistically indistinguishable from promiscuity. Our results are in contrast to an earlier study that demonstrated high variance in male reproductive success. Although an outcome of behavioural mating patterns, standardized variance in male reproductive success (I(m)) affects the opportunity for sexual selection. To gain a better understanding of the evolutionary implications of promiscuity for mammals in general, we compared our estimates of I(m) and total opportunity for sexual selection (I(m) /I(f), where I(f) is standardized variance in female reproductive success) with those of other known promiscuous species. We observed a broad range of I(m) /I(f) values across known promiscuous species, indicating our poor understanding of the evolutionary implications of promiscuous mating.

Males and females gain differentially from sociality in a promiscuous fruit bat Cynopterus sphinx.

Sociality emerges when the benefits of group living outweigh its costs. While both males and females are capable of strong social ties, the evolutionary drivers for sociality and the benefits accrued maybe different for each sex. In this study, we investigate the differential reproductive success benefits of group membership that males and females might obtain in the promiscuous fruit bat Cynopterus sphinx. Individuals of this species live in flexible social groups called colonies. These colonies are labile and there is high turnover of individuals. However, colony males sire more offspring within the colony suggesting that being part of a colony may result in reproductive benefits for males. This also raises the possibility that long-term loyalty towards the colony may confer additional advantage in terms of higher reproductive success. We used ten seasons of genetic parentage data to estimate reproductive success and relatedness of individuals in the colony. We used recapture data to identify long and short-term residents in the colony as well as to obtain rates of recapture for males and females. Our results reveal that males have a significantly higher chance of becoming long-term residents (than females), and these long-term resident males gain twice the reproductive success compared to short-term resident males. We also observed that long-term resident females are related to each other and also achieve higher reproductive success than short-term resident females. In contrast, long-term resident males do not differ from short-term resident males in their levels of relatedness. Our results re-iterate the benefits of sociality even in species that are promiscuous and socially labile and possible benefits of maintaining a colony.