Martina Nagy

Female-biased dispersal and patrilocal kin groups in a mammal with resource-defence polygyny.

In most mammals, dispersal rates are higher in males than in females. Using behavioural and genetic data of individually marked bats, we show that this general pattern is reversed in the greater sac-winged bat (Saccopteryx bilineata). Dispersal is significantly female biased and male philopatry in combination with rare male immigration causes a patrilineal colony structure. Female dispersal helps avoid father–daughter inbreeding, as male tenure exceeds female age at first breeding in this bat species. Furthermore, our data suggest that females may engage in extra-harem copulations to mate with genetically dissimilar males, and thus avoid their male descendants as mating partners. Acquaintance with the natal colony might facilitate territory takeover since male sac-winged bats queue for harem access. Given the virtual absence of male immigration and the possible lower reproductive success of dispersing males, we argue that enhancing the likelihood of settlement of male descendants could be adaptive despite local mate competition. We conclude that resource defence by males is important in promoting male philopatry, and argue that the potential overlap of male tenure and female first conception is the driving force for females to disperse.

Bat echolocation calls facilitate social communication

Bat echolocation is primarily used for orientation and foraging but also holds great potential for social communication. The communicative function of echolocation calls is still largely unstudied, especially in the wild. Eavesdropping on vocal signatures encoding social information in echolocation calls has not, to our knowledge, been studied in free-living bats so far. We analysed echolocation calls of the polygynous bat Saccopteryx bilineata and found pronounced vocal signatures encoding sex and individual identity. We showed experimentally that free-living males discriminate approaching male and female conspecifics solely based on their echolocation calls. Males always produced aggressive vocalizations when hearing male echolocation calls and courtship vocalizations when hearing female echolocation calls; hence, they responded with complex social vocalizations in the appropriate social context. Our study demonstrates that social information encoded in bat echolocation calls plays a crucial and hitherto underestimated role for eavesdropping conspecifics and thus facilitates social communication in a highly mobile nocturnal mammal.

SONGS, SCENTS, AND SENSES: SEXUAL SELECTION IN THE GREATER SAC-WINGED BAT, SACCOPTERYX BILINEATA

Abstract Like many other mammals, Saccopteryx bilineata exhibits a polygynous mating system, in which each male defends a group of females called a harem. Colonies consist of several harems, and nonharem males roost adjacent to harems. Unlike most other mammals, females disperse from their natal colony and most juvenile males remain in it. Thus, colonies consist of patrilines, which promotes intense local mate competition. Females are in estrus during a few weeks at the end of the rainy season. Mating is most likely initiated by females and preceded by intense courtship displays of males. Forty percent of colony males do not sire any offspring during their tenure in the colony, whereas a few males can sire up to 6 offspring in a single year. Males use olfactory, visual, and acoustic signals for courtship, and they demonstrate territory ownership by scent marks, low-frequency calls, and visual displays. Harem males sire on average more offspring than do nonharem males but produce only 30% of the offspring within their own harem territory, with 70% being sired by other harem males or nonharem males. Reproductive success of males increases with decreasing size, fluctuating asymmetry, and fundamental frequency of territorial calls. In addition, females that are closely related to the harem holder are more likely to mate with other males than with the harem holder. Sexual selection in S. bilineata is most likely influenced by intense local mate competition caused by scarce roosts and the patrilineal organization of colonies.

Female-biased dispersal in a bat with a female-defence mating strategy.

The ultimate causes for predominant male‐biased dispersal (MBD) in mammals and female‐biased dispersal (FBD) in birds are still subject to much debate. Studying exceptions to general patterns of dispersal, for example, FBD in mammals, provides a valuable opportunity to test the validity of proposed evolutionary pressures. We used long‐term behavioural and genetic data on individually banded Proboscis bats (Rhynchonycteris naso) to show that this species is one of the rare mammalian exceptions with FBD. Our results suggest that all females disperse from their natal colonies prior to first reproduction and that a substantial proportion of males are philopatric and reproduce in their natal colonies, although male immigration has also been detected. The age of females at first conception falls below the tenure of males, suggesting that females disperse to avoid father–daughter inbreeding. Male philopatry in this species is intriguing because Proboscis bats do not share the usual mammalian correlates (i.e. resource‐defence polygyny and/or kin cooperation) of male philopatry. They have a mating strategy based on female defence, where local mate competition between male kin is supposedly severe and should prevent the evolution of male philopatry. However, in contrast to immigrant males, philopatric males may profit from acquaintance with the natal foraging grounds and may be able to attain dominance easier and/or earlier in life. Our results on Proboscis bats lent additional support to the importance of inbreeding avoidance in shaping sex‐biased dispersal patterns and suggest that resource defence by males or kin cooperation cannot fully explain the evolution of male philopatry in mammals.

Highly diversified coronaviruses in neotropical bats

Bats host a broad diversity of coronaviruses (CoVs), including close relatives of human pathogens. There is only limited data on neotropical bat CoVs. We analysed faecal, blood and intestine specimens from 1562 bats sampled in Costa Rica, Panama, Ecuador and Brazil for CoVs by broad-range PCR. CoV RNA was detected in 50 bats representing nine different species, both frugivorous and insectivorous. These bat CoVs were unrelated to known human or animal pathogens, indicating an absence of recent zoonotic spill-over events. Based on RNA-dependent RNA polymerase (RdRp)-based grouping units (RGUs) as a surrogate for CoV species identification, the 50 viruses represented five different alphacoronavirus RGUs and two betacoronavirus RGUs. Closely related alphacoronaviruses were detected in Carollia perspicillata and C. brevicauda across a geographical distance exceeding 5600 km. Our study expands the knowledge on CoV diversity in neotropical bats and emphasizes the association of distinct CoVs and bat host genera.

MHC-dependent mate choice is linked to a trace-amine-associated receptor gene in a mammal

Major histocompatibility complex (MHC) genes play a pivotal role in vertebrate self/nonself recognition, parasite resistance and life history decisions. In evolutionary terms, the MHC’s exceptional diversity is likely maintained by sexual and pathogen-driven selection. Even though MHC-dependent mating preferences have been confirmed for many species, the sensory and genetic mechanisms underlying mate recognition remain cryptic. Since olfaction is crucial for social communication in vertebrates, variation in chemosensory receptor genes could explain MHC-dependent mating patterns. Here, we investigated whether female mate choice is based on MHC alleles and linked to variation in chemosensory trace amine-associated receptors (TAARs) in the greater sac-winged bat (Saccopteryx bilineata). We sequenced several MHC and TAAR genes and related their variation to mating and paternity data. We found strong evidence for MHC class I-dependent female choice for genetically diverse and dissimilar males. We also detected a significant interaction between mate choice and the female TAAR3 genotype, with TAAR3-heterozygous females being more likely to choose MHC-diverse males. These results suggest that TAARs and olfactory cues may be key mediators in mammalian MHC-dependent mate choice. Our study may help identify the ligands involved in the chemical communication between potential mates.

Characterization of eight novel microsatellite markers for the neotropical bat Rhynchonycteris naso and cross-species utility

Neotropical emballonurid bats are known to exhibit an exceptional diversity in social systems and dispersal strategies. Here we report the isolation of eight new microsatellite markers which will be employed to investigate ultimate causes and consequences of sex-biased dispersal by use of paternity, relatedness and population structure analyses. Novel microsatellite markers developed for the species Rhynchonycteris naso turned out to be highly polymorphic. Number of alleles ranged from seven to 31 alleles per locus and expected heterozygosities ranged from 0.74 to 0.95. Seven loci were autosomal and one locus appeared to be situated on the X-Chromosome. Cross-species amplification in four species was more successful in more closely related than in more distantly related genera of neotropical emballonurids. Together with other eleven microsatellites initially isolated for Saccopteryx bilineata, we now posses powerful tools for studying species of the two bat genera, Saccopteryx and Rhynchonycteris.

From resource to female defence: the impact of roosting ecology on a bat's mating strategy

With their extraordinary species richness and diversity in ecological traits and social systems, bats are a promising taxon for testing socio-ecological hypotheses in order to get new insights into the evolution of animal social systems. Regarding its roosting habits, proboscis bats form an extreme by occupying sites which are usually completely exposed to daylight (e.g. tree trunks, vines or rocks). This is accompanied by morphological and behavioural adaptations to remain cryptic in exposed day roosts. With long-term behavioural observations and genetic parentage analyses of individually marked proboscis bats, we assessed its social dispersion and male mating strategy during day and night. Our results reveal nocturnal male territoriality—a strategy which most closely resembles a resource-defence polygyny that is frequent also in other tropical bats. Its contrasting clumped social dispersion during the day is likely to be the result of strong selection for crypsis in exposed roosts and is accompanied by direct female defence in addition to male territoriality. To the best of our knowledge, such contrasting male mating strategies within a single day–night cycle have not been described in a vertebrate species so far and illustrate a possible evolutionary trajectory from resource-defence to female-defence strategy by small ecologically driven evolutionary steps.

Sexually Selected Vocalizations of Neotropical Bats

Acoustic signals are by far the best studied component of bats’ social communication. Various different vocalization types cover diverse social interactions, which are either under natural selection pressures, such as mother–pup recognition and group cohesion, or under sexual selection pressures, such as male–male aggression, territoriality, and courtship. Here, we summarize the current knowledge about sexually selected vocalizations in Neotropical bats. Specifically, we highlight research findings on sexually selected vocalizations in two species whose social organization and natural history are well understood, namely Seba’s Short-tailed Bat Carollia perspicillata (Phyllostomidae) and the Greater Sac-winged Bat Saccopteryx bilineata (Emballonuridae). Males of both species exhibit resource-defense polygyny and use distinct vocalizations during aggressive male–male interactions and to announce territory ownership. While territorial vocalizations are structurally more complex in S. bilineata than in C. perspicillata, the latter species uses a more sophisticated, ritualized suite of behavioral displays to mediate male–male aggression than S. bilineata. Moreover, males of both species exhibit acoustic courtship which displays with differing degrees of complexity. In S. bilineata, courtship vocalizations are long and elaborate, while courtship vocalizations of C. perspicillata are comparatively simpler, with one variable syllable repeated in succession. As a synopsis, we discuss whether differences in social organization and behavioral interactions may have implications for the structural complexity and information content of sexually selected vocalizations.

The evolution of a rare mammalian trait – benefits and costs of male philopatry in proboscis bats

While inbreeding avoidance is widely accepted as the major driver of female natal dispersal, the evolution of male philopatry is still poorly understood and discussed to be driven by male mating strategy, mate competition among male kin and kin cooperation. During a twelve-year study, we gathered detailed genetic and observational data of individually marked proboscis bats to assess the degree of male philopatry as well as its costs and benefits to improve the understanding of its evolution. Our results reveal several patrilines with simultaneous presence of closely related males and a small proportion of unrelated immigrant males in their colonies. Philopatric males benefit from avoiding the costs of immigration into foreign colonies through significantly longer tenure, better integration (i.e. frequent nocturnal presence in the colonies) and consequently significantly higher reproductive success compared to immigrant males. Finally, we illustrate that despite a high proportion of philopatric males in the groups, the number of closely related competing males is low. Thus, the hypothesised costs of mate competition among male kin seem to be low in promiscuous mammalian societies with unrelated females and a small degree of male immigration and are readily outweighed by the benefits of staying in the natal group.