Roger D. Ransome

Echolocation Calls of Bats are Influenced by Maternal Effects and Change over a Lifetime

The greater horseshoe bat, Rhinolophus ferrumequinum, is a model species in echolocation studies, and emits calls containing long constant-frequency (CF) components. The bats have auditory systems tuned sharply to frequencies close to the resting CF (RF) values. Call frequency and neural processing are both flexible within individual bats which use this mode of echolocation. The simple structure of the calls makes them ideal for sonagraphic analysis. Here, in a large-scale and long-term analysis of changes in the vocalizations of bats we show that: (i) the calls of R. ferrumequinum aged 1-28 years vary seasonally and over a lifetime in a predictable manner; and (ii) an infant’s RF is at least partly determined by the RF of its mother. We consider the relative importance of genetic and learning factors upon the correlation between RFS of mothers and offspring.

Genetic variation and population structure in the endangered greater horseshoe bat Rhinolophus ferrumequinum

Following a dramatic decline last century, the British population of the endangered greater horseshoe bat Rhinolophus ferrumequinum is highly fragmented. To examine the consequences of fragmentation and limited dispersal on patterns of genetic structure and variation, we used microsatellite markers to screen bats from around 50% of the known maternity colonies in Britain, and two areas from continental Europe. Analyses revealed that Welsh and English colonies were genetically isolated. This, and lower variability in Britain than north France, may result from either genetic drift, or the species’ colonization history. Gene flow among most neighbouring colonies was not generally restricted, with one exception. These findings have important implications for the ongoing conservation management of this species.

Outbreeding increases offspring survival in wild greater horseshoe bats (Rhinolophus ferrumequinum)

The factors influencing the survival of greater horseshoe bat (Rhinolophus ferrumequinum) offspring born over seven years at a maternity colony in south-west Britain were studied. The effects of a range of phenotypic and maternal variables were analysed using a historical data set. In addition, the influence of two genetic measures on mortality, individual heterozygosity and a new measure of outbreeding, termed mean d2, was assessed. Logistic regressions were undertaken with survival modelled as a binary response variable. Survival to two life stages was studied for each variable and all models were developed for both sexes separately and together. Only one variable, mean d2, was significantly associated with survival. Male offspring with high mean d2 scores were more likely to survive to their first and second summers. The influence of mean d2 was not due to a single locus under selection but a wider multilocus effect and probably represents heterosis as opposed to solely inbreeding depression. Therefore, the extent to which an individual is outbred may determine survival more than widely used phenotypic characteristics such as size and mass. Mean d2 may reflect immunocompetence, which influences mortality. Protection of mating sites in order to facilitate gene flow and, therefore, outbreeding may help to promote population stability and growth.

Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats form maternity colonies each summer in order to give birth and raise young. During the mating period, females visit males occupying territorial sites, copulation takes place and sperm are stored until ovulation occurs, normally in April. Using microsatellite markers and a likelihood method of parentage analysis, we studied breeding behaviour and male reproductive success over a five–year period in a population of bats in south–west Britain. Paternity was assigned with 80% confidence to 44% of young born in five successive cohorts. While a small annual skew in male reproductive success was detected, the variance increased over five years due to the repeated success of a few individuals. Mating was polygynous, although some females gave birth to offspring sired by the same male in separate years. Such repeated partnerships probably result from fidelity for either mating sites or individuals or from sperm competition. Females mated with males born both within and outside their own natal colony; however, relatedness between parents was no less than the average recorded for male–female pairs. Gene flow between colonies is likely to be primarily mediated by both female and male dispersal during the mating period rather than more permanent movements.

Mate fidelity and intra-lineage polygyny in greater horseshoe bats

Mating strategies that lead to increased kinship within socially cooperative groups may offer inclusive fitness benefits to individuals, but can also result in higher levels of inbreeding. Here we show in a sexually segregated bat species that females avoid this conflict through two mating behaviours. First, most females revisit and breed with specific, individual males across years, so that their single offspring born in different years are full siblings. Second, relatives in the maternal line, including mothers and daughters, share breeding partners (intra-lineage polygyny) more often than expected by chance. Although these behaviours increased levels of co-ancestry among colony members, there was no concomitant rise in inbreeding. We suggest that when females engage in mate fidelity and intra-lineage polygyny, kin ties among female roost mates will be strengthened, thereby potentially contributing to social group cohesiveness. Our findings reveal the hidden complexity that can underlie polygynous breeding, and highlight a new potential route by which female mate choice could influence social evolution.

Long‐term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism

Most mammalian groups are characterized by male‐biased sexual size dimorphism, in which size‐dependent male–male competition and reproductive skew are tightly linked. By comparison, little is known about the opportunity for sexual selection in mammalian systems without male‐biased dimorphism, where the traits under sexual selection might be less obvious. We examined 10 years of parentage data in a colony of greater horseshoe bats (Rhinolophus ferrumequinum) to determine the magnitude of male reproductive skew and the opportunity for sexual selection in a mammal in which females are the larger sex. Annual paternity success was weakly skewed but consistent patterns led to strong longitudinal paternity skew among breeders. Just three males accounted for a third of all paternity assignments, representing at least a fifth of all colony offspring born in a decade. Paternity success was in part determined by age but was not influenced by dispersal status. Our results show that paternity skew and the opportunity for sexual selection in a species with reversed sexual size dimorphism can approach levels reported for classical examples of species with polygyny and male‐biased dimorphism, even where the traits under sexual selection are not known.

Determinants and Patterns of Reproductive Success in the Greater Horseshoe Bat during a Population Recovery

An individuals reproductive success will depend on traits that increase access to mates, as well as the number of mates available. In most well-studied mammals, males are the larger sex, and body size often increases success in intra-sexual contests and thus paternity. In comparison, the determinants of male success in species with reversed sexual size dimorphism (RSD) are less well understood. Greater horseshoe bats (Rhinolophus ferrumequinum) exhibit RSD and females appear to exert mate choice when they visit and copulate with males in their underground territories. Here we assessed putative determinants of reproductive success in a colony of greater horseshoe bats during a 19-year period of rapid population growth. We genotyped 1080 bats with up to 40 microsatellite loci and assigned maternity to 99.5% of pups, and paternity to 76.8% of pups. We found that in spite of RSD, paternity success correlated positively with male size, and, consistent with our previous findings, also with age. Female reproductive success, which has not previously been studied in this population, was also age-related and correlated positively with individual heterozygosity, but not with body size. Remarkable male reproductive skew was detected that initially increased steadily with population size, possibly coinciding with the saturation of suitable territories, but then levelled off suggesting an upper limit to a males number of partners. Our results illustrate that RSD can occur alongside intense male sexual competition, that male breeding success is density-dependent, and that male and female greater horseshoe bats are subject to different selective pressures.

Growing old, yet staying young: The role of telomeres in bats’ exceptional longevity

Telomeres do not shorten with age in longest-lived bats. Understanding aging is a grand challenge in biology. Exceptionally long-lived animals have mechanisms that underpin extreme longevity. Telomeres are protective nucleotide repeats on chromosome tips that shorten with cell division, potentially limiting life span. Bats are the longest-lived mammals for their size, but it is unknown whether their telomeres shorten. Using >60 years of cumulative mark-recapture field data, we show that telomeres shorten with age in Rhinolophus ferrumequinum and Miniopterus schreibersii, but not in the bat genus with greatest longevity, Myotis. As in humans, telomerase is not expressed in Myotis myotis blood or fibroblasts. Selection tests on telomere maintenance genes show that ATM and SETX, which repair and prevent DNA damage, potentially mediate telomere dynamics in Myotis bats. Twenty-one telomere maintenance genes are differentially expressed in Myotis, of which 14 are enriched for DNA repair, and 5 for alternative telomere-lengthening mechanisms. We demonstrate how telomeres, telomerase, and DNA repair genes have contributed to the evolution of exceptional longevity in Myotis bats, advancing our understanding of healthy aging.