Hannah L. Dugdale

Polygynandry, extra-group paternity and multiple-paternity litters in European badger (Meles meles) social groups

The costs and benefits of natal philopatry are central to the formation and maintenance of social groups. Badger groups, thought to form passively according to the resource dispersion hypothesis (RDH), are maintained through natal philopatry and delayed dispersal; however, there is minimal evidence for the functional benefits of such grouping. We assigned parentage to 630 badger cubs from a high‐density population in Wytham Woods, Oxford, born between 1988 and 2005. Our methodological approach was different to previous studies; we used 22 microsatellite loci to assign parent pairs, which in combination with sibship inference provided a high parentage assignment rate. We assigned both parents to 331 cubs at ≥ 95% confidence, revealing a polygynandrous mating system with up to five mothers and five fathers within a social group. We estimated that only 27% of adult males and 31% of adult females bred each year, suggesting a cost to group living for both sexes. Any strong motivation or selection to disperse, however, may be reduced because just under half of the paternities were gained by extra‐group males, mainly from neighbouring groups, with males displaying a mixture of paternity strategies. We provide the strongest evidence to date for multiple‐paternity litters, and for the first time show that within‐group and extra‐group males can sire cubs in the same litter. We investigate the factors that may play a role in determining the degree of delayed dispersal and conclude that the ecological constraints hypothesis, benefits of philopatry hypothesis, and life history hypothesis may all play a part, as proposed by the broad constraints hypothesis.

Promiscuity, paternity and personality in the great tit

Understanding causes of variation in promiscuity within populations remain a major challenge. While most studies have focused on quantifying fitness costs and benefits of promiscuous behaviour, an alternative possibility—that variation in promiscuity within populations is maintained because of linkage with other traits—has received little attention. Here, we examine whether promiscuity in male and female great tits (Parus major)—quantified as extra-pair paternity (EPP) within and between nests—is associated with variation in a well-documented personality trait: exploration behaviour in a novel environment. Exploration behaviour has been shown to correlate with activity levels, risk-taking and boldness, and these are behaviours that may plausibly influence EPP. Exploration behaviour correlated positively with paternity gained outside the social pair among males in our population, but there was also a negative correlation with paternity in the social nest. Hence, while variation in male personality predicted the relative importance of paternity gain within and outside the pair bond, total paternity gained was unrelated to exploration behaviour. We found evidence that males paired with bold females were more likely to sire extra-pair young. Our data thus demonstrate a link between personality and promiscuity, with no net effects on reproductive success, suggesting personality-dependent mating tactics, in contrast with traditional adaptive explanations for promiscuity.

Female Receptiveity, Embryonic Diapause, and Superfetation in the European Badger (Meles Meles: Implications for the Reproductive Tactics of Males and Females

The European badger Meles meles is thought to mate throughout the year, with two mating peaks occurring in late winter/spring and summer/autumn. After mating, fertilized ova enter embryonic diapause (delayed implantation) at the blastocyst stage, which lasts up to eleven months. Even if mating is successful, however, the estrous cycle may continue during embryonic diapause, which suggests that female badgers are capable of superfetation (conception during pregnancy). This may increase female fitness by facilitating polyandry, and reduce the risk of infanticide by resident males through paternity confusion. Detailed understanding of female receptivity, specifically the association of superfetation with embryonic diapause, may explain field observations of seemingly inconsistent reproductive tactics of male badgers with regard to, for instance, whether or not they guard mates or defend territories. The combination of embryonic diapause and superfetation may occur in other mustelids; if so, the sociobiology of mustelids will need re‐evaluating, and the Mustelidae may prove to be a good model taxon for studies of sexual conflict in the reproduction of eutherian mammals.

Fewer invited talks by women in evolutionary biology symposia

Lower visibility of female scientists, compared to male scientists, is a potential reason for the under‐representation of women among senior academic ranks. Visibility in the scientific community stems partly from presenting research as an invited speaker at organized meetings. We analysed the sex ratio of presenters at the European Society for Evolutionary Biology (ESEB) Congress 2011, where all abstract submissions were accepted for presentation. Women were under‐represented among invited speakers at symposia (15% women) compared to all presenters (46%), regular oral presenters (41%) and plenary speakers (25%). At the ESEB congresses in 2001–2011, 9–23% of invited speakers were women. This under‐representation of women is partly attributable to a larger proportion of women, than men, declining invitations: in 2011, 50% of women declined an invitation to speak compared to 26% of men. We expect invited speakers to be scientists from top ranked institutions or authors of recent papers in high‐impact journals. Considering all invited speakers (including declined invitations), 23% were women. This was lower than the baseline sex ratios of early‐mid career stage scientists, but was similar to senior scientists and authors that have published in high‐impact journals. High‐quality science by women therefore has low exposure at international meetings, which will constrain Evolutionary Biology from reaching its full potential. We wish to highlight the wider implications of turning down invitations to speak, and encourage conference organizers to implement steps to increase acceptance rates of invited talks.

Age-specific breeding success in a wild mammalian population: selection, constraint, restraint and senescence

The Selection, Constraint, Restraint and Senescence Hypotheses predict how breeding success should vary with age. The Selection Hypothesis predicts between‐individual variation arising from quality differences; the other hypotheses predict within‐individual variation due to differing skills or physiological condition (Constraint), residual reproductive lifespan (Restraint), or somatic and reproductive investment (Senescence). Studies tend to focus on either the initial increase in breeding success or later decrease; however, both require consideration when unravelling the underlying evolutionary processes. Additionally, few studies present genetic fitness measures and rarely for both sexes. We therefore test these four hypotheses, which are not mutually exclusive, in a high‐density population of European badgers Meles meles. Using an 18‐year data set (including 22 microsatellite loci), we show an initial improvement in breeding success with age, followed by a later and steeper rate of reproductive senescence in male than in female badgers. Breeding success was skewed within age‐classes, indicating the influence of factors other than age‐class. This was partly attributable to selective appearance and disappearance of badgers (Selection Hypothesis). Individuals with a late age of last breeding showed a concave‐down relationship between breeding success and experience (Constraint Hypothesis). There was no evidence of abrupt terminal effects; rather, individuals showed a concave‐down relationship between breeding success and residual reproductive lifespan (Restraint Hypothesis), with an interaction with age of first breeding only in female badgers. Our results demonstrate the importance of investigating a comprehensive suite of factors in age‐specific breeding success analyses, in both sexes, to fully understand evolutionary and population dynamics.

Reproductive skew and relatedness in social groups of European badgers, Meles meles

Reproductive skew is a measure of the proportion of individuals of each sex that breed in a group and is a valuable measure for understanding the evolution and maintenance of sociality. Here, we provide the first quantification of reproductive skew within social groups of European badgers Meles meles, throughout an 18‐year study in a high‐density population. We used 22 microsatellite loci to analyse within‐group relatedness and demonstrated that badger groups contained relatives. The average within‐group relatedness was high (R = 0.20) and approximately one‐third of within‐group dyads were more likely to represent first‐order kin than unrelated pairs. Adult females within groups had higher pairwise relatedness than adult males, due to the high frequency of extra‐group paternities, rather than permanent physical dispersal. Spatial clustering of relatives occurred among neighbouring groups, which we suggest was due to the majority of extra‐group paternities being attributable to neighbouring males. Reproductive skew was found among within‐group candidate fathers (B = 0.26) and candidate mothers (B = 0.07), but not among breeding individuals; our power to detect skew in the latter was low. We use these results to evaluate reproductive skew models. Although badger society best fits the assumptions of the incomplete‐control models, our results were not consistent with their predictions. We suggest that this may be due to female control of paternity, female–female reproductive suppression occurring only in years with high food availability resulting in competition over access to breeding sites, extra‐group paternity masking the benefits of natal philopatry, and/or the inconsistent occurrence of hierarchies that are linear when established.

Senescence in the wild: Insights from a long-term study on Seychelles warblers.

Senescence--the progressive age-dependent decline in performance--occurs in most organisms. There is considerable variation in the onset and rate of senescence between and within species. Yet the causes of this variation are still poorly understood, despite being central to understanding the evolution of senescence. Long-term longitudinal studies on wild animals are extremely well-suited to studying the impact of environmental and individual characteristics (and the interaction between the two) on senescence, and can help us to understand the mechanisms that shape the evolution of senescence. In this review, we summarize and discuss the insights gained from our comprehensive long-term individual-based study of the Seychelles warbler (Acrocephalus sechellensis). This species provides an excellent model system in which to investigate the evolution of senescence in the wild. We found that Seychelles warblers show senescent declines in survival and reproduction, and discuss how individual characteristics (body condition, body size) and environmental effects (low- versus high-quality environments) may affect the onset and rate of senescence. Further, we highlight the evidence for trade-offs between early-life investment and senescence. We describe how key cellular and physiological processes (oxidative stress and telomere shortening) underpinning senescence are affected by individual and environmental characteristics in the Seychelles warbler (e.g. food availability, reproductive investment, disease) and we discuss how such physiological variation may mediate the relationship between environmental characteristics and senescence. Based on our work using Seychelles warblers as a model system, we show how insights from long-term studies of wild animals may help unravel the causes of the remarkable variation in senescence observed in natural systems, and highlight areas for promising future research.

Alloparental behaviour and long-term costs of mothers tolerating other members of the group in a plurally breeding mammal

Cooperative-breeding studies tend to focus on a few alloparental behaviours in highly cooperative species exhibiting high reproductive skew and the associated short-term, but less frequently long-term, fitness costs. We analysed a suite of alloparental behaviours (assessed via filming) in a kin-structured, high-density population of plurally breeding European badgers, Meles meles, which are not highly cooperative. Group members, other than mothers, performed alloparental behaviour; however, this was not correlated with their relatedness to within-group young. Furthermore, mothers babysat, allogroomed cubs without reciprocation, and allomarked cubs more than other members of the group (controlling for observation time). For welfare reasons, we could not individually mark cubs; however, the number observed pre-independence never exceeded that trapped. All 24 trapped cubs, in three filmed groups, were assigned both parents using 22 microsatellites. Mothers may breed cooperatively, as the time they babysat their assigned, or a larger, litter size did not differ. Furthermore, two mothers probably allonursed, as they suckled more cubs than their assigned litter size. An 18-year genetic pedigree, however, detected no short-term (litter size; maternal survival to the following year) or long-term (offspring breeding probability; offspring lifetime breeding success) fitness benefits with more within-group mothers or other members of the group. Rather, the number of other members of the group (excluding mothers) correlated negatively with long-term fitness. Mothers may tolerate other members of the group, as nonbreeders undertook more digging. Our study highlights that alloparental care varies on a continuum from that seen in this high-density badger population, where alloparenting behaviour is minimal, through to species where alloparental care is common and provides fitness benefits

Context-dependent linear dominance hierarchies in social groups of European badgers, Meles meles

A social hierarchy is generally assumed to exist in those mammalian societies in which the costs and benefits of group living are distributed unevenly among group members. We analysed infrared closed-circuit television footage, collected over 3 years in Wytham Woods, Oxfordshire, to test whether social groups of European badgers have dominance hierarchies. Analysis of directed aggression between dyads revealed linear dominance hierarchies in three social-group-years, but patterns within social groups were not consistent across years. Dominance hierarchies were significantly steeper than random in five out of six social-group-years. In those social-group-years where a linear hierarchy was determined, there was an effect of sex on dominance rank, with females gaining significantly higher rank than males in two social-group-years. Overall, rank was not related to age, nor did it appear to affect the likelihood of an individual being wounded, or an individuals breeding status. The latter resulted from nonorthogonality between sex and breeding status, as there were only two breeding males. Overall, hierarchies were primarily dominated by breeding females, and may occur when breeding competition arises. Relatedness, unreciprocated allogrooming and sequential allomarking were not consistently related to levels of directed aggression across social-group-years. We suggest that dominance structures within European badger groups may be context dependent, with future study required to complete our understanding of where, and when, they arise.

Telomere length reveals cumulative individual and transgenerational inbreeding effects in a passerine bird

Inbreeding results in more homozygous offspring that should suffer reduced fitness, but it can be difficult to quantify these costs for several reasons. First, inbreeding depression may vary with ecological or physiological stress and only be detectable over long time periods. Second, parental homozygosity may indirectly affect offspring fitness, thus confounding analyses that consider offspring homozygosity alone. Finally, measurement of inbreeding coefficients, survival and reproductive success may often be too crude to detect inbreeding costs in wild populations. Telomere length provides a more precise measure of somatic costs, predicts survival in many species and should reflect differences in somatic condition that result from varying ability to cope with environmental stressors. We studied relative telomere length in a wild population of Seychelles warblers (Acrocephalus sechellensis) to assess the lifelong relationship between individual homozygosity, which reflects genome‐wide inbreeding in this species, and telomere length. In juveniles, individual homozygosity was negatively associated with telomere length in poor seasons. In adults, individual homozygosity was consistently negatively related to telomere length, suggesting the accumulation of inbreeding depression during life. Maternal homozygosity also negatively predicted offspring telomere length. Our results show that somatic inbreeding costs are environmentally dependent at certain life stages but may accumulate throughout life.