Cost, risk, and avoidance of inbreeding in a cooperatively breeding bird.

Inbreeding is often avoided in natural populations by passive processes such as sex-biased dispersal. But, in many social animals, opposite-sexed adult relatives are spatially clustered, generating a risk of incest and hence selection for active inbreeding avoidance. Here we show that, in long-tailed tits (Aegithalos caudatus), a cooperative breeder that risks inbreeding by living alongside opposite-sex relatives, inbreeding carries fitness costs and is avoided by active kin discrimination during mate choice. First, we identified a positive association between heterozygosity and fitness, indicating that inbreeding is costly. We then compared relatedness within breeding pairs to that expected under multiple mate-choice models, finding that pair relatedness is consistent with avoidance of first-order kin as partners. Finally, we show that the similarity of vocal cues offers a plausible mechanism for discrimination against first-order kin during mate choice. Long-tailed tits are known to discriminate between the calls of close kin and nonkin, and they favor first-order kin in cooperative contexts, so we conclude that long-tailed tits use the same kin discrimination rule to avoid inbreeding as they do to direct help toward kin.

Sex-independent senescence in a cooperatively breeding mammal.

Researchers studying mammals have frequently interpreted earlier or faster rates of ageing in males as resulting from polygyny and the associated higher costs of reproductive competition. Yet, few studies conducted on wild populations have compared sex-specific senescence trajectories outside of polygynous species, making it difficult to make generalized inferences on the role of reproductive competition in driving senescence, particularly when other differences between males and females might also contribute to sex-specific changes in performance across lifespan. Here, we examine age-related variation in body mass, reproductive output and survival in dominant male and female meerkats, Suricata suricatta. Meerkats are socially monogamous cooperative breeders where a single dominant pair virtually monopolizes reproduction in each group and subordinate group members help to rear offspring produced by breeders. In contrast to many polygynous societies, we find that neither the onset nor the rate of senescence in body mass or reproductive output shows clear differences between males and females. Both sexes also display similar patterns of age-related survival across lifespan, but unlike most wild vertebrates, survival senescence (increases in annual mortality with rising age) was absent in dominants of both sexes, and as a result, the fitness costs of senescence were entirely attributable to declines in reproductive output from mid- to late-life. We suggest that the potential for intrasexual competition to increase rates of senescence in females-who are hormonally masculinized and frequently aggressive-is offset by their ability to maintain longer tenures of dominance than males, and that these processes when combined lead to similar patterns of senescence in both sexes. Our results stress the need to consider the form and intensity of sexual competition as well as other sex-specific features of life history when investigating the operation of senescence in wild populations.

Fine-scale genetic structure and helping decisions in a cooperatively breeding bird.

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long-term field data to investigate genetic structure in an adult population of long-tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine-scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male-biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long-tailed tits and support models identifying kin selection as the driver of cooperation.

Ecological and demographic correlates of helping behaviour in a cooperatively breeding bird.

The evolution of cooperation is a persistent problem for evolutionary biologists. In particular, understanding of the factors that promote the expression of helping behaviour in cooperatively breeding species remains weak, presumably because of the diverse nature of ecological and demographic drivers that promote sociality. In this study, we use data from a long-term study of a facultative cooperative breeder, the long-tailed tit Aegithalos caudatus, to investigate the factors influencing annual variation in helping behaviour. Long-tailed tits exhibit redirected helping in which failed breeders may become helpers, usually at a relative's nest; thus, helping is hypothesised to be associated with causes of nest failure and opportunities to renest or help. We tested predictions regarding the relationship between annual measures of cooperative behaviour and four explanatory variables: nest predation rate, length of the breeding season, population-level relatedness and population density. We found that the degree of helping was determined principally by two factors that constrain successful independent reproduction. First, as predicted, cooperative behaviour peaked at intermediate levels of nest predation, when there are both failed breeders (i.e. potential helpers) and active nests (i.e. potential recipients) available. Second, there were more helpers in shorter breeding seasons when opportunities for renesting by failed breeders are more limited. These are novel drivers of helping behaviour in avian cooperative breeding systems, and this study illustrates the difficulty of identifying common ecological or demographic factors underlying the evolution of such systems.

Assessing variability in marine traffic exposure between baleen whale species off the Galician Coast, Spain.

Increases in marine traffic represent a growing issue for marine wildlife, posing threats through the impacts of ship strikes and noise pollution. Baleen whales are especially vulnerable to these impacts, yet regional and species-specific information on exposure to such threats is lacking. This study uses AIS and observational data to provide the first assessment of baleen whale exposure to vessel traffic on the NW coast of Spain. Overlap with vessel traffic was detected for all areas where whales were sighted, indicating that these species may be at risk of vessel exposure and its associated impacts. Level of exposure to vessel traffic experienced by whales was species-specific, with risk of exposure appearing highest for minke whales. Vessel exposure also displayed intra- and inter-annual variability and a significant influence of feeding behaviour highlighting the need for dynamic management tools to minimise interactions between baleen whales and marine traffic off the Galician Coast.

Learned kin recognition cues in a social bird.

In many cooperatively breeding birds, kin selection has an important role in the evolution and maintenance of social behaviour, and 'helpers' can maximize indirect fitness gains by preferentially allocating care to close relatives. Although there is evidence for kin-biased helping behaviour in several species, the mechanism of kin recognition underlying this behaviour is poorly understood. Vocalizations are the most commonly used cues in avian recognition systems, but the effectiveness of vocal signals as reliable recognition cues must depend on how they are acquired. However, there have been no experimental studies of the development of vocal recognition cues in cooperative birds; indeed, the ontogeny of all bird vocalizations other than song is poorly known in any species. Here, we show that cooperatively breeding long-tailed tits (Aegithalos caudatus) can discriminate between kin and non-kin according to the individual-specific characteristics of contact calls, and show experimentally that individuals learn these calls from provisioning adults during the nestling period. Finally, we show that the pattern of cooperative behaviour in this species is consistent with the use of recognition cues learned through association.

Flyway-scale analysis reveals that the timing of migration in wading birds is becoming later.

Understanding the implications of climate change for migratory animals is paramount for establishing how best to conserve them. A large body of evidence suggests that birds are migrating earlier in response to rising temperatures, but many studies focus on single populations of model species.Migratory patterns at large spatial scales may differ from those occurring in single populations, for example because of individuals dispersing outside of study areas. Furthermore, understanding phenological trends across species is vital because we need a holistic understanding of how climate change affects wildlife, especially as rates of temperature change vary globally.The life cycles of migratory wading birds cover vast latitudinal gradients, making them particularly susceptible to climate change and, therefore, ideal model organisms for understanding its effects. Here, we implement a novel application of changepoint detection analysis to investigate changes in the timing of migration in waders at a flyway scale using a thirteen-year citizen science dataset (eBird) and determine the influence of changes in weather conditions on large-scale migratory patterns.In contrast to most previous research, our results suggest that migration is getting later in both spring and autumn. We show that rates of change were faster in spring than autumn in both the Afro-Palearctic and Nearctic flyways, but that weather conditions in autumn, not in spring, predicted temporal changes in the corresponding season. Birds migrated earlier in autumn when temperatures increased rapidly, and later with increasing headwinds.One possible explanation for our results is that migration is becoming later due to northward range shifts, which means that a higher proportion of birds travel greater distances and therefore take longer to reach their destinations. Our findings underline the importance of considering spatial scale when investigating changes in the phenology of migratory bird species.

Kinship affects investment by helpers in a cooperatively breeding bird.

Helping behaviour in cooperative breeding systems has been attributed to kin selection, but the relative roles of direct and indirect fitness benefits in the evolution of such systems remain a matter of debate. In theory, helpers could maximize the indirect fitness benefits of cooperation by investing more in broods with whom they are more closely related, but there is little evidence for such fine-scale adjustment in helper effort among cooperative vertebrates. In this study, we used the unusual cooperative breeding system of the long-tailed tit Aegithalos caudatus to test the hypothesis that the provisioning effort of helpers was positively correlated with their kinship to broods. We first use pedigrees and microsatellite genotypes to characterize the relatedness between helpers and breeders from a 14 year field study. We used both pedigree and genetic approaches because long-tailed tits have access to pedigree information acquired through social relationships, but any fitness consequences will be determined by genetic relatedness. We then show using both pedigrees and genetic relatedness estimates that alloparental investment by helpers increases as their relatedness to the recipients of their care increases. We conclude that kin selection has played a critical role in moulding the investment decisions of helpers in this cooperatively breeding species.

Reproductive senescence in a cooperatively breeding mammal.

1. Senescence (or 'ageing') is a widespread and important process in wild animal populations, but variation in ageing patterns within and between species is poorly understood. 2. In cooperatively breeding species, the costs of reproduction are shared between breeders and one or more helpers. The effects of ageing in breeders may therefore be moderated by the presence of helpers, but there have been very few studies of senescence patterns in natural populations of cooperative breeders. 3. Here, we use 13 years of data from a long-term study population of wild meerkats (Suricata suricatta) to investigate age-related changes in several traits known to be key components of reproductive success in females of this species. 4. Four of the six traits studied exhibited significant declines with age, indicating senescence. Litter size, the number of litters produced per year and the number of pups that survived to emergence from the natal burrow per year all increased with female age up to a peak at c. 4 years, and declined steeply thereafter; the mean pup weight at emergence in a given litter declined steadily from age zero. 5. These results provide the first evidence of reproductive senescence in a wild population of a cooperatively breeding vertebrate. Breeding success declined with age despite the sharing of reproductive costs in this species, but further study is needed to investigate whether helping affects other aspects of senescence, including survival.

Independent colonization of multiple urban centres by a formerly forest specialist bird species.

Urban areas are expanding rapidly, but a few native species have successfully colonized them. The processes underlying such colonization events are poorly understood. Using the blackbird Turdus merula, a former forest specialist that is now one of the most common urban birds in its range, we provide the first assessment of two contrasting urban colonization models. First, that urbanization occurred independently. Second, that following initial urbanization, urban-adapted individuals colonized other urban areas in a leapfrog manner. Previous analyses of spatial patterns in the timing of blackbird urbanization, and experimental introductions of urban and rural blackbirds to uncolonized cities, suggest that the leapfrog model is likely to apply. We found that, across the western Palaearctic, urban blackbird populations contain less genetic diversity than rural ones, urban populations are more strongly differentiated from each other than from rural populations and assignment tests support a rural source population for most urban individuals. In combination, these results provide much stronger support for the independent urbanization model than the leapfrog one. If the former model predominates, colonization of multiple urban centres will be particularly difficult when urbanization requires genetic adaptations, having implications for urban species diversity.

Dispersal of sibling coalitions promotes helping among immigrants in a cooperatively breeding bird.

Kin selection is a major force in social evolution, but dispersal is often assumed to reduce its impact by diluting kinship. In most cooperatively breeding vertebrates, in which more than two individuals care for young, juveniles delay dispersal and become helpers in family groups. In long-tailed tits (Aegithalos caudatus), however, offspring disperse to breed and helpers are failed breeders that preferentially aid kin. Helping also occurs among immigrants, but their origins are unknown and cooperation in these cases is poorly understood. Here, we combine long-term demographic and genetic data from our study population to investigate immigration and helping in this species. We first used a novel application of parentage analysis to discriminate between immigrants and unknown philopatric recruits. We then cross-checked sibship reconstruction with pairwise relatedness estimates to show that immigrants disperse in sibling coalitions and helping among them is kin biased. These results indicate that dispersal need not preclude sociality, and dispersal of kin coalitions may help maintain kin-selected cooperation in the absence of delayed dispersal.

The effect of early life conditions on song traits in male dippers (Cinclus cinclus).

Song complexity and singing frequency in male birds are shaped by female choice; they signal male quality because song is costly to develop and produce. The timing of song learning and the development of the brain structures involved occur during a period when chicks are exposed to a number of potential stressors. The quality and quantity of song produced by adults may therefore reflect the level of stress experienced during early life, a theory known as the 'developmental stress hypothesis'. We tested this hypothesis using song recordings and life-history data from an individually marked, long-term study population of wild dippers (Cinclus cinclus). The extent to which early life conditions predict adult song traits was investigated using natal brood size as a measure of sibling competition; the rate of provisioning by parents as a proxy for nutritional stress; and residuals of the linear regression between body mass and tarsus length as a measure of nestling condition. The syllable diversity in the songs of adult males was positively correlated with their body condition as nestlings, but there was no significant correlation with either provisioning rate or brood size. Provisioning rate did, however, predict song rate; males in relatively poor condition as nestlings or those raised in smaller broods which were fed more frequently by their parents sang at a higher rate in adulthood. These results support the developmental stress hypothesis and provide some of the first evidence from a wild bird of how the conditions experienced during early life impact adult song. Song traits may therefore provide females with information regarding both the current condition and developmental history of males.

Carnivore hotspots in Peninsular Malaysia and their landscape attributes.

Mammalian carnivores play a vital role in ecosystem functioning. However, they are prone to extinction because of low population densities and growth rates, and high levels of persecution or exploitation. In tropical biodiversity hotspots such as Peninsular Malaysia, rapid conversion of natural habitats threatens the persistence of this vulnerable group of animals. Here, we carried out the first comprehensive literature review on 31 carnivore species reported to occur in Peninsular Malaysia and updated their probable distribution. We georeferenced 375 observations of 28 species of carnivore from 89 unique geographic locations using records spanning 1948 to 2014. Using the Getis-Ord Gi*statistic and weighted survey records by IUCN Red List status, we identified hotspots of species that were of conservation concern and built regression models to identify environmental and anthropogenic landscape factors associated with Getis-Ord Gi* z scores. Our analyses identified two carnivore hotspots that were spatially concordant with two of the peninsula's largest and most contiguous forest complexes, associated with Taman Negara National Park and Royal Belum State Park. A cold spot overlapped with the southwestern region of the Peninsula, reflecting the disappearance of carnivores with higher conservation rankings from increasingly fragmented natural habitats. Getis-Ord Gi* z scores were negatively associated with elevation, and positively associated with the proportion of natural land cover and distance from the capital city. Malaysia contains some of the world's most diverse carnivore assemblages, but recent rates of forest loss are some of the highest in the world. Reducing poaching and maintaining large, contiguous tracts of lowland forests will be crucial, not only for the persistence of threatened carnivores, but for many mammalian species in general.