Hot and dry conditions predict shorter nestling telomeres in an endangered songbird: Implications for population persistence.

Climate warming is increasingly exposing wildlife to sublethal high temperatures, which may lead to chronic impacts and reduced fitness. Telomere length (TL) may link heat exposure to fitness, particularly at early-life stages, because developing organisms are especially vulnerable to adverse conditions, adversity can shorten telomeres, and TL predicts fitness. Here, we quantify how climatic and environmental conditions during early life are associated with TL in nestlings of wild purple-crowned fairy-wrens (Malurus coronatus), endangered songbirds of the monsoonal tropics. We found that higher average maximum air temperature (range 31 to 45 °C) during the nestling period was associated with shorter early-life TL. This effect was mitigated by water availability (i.e., during the wet season, with rainfall), but independent of other pertinent environmental conditions, implicating a direct effect of heat exposure. Models incorporating existing information that shorter early-life TL predicts shorter lifespan and reduced fitness showed that shorter TL under projected warming scenarios could lead to population decline across plausible future water availability scenarios. However, if TL is assumed to be an adaptive trait, population viability could be maintained through evolution. These results are concerning because the capacity to change breeding phenology to coincide with increased water availability appears limited, and the evolutionary potential of TL is unknown. Thus, sublethal climate warming effects early in life may have repercussions beyond individual fitness, extending to population persistence. Incorporating the delayed reproductive costs associated with sublethal heat exposure early in life is necessary for understanding future population dynamics with climate change.

Cooperative breeding and the emergence of multilevel societies in birds.

Multilevel societies (MLSs), where social levels are hierarchically nested within each other, are considered one of the most complex forms of animal societies. Although thought to mainly occurs in mammals, it is suggested that MLSs could be under-detected in birds. Here, we propose that the emergence of MLSs could be common in cooperatively breeding birds, as both systems are favoured by similar ecological and social drivers. We first investigate this proposition by systematically comparing evidence for multilevel social structure in cooperative and non-cooperative birds in Australia and New Zealand, a global hotspot for cooperative breeding. We then analyse non-breeding social networks of cooperatively breeding superb fairy-wrens (Malurus cyaneus) to reveal their structured multilevel society, with three hierarchical social levels that are stable across years. Our results confirm recent predictions that MLSs are likely to be widespread in birds and suggest that these societies could be particularly common in cooperatively breeding birds.

Kinship and familiarity mitigate costs of social conflict between Seychelles warbler neighbors.

Because virtually all organisms compete with others in their social environment, mechanisms that reduce conflict between interacting individuals are crucial for the evolution of stable families, groups, and societies. Here, we tested whether costs of social conflict over territorial space between Seychelles warblers (Acrocephalus sechellensis) are mitigated by kin-selected (genetic relatedness) or mutualistic (social familiarity) mechanisms. By measuring longitudinal changes in individuals' body mass and telomere length, we demonstrated that the fitness costs of territoriality are driven by a complex interplay between relatedness, familiarity, local density, and sex. Physical fights were less common at territory boundaries shared between related or familiar males. In line with this, male territory owners gained mass when living next to related or familiar males and also showed less telomere attrition when living next to male kin. Importantly, these relationships were strongest in high-density areas of the population. Males also had more rapid telomere attrition when living next to unfamiliar male neighbors, but mainly when relatedness to those neighbors was also low. In contrast, neither kinship nor familiarity was linked to body mass or telomere loss in female territory owners. Our results indicate that resolving conflict over territorial space through kin-selected or mutualistic pathways can reduce both immediate energetic costs and permanent somatic damage, thus providing an important mechanism to explain fine-scale population structure and cooperation between different social units across a broad range of taxa.

Early-life telomere length predicts lifespan and lifetime reproductive success in a wild bird.

Poor conditions during early development can initiate trade-offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life-history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early-life conditions to lifespan and fitness. In wild purple-crowned fairy-wrens, we combined measurements of nestling telomere length (TL) with detailed life-history data to investigate whether early-life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age-dependent with early-life TL having a positive effect on lifespan only among individuals that survived their first year. Early-life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early-life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early-life TL, which reflects growth, accumulated early-life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early-life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early- and late-life performance and trade-offs across a lifetime.

Rapid plastic breeding response to rain matches peak prey abundance in a tropical savanna bird.

Changes in climate are shifting the timing of life cycle events in the natural world. Compared to northern temperate areas, these effects are relatively poorly understood in tropical and southern regions, where there is limited information on how timing of breeding and food availability are affected by climatic factors, and where patterns of breeding activity are more unpredictable within and between years. Combining a new statistical modelling approach with 5 years of continuous individual-based monitoring of a monsoonal tropical insectivorous bird, we quantified (a) the proximate climatic drivers at two trophic levels: timing of breeding and abundance of arthropod prey; (b) the effect of climate variation on reproductive output and (c) the role of individual plasticity. Rainfall was identified as the main determinant of phenology at both trophic levels. Throughout the year, likelihood of egg laying increased very rapidly in response to even small amounts of rain during the preceding 0-3 weeks. Adult body mass and male sperm storage also increased rapidly after rain, suggesting high breeding preparedness. Additionally, females were flexible, since they were more likely to nest whether their previous attempt was longer ago and unsuccessful. Arthropod abundance also increased after rainfall, but more slowly, with a peak around 10 weeks. Therefore, the peak food availability coincided with the presence of dependent fledglings. Fitness benefits of nesting after more rain appeared to be linked to offspring quantity rather than quality: nest attempts following higher rainfall produced larger clutches, but showed no improvement in nestling mass or relative fledging success. The response of clutch size to rainfall was plastic, since repeated sampling showed that individual females laid larger clutches after more rain, possibly mediated by improved body mass. Rapid, individually flexible breeding in response to rainfall and slower increase in arthropod abundance also as a response to rainfall, might buffer insectivorous species living in tropical seasonal environments from climate change-induced phenological trophic mismatches.

Food, friends or family: What drives delayed dispersal in group-living animals?

In Focus: Nelson-Flower, M. A., Wiley, E. M., Flower, T. P., & Ridley, A. R. (2018). Individual dispersal delays in a cooperative breeder: Ecological constraints, the benefits of philopatry and the social queue for dominance. Journal of Animal Ecology, 87, 1227-1238. https://doi.org/10.1111/1365-2656.12814 Explaining why sexually mature individuals in social species delay dispersal and independent breeding is a major unresolved evolutionary puzzle. In this issue, Nelson-Flower, Wiley, Flower, and Ridley () use a comprehensive dataset to study delayed dispersal in cooperatively breeding southern pied babblers. They test traditional hypotheses relating to ecological constraints inhibiting individuals to reproduce independently and benefits of philopatry motivating individuals to stay. Importantly, they also test the recently developed "dual-benefits" hypothesis, which explicitly takes into account that groups (even those containing unrelated individuals) may form because of opportunities for collective actions that increase the fitness of the whole group. While they show that male dispersal decisions are mainly determined by ecological constraints and the presence of related individuals, female dispersal cannot be explained this way. Instead, females from smaller groups were more likely to disperse than females from larger groups. In combination with evidence that smaller groups are more likely to accept (unrelated) subordinates and clear (collective-action) benefits of living in a larger group in this species, the study provides empirical evidence that considering social context and collective-action benefits as part of a comprehensive predictive framework is important to explain the evolutionary stability of delayed dispersal, group formation and, ultimately, cooperative breeding.

From ornament to armament or loss of function? Breeding plumage acquisition in a genetically monogamous bird.

The evolution of conspicuous male traits is thought to be driven by female mate choice or male-male competition. These two mechanisms are often viewed as distinct processes, with most studies focusing on female choice. However, both mechanisms of sexual selection can act simultaneously on the same trait (i.e., dual function) and/or interact in a synergistic or conflicting way. Dual-function traits are commonly assumed to originate through male-male competition before being used in female choice; yet, most studies focusing on such traits could not determine the direction of change, lacking phylogenetic information. We investigated the role of conspicuous male seasonal plumage in male-male competitive interactions in the purple-crowned fairy-wren Malurus coronatus, a cooperatively breeding bird. Male breeding plumage in most Malurus species is selected by female choice through extra-pair mate choice, but unlike its congeners, M. coronatus is genetically monogamous, and females do not seem to choose males based on breeding plumage acquisition. Our study shows that, within groups, subordinate males that were older, and therefore higher-ranked in the queue for breeder position inheritance, produced a more complete breeding plumage. In line with this, subordinate males that were older and/or displayed a more complete breeding plumage were more successful in competitively acquiring a breeder position. A role as a signal of competitive ability was experimentally confirmed by presenting models of males: in breeding colours, these received more aggression from resident breeder males than in nonbreeding colours, but elicited limited response from females, consistent with competitors in breeding plumage being perceived as a bigger threat to the breeder male. The role of the conspicuous breeding plumage in mediating male-male interactions might account for its presence in this genetically monogamous species. As phylogenetic reconstructions suggest a past female choice function in M. coronatus, this could represent a sexual trait that shifted functions, or a dual-function trait that lost one function. These evolutionary scenarios imply that intra- and intersexual functions of ornaments may be gained or lost independently and offer new perspectives in understanding the complex dynamics of sexual selection.

Subordinate females in the cooperatively breeding Seychelles warbler obtain direct benefits by joining unrelated groups.

In many cooperatively breeding animals, a combination of ecological constraints and benefits of philopatry favours offspring taking a subordinate position on the natal territory instead of dispersing to breed independently. However, in many species individuals disperse to a subordinate position in a non-natal group ("subordinate between-group" dispersal), despite losing the kin-selected and nepotistic benefits of remaining in the natal group. It is unclear which social, genetic and ecological factors drive between-group dispersal. We aim to elucidate the adaptive significance of subordinate between-group dispersal by examining which factors promote such dispersal, whether subordinates gain improved ecological and social conditions by joining a non-natal group, and whether between-group dispersal results in increased lifetime reproductive success and survival. Using a long-term dataset on the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), we investigated how a suite of proximate factors (food availability, group composition, age and sex of focal individuals, population density) promote subordinate between-group dispersal by comparing such dispersers with subordinates that dispersed to a dominant position or became floaters. We then analysed whether subordinates that moved to a dominant or non-natal subordinate position, or became floaters, gained improved conditions relative to the natal territory and compared fitness components between the three dispersal strategies. We show that individuals that joined another group as non-natal subordinates were mainly female and that, similar to floating, between-group dispersal was associated with social and demographic factors that constrained dispersal to an independent breeding position. Between-group dispersal was not driven by improved ecological or social conditions in the new territory and did not result in higher survival. Instead, between-group dispersing females often became cobreeders, obtaining maternity in the new territory, and were likely to inherit the territory in the future, leading to higher lifetime reproductive success compared to females that floated. Males never reproduced as subordinates, which may be one explanation why subordinate between-group dispersal by males is rare. Our results suggest that subordinate between-group dispersal is used by females to obtain reproductive benefits when options to disperse to an independent breeding position are limited. This provides important insight into the additional strategies that individuals can use to obtain reproductive benefits.

Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family.

Extra-pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.

The importance of the altricial - precocial spectrum for social complexity in mammals and birds - a review.

Various types of long-term stable relationships that individuals uphold, including cooperation and competition between group members, define social complexity in vertebrates. Numerous life history, physiological and cognitive traits have been shown to affect, or to be affected by, such social relationships. As such, differences in developmental modes, i.e. the 'altricial-precocial' spectrum, may play an important role in understanding the interspecific variation in occurrence of social interactions, but to what extent this is the case is unclear because the role of the developmental mode has not been studied directly in across-species studies of sociality. In other words, although there are studies on the effects of developmental mode on brain size, on the effects of brain size on cognition, and on the effects of cognition on social complexity, there are no studies directly investigating the link between developmental mode and social complexity. This is surprising because developmental differences play a significant role in the evolution of, for example, brain size, which is in turn considered an essential building block with respect to social complexity. Here, we compiled an overview of studies on various aspects of the complexity of social systems in altricial and precocial mammals and birds. Although systematic studies are scarce and do not allow for a quantitative comparison, we show that several forms of social relationships and cognitive abilities occur in species along the entire developmental spectrum. Based on the existing evidence it seems that differences in developmental modes play a minor role in whether or not individuals or species are able to meet the cognitive capabilities and requirements for maintaining complex social relationships. Given the scarcity of comparative studies and potential subtle differences, however, we suggest that future studies should consider developmental differences to determine whether our finding is general or whether some of the vast variation in social complexity across species can be explained by developmental mode. This would allow a more detailed assessment of the relative importance of developmental mode in the evolution of vertebrate social systems.