Ecogeography of group size suggests differences in drivers of sociality among cooperatively breeding fairywrens

Cooperatively breeding species exhibit a range of social behaviors associated with different costs and benefits to group-living, often in association with different environmental conditions. For example, species in which collective-care of offspring reduces the cost of reproduction are more common in harsh environments (true cooperative breeding), while species that collectively defend resources are present in benign environments (family-living). Here, we examine whether environment also shapes sociality within cooperatively-breeding species. We illustrate that Purple-backed Fairywrens, which primarily gain intrinsic, or collective-care benefits, have larger groups in hot, dry environments and smaller groups in cool, wet environments, whereas Superb Fairywrens which primarily gain extrinsic, or resource defense benefits, exhibit the opposite trend. We suggest differences in the costs and benefits of sociality contribute to these opposing ecogeographic patterns, demonstrating that comparisons of intraspecific patterns of social variation across species can provide insight into how ecology shapes transitions between social systems.

Extended and cumulative effects of experimentally induced intergroup conflict in a cooperatively breeding mammal

Conflict between rival groups is rife in nature. While recent work has begun exploring the behavioural consequences of this intergroup conflict, studies have primarily considered just the 1–2 h immediately after single interactions with rivals or their cues. Using a habituated population of wild dwarf mongooses ( Helogale parvula ), we conducted week-long manipulations to investigate longer-term impacts of intergroup conflict. Compared to a single presentation of control herbivore faeces, one rival-group faecal presentation (simulating a territorial intrusion) resulted in more within-group grooming the following day, beyond the likely period of conflict-induced stress. Repeated presentations of outsider cues led to further changes in baseline behaviour by the end of the week: compared to control weeks, mongooses spent less time foraging and foraged closer to their groupmates, even when there had been no recent simulated intrusion. Moreover, there was more baseline territorial scent-marking and a higher likelihood of group fissioning in intrusion weeks. Consequently, individuals gained less body mass at the end of weeks with repeated simulated intrusions. Our experimental findings provide evidence for longer-term, extended and cumulative, effects of an elevated intergroup threat, which may lead to fitness consequences and underpin this powerful selective pressure.

An intergenerational androgenic mechanism of female intrasexual competition in the cooperatively breeding meerkat

Female intrasexual competition can be intense in cooperatively breeding species, with some dominant breeders (matriarchs) limiting reproduction in subordinates via aggression, eviction or infanticide. In males, such tendencies bidirectionally link to testosterone, but in females, there has been little systematic investigation of androgen-mediated behaviour within and across generations. In 22 clans of wild meerkats (Suricata suricatta), we show that matriarchs 1) express peak androgen concentrations during late gestation, 2) when displaying peak feeding competition, dominance behaviour, and evictions, and 3) relative to subordinates, produce offspring that are more aggressive in early development. Late-gestation antiandrogen treatment of matriarchs 4) specifically reduces dominance behaviour, is associated with infrequent evictions, decreases social centrality within the clan, 5) increases aggression in cohabiting subordinate dams, and 6) reduces offspring aggression. These effects implicate androgen-mediated aggression in the operation of female sexual selection, and intergenerational transmission of masculinised phenotypes in the evolution of meerkat cooperative breeding.

The Cost of Reproduction in a Cooperatively Breeding Mammal: Consequences of Seasonal Variation in Rainfall, Reproduction, and Reproductive Suppression

Biological investments, such as reproduction, are influenced by both biotic and abiotic factors and their interactions. The trade-off between reproduction and survival has been well established. Seasonally breeding species, therefore, may exhibit variations in these trade-offs, but there is a dearth of knowledge concerning this. This study investigated the physiological cost of reproduction (measured through oxidative stress) across seasons in the cooperatively breeding highveld mole-rat (Cryptomys hottentotus pretoriae), one of the few seasonal breeding mole-rats. Oxidative stress indicates elevated reactive oxygen species (ROS) levels, which can overwhelm antioxidant defences resulting in damaged proteins, lipids and DNA, which overall can reduce longevity and compromise reproduction. Oxidative markers such as total oxidant status (TOS-measure of total peroxides present), total antioxidant capacity (TAC), oxidative stress index (OSI), and malondialdehyde (MDA) are utilised to measure oxidative stress. In this study, breeding and non-breeding male (NBM) and female mole-rats were captured during the dry season (breeding period) and wet season (non-breeding period). There was an apparent cost of reproduction in the highveld mole-rat; however, the seasonality pattern to the cost of reproduction varied between the sexes. Breeding females (BFs) had significantly higher MDA during the breeding period/dry season in comparison to the non-breeding period/wet season; this is possibly a consequence of bearing and nursing offspring. Contrastingly, breeding males (BMs) showed increased oxidative damage in the non-breeding/wet season compared to the breeding/dry season, possibly due to increased activities of protecting their mating rights for the next breeding/dry season, but this was not significant. Interestingly, during the non-breeding period/wet season, non-breeding females (NBFs) are released from their reproductive suppression, which resulted in increases in TOS and OSI, which again indicated that just the mere ability to be able to breed results in a cost (oxidative stress). Therefore we can speculate that highveld mole-rats exhibited seasonal variation in redox balance brought about by variation in abiotic variables (e.g., rainfall), physiology and behaviour. We conclude that physiological changes associated with reproduction are sufficient to induce significant acute oxidative stress in the plasma of female highveld mole-rats, which become alleviated following transition to the non-breeding season/wet period suggesting a possible hormetic effect.

Environmental quality mediates the ecological dominance of cooperatively breeding birds

Species as diverse as humans and ants are among the most abundant organisms on Earth, partly because of their ability to form cooperative societies1-3. Yet, animals form groups for many reasons4,5, and how these differences affect their ‘social conquests’2 remains unknown. Here we use a theoretical model to demonstrate that the different fitness benefits that animals receive by forming groups4,6 depend on the quality of their environment, which in turn impacts their ecological dominance and resilience to global change. Our model predicts species that group because of environmental hardships will have wider ecological niches, larger geographic ranges, and higher abundances than non-social species, whereas those that group because of intraspecific resource competition will not. As predicted, an analysis of >1500 avian species finds that cooperative breeders occurring in harsh and fluctuating environments have larger ranges and higher abundances than non-cooperative breeders, whereas cooperative breeders occurring in benign and stable environments do not. These results are consistent with our model predictions showing that species cooperating in harsh or fluctuating environments will be less vulnerable to climate change than non-social species and those cooperating against intra-specific competitors in benign or stable environments. Ultimately, by combining macroecological and sociobiological perspectives, our study helps understand and predict the past, present, and future state of social species, including our own.

Mothers front-load their investment to the egg stage when helped in a wild cooperative bird

In many cooperative societies, including our own, helpers assist with the post-natal care of breeders' young, and may thereby benefit the post-natal development of offspring. Here we present evidence of a novel mechanism by which such post-natal helping could also have hitherto unexplored beneficial effects on pre-natal development: by lightening post-natal maternal workloads, helpers may allow mothers to increase their pre-natal investment per offspring. We present the findings of a decade-long study of cooperatively breeding white-browed sparrow weaver, Plocepasser mahali, societies. Within each social group, reproduction is monopolized by a dominant breeding pair, and non-breeding helpers assist with nestling feeding. Using a within-mother reaction norm approach to formally identify maternal plasticity, we demonstrate that when mothers have more female helpers they decrease their own post-natal investment per offspring (feed their nestlings at lower rates) but increase their pre-natal investment per offspring (lay larger eggs, which yield heavier hatchlings). That these plastic maternal responses are predicted by female helper number, and not male helper number, implicates the availability of post-natal helping per se as the likely driver (rather than correlated effects of group size), because female helpers feed nestlings at substantially higher rates than males. We term this novel maternal strategy 'maternal front-loading' and hypothesize that the expected availability of post-natal help allows helped mothers to focus maternal investment on the pre-natal phase, to which helpers cannot contribute directly. Such cryptic maternally mediated helper effects on pre-natal development may markedly complicate attempts to identify and quantify the fitness consequences of helping.

Sex-Specific Routes to Independent Breeding in a Polygynous Cooperative Breeder

How can individuals obtain a breeding position and what are the benefits associated with philopatry compared to dispersal? These questions are particularly intriguing in polygamous cooperative breeders, where dispersal strategies reflect major life history decisions, and routes to independent breeding may utterly differ between the sexes. We scrutinized sex-dependent life-history routes by investigating dispersal patterns, growth rates and mortality in a wild colony of the cooperatively breeding cichlid Neolamprologus savoryi. Our data reveal that female helpers typically obtain dominant breeding positions immediately after reaching sexual maturity, which is associated with strongly reduced growth. In contrast, males obtain breeder status only at twice the age of females. After reaching sexual maturity, males follow one of two strategies: (i) they may retain their subordinate status within the harem of a dominant male, which may provide protection against predators but involves costs by helping in territory maintenance, defence and brood care; or (ii) they may disperse and adopt a solitary status, which diminishes survival chances and apparently reflects a best-of-a-bad-job strategy, as there are no obvious compensating future fitness benefits associated with this pathway. Our study illustrates that sex-dependent life history strategies strongly relate to specific social structures and mating patterns, with important implications for growth rates, the age at which breeding status is obtained, and survival.