Better together:Cooperative breeding under environmental heterogeneity

Cooperative breeding – where more than two individuals engage in rearing offspring – has historically been attributed to a lack of independent breeding opportunities and high levels of within-group relatedness. However, cooperation often occurs between non-relatives and in non-saturated environments, suggesting alternative evolutionary causes of cooperative breeding. Environmental conditions can strongly influence the evolution of cooperative breeding, for instance when low food availability or high predation risk affects the costs of dispersal, or when cooperation under such conditions is necessary to successfully raise young. In this thesis, I investigate the relationship between environmental conditions and important components of cooperative breeding, using two distinct systems: the Seychelles warbler Acrocephalus sechellensis and the social cichlid Neolamprologus pulcher. This study offers three main conclusions. First, I argue that predation risk, while acknowledged as an important factor promoting group-living, is also an important driver of cooperative breeding and social complexity. Second, cooperative breeding has been suggested to function as a bet-hedging strategy, where groups allow reproduction under adverse conditions such as low food abundance. I show that this conclusion might be premature and that periods of low food abundance may lead to group formation, but not to cooperative breeding per se. Third, while subordinates in cooperative breeders have been suggested to make the best of a bad job, I argue that these conclusions may change if the ecological and environmental conditions under which breeding occurs are considered. Together, this thesis shows the importance of the environment and ecology for the evolution of cooperative breeding in vertebrates

Experimentally induced antipredator responses are mediated by social and environmental factors

Nest predation is a common cause of reproductive failure for many bird species, and various antipredator defense behaviors have evolved to reduce the risk of nest predation. However, trade-offs between current reproductive duties and future reproduction often limit the parent’s ability to respond to nest predation risk. Individual responses to experimentally increased nest predation risk can give insights into these trade-offs. Here, we investigate whether social and ecological factors affect individual responses to predation risk by experimentally manipulating the risk of nest predation using taxidermic mounts in the cooperative breeding Seychelles warbler (Acrocephalus sechellensis). Our results show that dominant females, but not males, alarm called more often when they confront a nest predator model alone than when they do so with a partner, and that individuals that confront a predator together attacked more than those that did so alone. Dominant males increased their antipredator defense by spending more time nest guarding after a presentation with a nest predator, compared with a nonpredator control, but no such effect was found for females, who did not increase the time spent incubating. In contrast to incubation by females, nest guarding responses by dominant males depended on the presence of other group members and food availability. These results suggest that while female investment in incubation is always high and not dependent on social and ecological conditions, males have a lower initial investment, which allows them to respond to sudden changes in nest predation risk

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

1. 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. 2. 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. 3. 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. 4. 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 co-breeders, 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. 5. 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

Extra-pair mating opportunities mediate parenting and mating effort trade-offs in a songbird

In socially monogamous species with bi-parental care, males may face a trade-off between providing parental care and pursuing extra-pair matings. The "parenting-mating trade-off" hypothesis predicts that high-quality males-who have greater potential to gain extra-pair matings, for example, larger males usually win the competition for extra-pair mating-should reduce parental care and spend more time looking for extra-pair matings. However, the trade-off between parenting and mating efforts may be complicated by variation in the availability of extra-pair mating opportunities. By using field data of hair-crested drongos (Dicrurus hottentottus), a species exhibiting bi-parental incubation behavior, collected in central China from 2010 to 2017, we tested whether the potential negative relationship between male quality and paternal care was dependent on the number of nearby fertile females. We found that male drongos mainly seek extra-pair matings during the incubation period and high-quality individuals (males with longer tarsi) are more likely to sire extra-pair offspring. In agreement with the "parenting-mating trade-off" hypothesis, high-quality males incubated less by recessing longer between incubation bouts. However, this was only the case when sufficient fertile females nearby for extra-pair mating opportunities. Females compensated for reduced male care, but this was independent of male quality. This suggests that the reduction in care by high-quality males might be a direct response to extra-pair mating opportunities rather than facilitated by differential allocation of females. Our results indicate that individual quality and available mating opportunities may shape the optimal trade-off between parental care and seeking additional matings for males. Lay Summary: How do individual quality and the number of potential extra-pair mates influence the optimal trade-off between parental care and engaging extra-pair courtship in animals? In hair-crested drongos, high-quality males, who are more successful in obtaining extra-pair fertilizations, reduced their share in incubation, but only when they had sufficient extra-pair mating opportunities. Females partially compensate for the reduced incubation of their partners, but the compensation was not affected by male quality

Group-size-dependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay

In cooperative breeding systems, dominant breeders sometimes tolerate unrelated individuals even if they inflict costs on the dominants. According to the 'pay-to-stay' hypothesis, (i) subordinates can outweigh these costs by providing help and (ii) dominants should be able to enforce help by punishing subordinates that provide insufficient help. This requires that dominants can monitor helping and can recognize group members individually. In a field experiment, we tested whether cooperatively breeding cichlid Neolamprologus pulcher subordinates increase their help after a forced 'idle' period, how other group members respond to a previously idle helper, and how helper behaviour and group responses depend on group size. Previously, idle helpers increased their submissiveness and received more aggression than control helpers, suggesting that punishment occurred to enforce help. Subordinates in small groups increased their help more than those in large groups, despite receiving less aggression. When subordinates were temporarily removed, dominants in small groups were more likely to evict returning subordinates. Our results suggest that only in small groups do helpers face a latent threat of punishment by breeders as predicted by the pay-to-stay hypothesis. In large groups, cognitive constraints may prevent breeders from tracking the behaviour of a large number of helpers

Pregnancy reduces concurrent pup care behaviour in meerkats, generating differences between dominant and subordinate females

DATA AVAILABILITY : Data available from the Dryad Digital Repository:https://doi.org/10.5061/dryad.gxd2547rf (Rotics et al., 2023).SUPPORTING INFORMATION: TABLES S1a- b. Pregnancy status effects on individual relative contribution to pup provisioning - results of a GLMM and post-hoc comparisons. TABLES S2a- b. Pregnancy status effects on individual relative contribution to guarding - results of a GLMM and post-hoc comparisons. TABLES S3a- b. Pregnancy status effects on babysitting- results of a GLMM and post-hoc comparisons. TABLE S4. Pregnancy status effects on the proportion of food items that females donated to pups (generosity)- results of a GLMM. Table S5. Changes throughout pregnancy days in relative individual contribution to provision modelled using GAMM. TABLE S6. Changes throughout pregnancy days in body weight (g) modelled using GAMM. TABLE S7. The effect of being pregnant while lactating (yes/no) on lactation duration - results of an LMM. TABLE S8. Rank (dominant/subordinate) differences in the probability of being pregnant (yes/no) during the pup-provisioning period - results of a GLMM. TABLE S9. Subordinates contraception experiment: comparisons of cooperative behaviours between subordinate females treated with contraceptive jab versus control subordinate females (saline jab). TABLE S10. Pregnant females feeding experiment: comparisons of cooperative behaviours between late pregnant dominant females that were provided with food supplement versus control unfed dominant females. TABLE S11. Pregnancy status effects on individual absolute contributions to provisioning and guarding - results of two separate GLMMs. This table summarizes the results of repeating the analyses conducted on relative contributions to provisioning and guarding (Tables S1 and S2) with analyses on absolute contributions. FIGURE S1. Pregnancy effects on absolute contributions to cooperative behaviours. This figure is equivalent to Figure 1a,b in the manuscript but presents absolute contributions rather than relative ones.   FIGURE S2. Effects of pregnancy-related, experimental manipulations on individual absolute contributions to provisioning. This figure is equivalent to Figure 3 in the manuscript but presents absolute contributions rather than relative ones.    FIGURE S3. Differences between dominants (DOM) and subordinates (SUB) in cooperative behaviours (provisioning, guarding and babysitting) without accounting for pregnancy status.1. In some mammals, and particularly in cooperative breeding ones, successive bouts of reproduction can overlap so that a female is often pregnant while still nurturing dependent young from her previous litter. Such an overlap requires fe-males to divide their energetic budget between two reproductive activities, and pregnancy costs would consequently be expected to reduce investment in con-current offspring care. However, explicit evidence for such reductions is scarce, and the potential effects they may have on work division in cooperative breeders have not been explored. 2.Using 25 years of data on reproduction and cooperative behaviour in wild Kalahari meerkats, supplemented with field experiments, we investigated whether pregnancy's reduces contributions to cooperative pup care behaviours, including babysitting, provisioning and raised guarding. We also explored whether pregnancy, which is more frequent in dominants than subordinates, could account for the reduced contributions of dominants to the cooperative pup care behaviours. 3. We found that pregnancy, particularly at late stages of gestation, reduces con-tributions to cooperative pup care; that these reductions are eliminated when the food available to pregnant females is experimentally supplemented; and that pregnancy effects accounted for differences between dominants and subordi-nates in two of the three cooperative behaviours examined (pup provisioning and raised guarding but not babysitting). 4. By linking pregnancy costs with reductions in concurrent pup care, our findings illuminate a trade-off between investment in successive, overlapping bouts of reproduction. They also suggest that some of the differences in cooperative behaviour between dominant and subordinate females in cooperative breeding mammals can be a direct consequence of differences in their breeding frequency.European Research Council; Human Frontier Science Program; University of Zurich; MAVA Foundation; Swiss National Science Foundation; Northern Cape Department of Environment and Nature Conservation.http://www.wileyonlinelibrary.com/journal/janeMammal Research InstituteZoology and Entomolog