Delayed dispersal of sexually mature offspring is a fundamental component of cooperative breeding. In ambrosia beetles, female offspring temporarily remain in their natal nest and refrain from reproduction, instead investing in alloparental care. Previous work has demonstrated a link between helping behaviour and the increased need for pathogen defence, arising from their close association with fungal cultivars. In the ambrosia beetle Xyleborinus saxesenii, mature female offspring can effectively fight pathogen infections and manage the microbial composition within the nest by adjusting the frequency of different hygienic and nest maintenance behaviours. This suggests a potential to respond flexibly to the ecology of their nest, which calls for a better understanding of the connection between behaviour and the microbial community thriving within their nests. Here, we studied the significance of the mutualistic fungus garden composition for the beetles’ nest ecology and fitness by experimentally varying substrate quality. We found that the vertically transmitted ambrosia fungus garden is composed of at least two fungus mutualist species and a wide variety of other microbes varying in their relative abundance. This is strongly affected by the moisture content of the substrate, which in nature depends on the age and type of wood. We found that the mutualist fungi complement each other in terms of dryness-resistance, allowing the beetles to utilise a broad range of substrates over prolonged time during which the wood gradually desiccates. Under suboptimal humidity conditions, the interaction between host and multiple fungus species has important ramifications for the behaviour of philopatric helpers, including their alloparental investment, sibling cannibalism and the timing of dispersal. Rearing five generations of beetles consecutively in dry substrate resulted in transgenerational effects on philopatry and alloparental care, probably mediated through the dominance of a particular fungus species that was driven by the experimental habitat condition. Interestingly, the nests of these selection lines produced much more offspring after five generations than any first-generation nest, which may have reflected increased egg laying by non-dispersing daughters. Our study highlights the importance of considering the interactions between the microbial community and their insect hosts for understanding social evolution in cooperatively breeding beetles.

Kin competition often reduces – and sometimes entirely negates – the benefits of cooperation among family members. Surprisingly, the impact of kin competition on the fitness effects of family life only received close scrutiny in studies on sibling rivalry, whereas the possibility of parent–offspring competition has attracted much less attention. As a consequence, it remains unclear whether and how parent–offspring competition could have affected the early evolution of parental care and family life. Here, we examined the occurrence and consequences of parent–offspring competition over food access in the European earwig Forficula auricularia, an insect with facultative family life reminiscent of an ancestral state. Specifically, we (1) raised earwig offspring under food limitation either together with or without their mother, and (2) tested whether and how the — potentially competitive — weight gains of mothers and offspring during family life affected the offsprings' survival rate and morphology, and the future reproductive investment of their mother. In line with the occurrence of parent–offspring competition, we showed that high maternal weight gains during family life reduced the survival prospects of maternally tended offspring, while they increased the mothers' investment into the production of a second clutch (but not the body size of the surviving offspring). Conversely, high offspring weight gains generally increased the offsprings' survival, but did so to a larger extent when they were together with their mother. Intriguingly, mothers that had exhibited a low initial weight showed especially high weight gains. Overall, our results demonstrate that maternal presence under food restriction triggered a local competition between mothers and their offspring. This competition limited offspring survival, but allowed mothers to increase their investment into future reproduction and/or to maintain their current body condition. On a general level, our findings reveal that parent–offspring competition can counteract the benefits of (facultative) parental care, and may thus impede the evolution of family life in resource‐poor environments. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12915/suppinfo is available for this article.

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Pathogens are ubiquitous in nature and typically entail major fitness costs in their hosts. These costs can be particularly important when individuals exhibit poor immune defences, as it is often the case during early developmental stages. Hence, selection should favor parental strategies limiting the risks of pathogen exposure and infection in their offspring. In this study, we investigated (1) whether females of the European earwig Forficula auricularia avoid areas contaminated with spores of the entomopathogenic fungus Metarhizium brunneum prior to and at egg laying, as well as (2) whether spore presence entails an increase in females' investment into both pre-hatching forms of care and clutch quantity and quality. Our results first show that females did not avoid contaminated areas prior to and at egg laying. However, females returned to their eggs faster in presence of living spores compared to UV-killed or no spores. They were also more likely to construct a nest when in presence of both living and UVkilled spores (but only in one studied population). Finally, we found that spore presence did not influence maternal investment into egg grooming, egg gathering and egg defence, as well as into clutch quantity and quality. Overall, our results demonstrate that earwig females do not avoid contaminated environments, but could mitigate the associated costs of pathogen exposure by adjusting their level of egg care. These findings emphasize the importance of pathogens in the evolution of pre-hatching parental care and, more generally, in the emergence and maintenance of family life in nature.

BackgroundSocial animals have the unique capability of mounting social defenses against pathogens. Over the last decades, social immunity has been extensively studied in species with obligatory and permanent forms of social life. However, its occurrence in less derived social systems and thus its role in the early evolution of group-living remains unclear. Here, we investigated whether lining nests with feces is a form of social immunity against microbial growth in the European earwig Forficula auricularia, an insect with temporary family life and facultative maternal care.ResultsUsing a total of 415 inhibition zone assays, we showed that earwig feces inhibit the growth of two GRAM+ bacteria, two fungi, but not of a GRAM- bacteria. These inhibitions did not result from the consumed food or the nesting environment. We then demonstrated that the antimicrobial activity against fungus was higher in offspring than maternal feces, but that this difference was absent against bacteria. Finally, we showed that family interactions inhibited the antibacterial activity of maternal feces against one of the two GRAM+ bacteria, whereas it had no effect on the one of nymphal feces. By contrast, antifungal activities of the feces were independent of mother-offspring interactions.ConclusionThese results demonstrate that social immunity occurs in a species with simple and facultative social life, and thus shed light on the general importance of this process in the evolution of group-living. These results also emphasize that defecation can be under selection for other life-history traits than simple waste disposal.