Cryptic recessive lethality of a supergene controlling social organization in ants.

Supergenes are clusters of linked loci that control complex phenotypes, such as alternative forms of social organization in ants. Explaining the long-term maintenance of supergenes is challenging, particularly when the derived haplotype lacks homozygous lethality and causes gene drive. In the Alpine silver ant, Formica selysi, a large and ancient social supergene with two haplotypes, M and P, controls colony social organization. Single-queen colonies only contain MM females, while multiqueen colonies contain MP and PP females. The derived P haplotype, found only in multiqueen colonies, selfishly enhances its transmission through maternal effect killing, which could have led to its fixation. A population genetic model showed that a stable social polymorphism can only be maintained under a narrow set of conditions, which includes partial assortative mating by social form (which is known to occur in the wild), and low fitness of PP queens. With a combination of field and laboratory experiments, we show that the P haplotype has deleterious effects on female fitness. The survival rate of PP queens and workers was around half that of other genotypes. Moreover, P-carrying queens had lower fertility and fecundity compared to other queens. We discuss how cryptic lethal effects of the P haplotype help stabilize this ancient polymorphism.

Socially transferred materials: why and how to study them.

When biological material is transferred from one individual's body to another, as in ejaculate, eggs, and milk, secondary donor-produced molecules are often transferred along with the main cargo, and influence the physiology and fitness of the receiver. Both social and solitary animals exhibit such social transfers at certain life stages. The secondary, bioactive, and transfer-supporting components in socially transferred materials have evolved convergently to the point where they are used in applications across taxa and type of transfer. The composition of these materials is typically highly dynamic and context dependent, and their components drive the physiological and behavioral evolution of many taxa. Our establishment of the concept of socially transferred materials unifies this multidisciplinary topic and will benefit both theory and applications.

Disentangling the mechanisms linking dispersal and sociality in supergene-mediated ant social forms.

The coevolution between dispersal and sociality can lead to linked polymorphisms in both traits, which may favour the emergence of supergenes. Supergenes have recently been found to control social organization in several ant lineages. Whether and how these 'social supergenes' also control traits related to dispersal is yet unknown. Our goal here was to get a comprehensive view of the dispersal mechanisms associated with supergene-controlled alternative social forms in the ant Formica selysi. We measured the production and emission of young females and males by single-queen (monogyne) and multiple-queen (polygyne) colonies, the composition of mating aggregations, and the frequency of crosses within and between social forms in the wild. We found that males and females from alternative social forms did not display strong differences in their propensity to leave the nest and disperse, nor in their mating behaviour. Instead, the social forms differed substantially in sex allocation. Monogyne colonies produced 90% of the females flying to swarms, whereas 57% of the males in swarms originated from polygyne colonies. Most crosses were assortative with respect to social form. However, 20% of the monogyne females did mate with polygyne males, which is surprising as this cross has never been found in mature monogyne colonies. We suggest that the polygyny-determining haplotype free rides on monogyne females, who establish independent colonies that later become polygyne. By identifying the steps in dispersal where the social forms differ, this study sheds light on the behavioural and colony-level traits linking dispersal and sociality through supergenes.

Cooperation by ant queens during colony-founding perpetuates alternative forms of social organization.

ABSTRACT: Key social traits, like queen number in eusocial insect colonies, have long been considered plastic, but the recent finding that colony social organization is under strict genetic control in multiple ant lineages challenges this view. This begs the question of which hardwired behavioral mechanism(s) generate alternative forms of social organization during colony development. We addressed this question in the Alpine silver ant, Formica selysi, a species with two social forms determined by a supergene. Queens that carry exclusively the M haplotype are produced by and live in monogyne (= single-queen) colonies, whereas queens that carry at least one copy of the P haplotype are produced by and live in polygyne (= multiple-queen) colonies. With extensive field samplings and laboratory experiments, we show that both types of queens successfully establish colonies independently, without being accompanied by workers, but that they do so in contrasting ways. Monogyne queens were generally intolerant of other queens and founded colonies solitarily, whereas polygyne queens were mutually attracted to each other and mainly founded colonies cooperatively. These associations persisted for months after worker emergence, suggesting that cooperative colony-founding leads to permanent multiple queening. Overall, our study shows that queens of each social form found colonies independently in the field but that P-carrying queens are more likely to cooperate, thereby contributing to perpetuate alternative forms of social organization. SIGNIFICANCE STATEMENT: Understanding the genetic and behavioral underpinnings of social organization is a major goal in evolutionary biology. Recent studies have shown that colony social organization is controlled by supergenes in multiple ant lineages. But the behavioral processes linking the genotype of a queen to the type of colony she will form remain largely unknown. Here, we show that in Alpine silver ants, alternative supergene genotypes are associated with different levels of social attraction and tolerance in young queens. These hardwired differences in social traits make queens carrying the P supergene haplotype more prone to cooperate and form durable associations during independent colony-founding. These findings help explain how genetic variants induce alternative forms of social organization during the ontogeny of a colony. They also illustrate how simple phenotypic differences at the individual level can result in large differences at higher levels of organization. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00265-021-03105-1.

Winter is coming: harsh environments limit independent reproduction of cooperative-breeding queens in a socially polymorphic ant.

Cooperative breeding animals frequently inhabit harsh environments. It is widely accepted that harsh environments hinder independent reproduction, and this constraint maintains individuals in family groups. Yet the assumption that harsh ecological conditions reduce the success of members of cooperative breeding groups when breeding independently has not been experimentally tested. We addressed this shortcoming using the socially polymorphic Alpine silver ant, Formica selysi. This species has single-queen (independent breeders) and multiple-queen (cooperative breeders) colonies coexisting within populations. We placed newly mated queens emerging from each type of colony to breed alone in either a harsh or mild winter condition and recorded their brood production and survival. Queens emerging from single-queen colonies were unaffected by the winter condition and were more successful at founding a nest independently than queens from multiple-queen colonies. By contrast, queens from multiple-queen colonies had higher mortality after a harsh than after a mild winter. These results support the long-held assumption that harsh environments constrain independent reproduction of members of cooperative breeding groups.

The early-life environment and individual plasticity in life-history traits.

We tested whether the early-life environment can influence the extent of individual plasticity in a life-history trait. We asked: can the early-life environment explain why, in response to the same adult environmental cue, some individuals invest more than others in current reproduction? Moreover, can it additionally explain why investment in current reproduction trades off against survival in some individuals, but is positively correlated with survival in others? We addressed these questions using the burying beetle, which breeds on small carcasses and sometimes carries phoretic mites. These mites breed alongside the beetle, on the same resource, and are a key component of the beetle's early-life environment. We exposed female beetles to mites twice during their lives: during their development as larvae and again as adults during their first reproductive event. We measured investment in current reproduction by quantifying average larval mass and recorded the female's life span after breeding to quantify survival. We found no effect of either developing or breeding alongside mites on female reproductive investment, nor on her life span, nor did developing alongside mites influence her size. In post hoc analyses, where we considered the effect of mite number (rather than their mere presence/absence) during the female's adult breeding event, we found that females invested more in current reproduction when exposed to greater mite densities during reproduction, but only if they had been exposed to mites during development as well. Otherwise, they invested less in larvae at greater mite densities. Furthermore, females that had developed with mites exhibited a trade-off between investment in current reproduction and future survival, whereas these traits were positively correlated in females that had developed without mites. The early-life environment thus generates individual variation in life-history plasticity. We discuss whether this is because mites influence the resources available to developing young or serve as important environmental cues.

No evidence of a cleaning mutualism between burying beetles and their phoretic mites.

Burying beetles (Nicrophorus vespilloides) breed on small vertebrate carcasses, which they shave and smear with antimicrobial exudates. Producing antimicrobials imposes a fitness cost on burying beetles, which rises with the potency of the antimicrobial defence. Burying beetles also carry phoretic mites (Poecilochirus carabi complex), which breed alongside them on the carcass. Here we test the novel hypothesis that P. carabi mites assist burying beetles in clearing the carcass of bacteria as a side-effect of grazing on the carrion. We manipulated the bacterial environment on carcasses and measured the effect on the beetle in the presence and absence of mites. With next-generation sequencing, we investigated how mites influence the bacterial communities on the carcass. We show that mites: 1) cause beetles to reduce the antibacterial activity of their exudates but 2) there are no consistent fitness benefits of breeding alongside mites. We also find that mites increase bacterial diversity and richness on the carcass, but do not reduce bacterial abundance. The current evidence does not support a cleaning mutualism between burying beetles and P. carabi mites, but more work is needed to understand the functional significance and fitness consequences for the beetle of mite-associated changes to the bacterial community on the carcass.

Fitness costs associated with building and maintaining the burying beetle's carrion nest.

It is well-known that features of animal nest architecture can be explained by fitness benefits gained by the offspring housed within. Here we focus on the little-tested suggestion that the fitness costs associated with building and maintaining a nest should additionally account for aspects of its architecture. Burying beetles prepare an edible nest for their young from a small vertebrate carcass, by ripping off any fur or feathers and rolling the flesh into a rounded ball. We found evidence that only larger beetles are able to construct rounder carcass nests, and that rounder carcass nests are associated with lower maintenance costs. Offspring success, however, was not explained by nest roundness. Our experiment thus provides rare support for the suggestion that construction and maintenance costs are key to understanding animal architecture.

Interspecific Interactions and the Scope for Parent-Offspring Conflict: High Mite Density Temporarily Changes the Trade-Off between Offspring Size and Number in the Burying Beetle, Nicrophorus vespilloides.

Parents have a limited amount of resources to invest in reproduction and commonly trade-off how much they invest in offspring size (or quality) versus brood size. A negative relationship between offspring size and number has been shown in numerous taxa and it underpins evolutionary conflicts of interest between parents and their young. For example, previous work on vertebrates shows that selection favours mothers that produce more offspring, at the expense of individual offspring size, yet favours offspring that have relatively few siblings and therefore attain a greater size at independence. Here we analyse how this trade-off is temporarily affected by stochastic variation in the intensity of interspecific interactions. We examined the effect of the mite Poecilochirus carabi on the relationship between offspring size and number in the burying beetle, Nicrophorus vespilloides. We manipulated the initial number of mites in the reproductive event (by introducing either no mites, 4 mites, 10 mites, or 16 mites), and assessed the effect on the brood. We found a similar trade-off between offspring size and number in all treatments, except in the '16 mite' treatment where the correlation between offspring number and size flattened considerably. This effect arose because larvae in small broods failed to attain a high mass by dispersal. Our results show that variation in the intensity of interspecific interactions can temporarily change the strength of the trade-off between offspring size and number. In this study, high densities of mites prevented individual offspring from attaining their optimal weight, thus potentially temporarily biasing the outcome of parent-offspring conflict in favour of parents.

Social immunity of the family: parental contributions to a public good modulated by brood size.

Social immunity refers to any immune defence that benefits others, besides the individual that mounts the response. Since contributions to social immunity are known to be personally costly, they are contributions to a public good. However, individuals vary in their contributions to this public good and it is unclear why. Here we investigate whether they are responding to contributions made by others with experiments on burying beetle (Nicrophorus vespilloides) families. In this species, females, males and larvae each contribute to social immunity through the application of antimicrobial exudates upon the carrion breeding resource. We show experimentally that mothers reduce their contributions to social immunity when raising large broods, and test two contrasting hypotheses to explain why. Either mothers are treating social immunity as a public good, investing less in social immunity when their offspring collectively contribute more, or mothers are trading off investment in social immunity with investment in parental care. Overall, our experiments yield no evidence to support the existence of a trade-off between social immunity and other parental care traits: we found no evidence of a trade-off in terms of time allocated to each activity, nor did the relationship between social immunity and brood size change with female condition. Instead, and consistent with predictions from models of public goods games, we found that higher quality mothers contributed more to social immunity. Therefore our results suggest that mothers are playing a public goods game with their offspring to determine their personal contribution to the defence of the carrion breeding resource.

Friend or foe: inter-specific interactions and conflicts of interest within the family.

Interactions between species can vary from mutually beneficial to evolutionarily neutral to antagonistic, even when the same two species are involved. Similarly, social interactions between members of the same species can lie on a spectrum from conflict to cooperation.The aim of the present study was to investigate whether variation in the two types of social behaviour are interconnected. Is the fitness of the various classes of social partner within species (such as parent and offspring, or male and female) differently affected by interactions with a second species? Moreover, can inter-specific interactions influence the outcome of social interactions within species?The present experiments focus on the interactions between the burying beetle Nicrophorus vespilloides Herbst and the phoretic mite Poecilochirus carabi G. Canestrini & R. Canestrini. The approach was to measure the fitness of burying beetle mothers, fathers, and offspring after reproduction, which took place either in the presence or absence of mites.We found that male, female, and larval burying beetles derive contrasting fitness costs and benefits from their interactions with the mite, despite sharing a common family environment. From the mite's perspective, its relationship with the burying beetle can, therefore, be simultaneously antagonistic, neutral, and possibly even mutualistic, depending on the particular family member involved. We also found that mites can potentially change the outcome of evolutionary conflicts within the family.We conclude that inter-specific interactions can explain some of the variation in social interactions seen within species. It is further suggested that intra-specific interactions might contribute to variation in the outcome of interactions between species.

Parental effects alter the adaptive value of an adult behavioural trait.

The parents' phenotype, or the environment they create for their young, can have long-lasting effects on their offspring, with profound evolutionary consequences. Yet, virtually no work has considered how such parental effects might change the adaptive value of behavioural traits expressed by offspring upon reaching adulthood. To address this problem, we combined experiments on burying beetles (Nicrophorus vespilloides) with theoretical modelling and focussed on one adult behavioural trait in particular: the supply of parental care. We manipulated the early-life environment and measured the fitness payoffs associated with the supply of parental care when larvae reached maturity. We found that (1) adults that received low levels of care as larvae were less successful at raising larger broods and suffered greater mortality as a result: they were low-quality parents. Furthermore, (2) high-quality males that raised offspring with low-quality females subsequently suffered greater mortality than brothers of equivalent quality, which reared larvae with higher quality females. Our analyses identify three general ways in which parental effects can change the adaptive value of an adult behavioural trait: by influencing the associated fitness benefits and costs; by consequently changing the evolutionary outcome of social interactions; and by modifying the evolutionarily stable expression of behavioural traits that are themselves parental effects.

Interspecific interactions explain variation in the duration of paternal care in the burying beetle.

Why is there so much variation within species in the extent to which males contribute to offspring care? Answers to this question commonly focus on intraspecific sources of variation in the relative costs and benefits of supplying paternal investment. With experiments in the laboratory on the burying beetle, Nicrophorus vespilloides, and its phoretic mite Poecilochirus carabi, we investigated whether interactions with a second species might also account for intraspecific variation in the extent of paternal care, and whether this variation is due to adaptation or constraint. In our first experiment we bred beetles in the presence or absence of phoretic mites, using a breeding box that mimicked natural conditions by allowing parents to leave the breeding attempt at a time of their choosing. We found that males abandoned their brood sooner when breeding alongside mites than when breeding in their absence. Female patterns of care were unchanged by the mites. Nevertheless, in this experiment, no correlates of beetle fitness were affected by the presence of the mites during reproduction (neither paternal life span after reproduction nor brood size or average larval mass). In a second experiment, we again bred beetles with or without mites but this time we prevented parents from abandoning the brood. This time we found that both parents and the brood suffered fitness costs when breeding alongside mites, compared with families breeding in the absence of mites. We conclude that males adaptively reduce their contributions to care when mites are present, so as to defend their offspring's fitness and their own residual fitness. Interspecific interactions thus account for intraspecific variation in the duration of paternal care.

Interspecific interactions change the outcome of sexual conflict over prehatching parental investment in the burying beetle Nicrophorus vespilloides.

Sexual conflict arises when the optimal reproductive strategy differs for males and females. It is associated with every reproductive stage, yet few studies have considered how the outcome may be changed by interactions with other species. Here, we show that phoretic mites Poecilochirus carabi change the outcome of sexual conflict over the supply of prehatching parental investment in the burying beetle Nicrophorus vespilloides. Burying beetles require a small dead vertebrate for reproduction, which they prepare by shaving it, rolling up the flesh, and burying it. When pairs were given a medium-sized mouse to prepare (13-16 g), mites changed how the costs of reproduction were divided between the sexes, with males then sustaining greater costs than females. We found no equivalent difference when pairs prepared larger or smaller carcasses. Thus, our experiment shows that the outcome of sexual conflict over prehatching parental investment is changed by interactions with other species during reproduction.