Cooperative interactions within the family enhance the capacity for evolutionary change in body size.
ABSTRACT: Classical models of evolution seldom predict the rate at which populations evolve in the wild. One explanation is that the social environment affects how traits change in response to natural selection. Here, we determine how social interactions between parents and offspring, and among larvae, influence the response to experimental selection on adult size. Our experiments focus on burying beetles (Nicrophorus vespilloides), whose larvae develop within a carrion nest. Some broods exclusively self-feed on the carrion while others are also fed by their parents. We found populations responded to selection for larger adults but only when parents cared for their offspring. We also found populations responded to selection for smaller adults too, but only by removing parents and causing larval interactions to exert more influence on eventual adult size. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genus Nicrophorus are associated with the obligate provision of care. Synthesising our results with previous studies, we suggest that cooperative social environments enhance the response to selection whereas excessive conflict can prevent further directional selection.
Project description:Although cooperative social interactions within species are considered an important driver of evolutionary change, few studies have experimentally demonstrated that they cause adaptive evolution. Here we address this problem by studying the burying beetle Nicrophorus vespilloides. In this species, parents and larvae work together to obtain nourishment for larvae from the carrion breeding resource: parents feed larvae and larvae also self-feed. We established experimentally evolving populations in which we varied the assistance that parents provided for their offspring and investigated how offspring evolved in response. We show that in populations where parents predictably supplied more care, larval mandibles evolved to be smaller in relation to larval mass, and larvae were correspondingly less self-sufficient. Previous work has shown that antagonistic social interactions can generate escalating evolutionary arms races. Our study shows that cooperative interactions can yield the opposite evolutionary outcome: when one party invests more, the other evolves to invest less.
Project description:There is growing interest in how environmental conditions, such as resource availability, can modify the severity of inbreeding depression. However, little is known about whether inbreeding depression is also associated with differences in individual decision-making. For example, decisions about how many offspring to produce are often based upon the prevailing environmental conditions, such as resource availability, and getting these decisions wrong may have important fitness consequences for both parents and offspring. We tested for effects of inbreeding on individual decision-making in the burying beetle Nicrophorus vespilloides, which uses the size of a carrion resource to make decisions about number of offspring. Both inbred and outbred females adjusted their initial decisions about number of eggs to lay based on carcass size. However, when we forced individuals to update this initial decision by providing them with a different-sized carcass partway through reproduction, inbred females failed to update their decision about how many larvae to cull. Consequently, inbred females reared too many larvae, resulting in negative fitness consequences in the form of smaller offspring and reduced female post-reproductive condition. Our study provides novel insights into the effects of inbreeding by showing that poor decision-making by inbred individuals can negatively affect fitness.
Project description:In animal families, parents are expected to adapt to their offspring's traits, and offspring, in turn, are expected to adapt to the environment circumscribed by their parents. However, whether such coevolutionary trajectories differ between closely related species is poorly understood. Here, we employ interspecific cross-fostering in three species of burying beetles, Nicrophorus orbicollis, Nicrophorus pustulatus and Nicrophorus vespilloides, to test for divergent co-adaptation among species with different degrees of offspring dependency on parental care, and to test whether they are able to discriminate against interspecific parasites. We found that offspring survival was always higher when offspring were reared by conspecific rather than heterospecific parents. In the case of N. orbicollis raising N. pustulatus, none of the larvae survived. Overall, these results indicate that parent and offspring traits have diverged between species, and that the differential survival of conspecific and heterospecific larvae is because of improper matching of co-adapted traits, or, in the case of N. orbicollis with larval N. pustulatus, because of selection on parents to recognize and destroy interspecific brood parasites. We suggest that burying beetles experiencing a high risk of brood parasitism have evolved direct recognition mechanisms that enable them to selectively kill larvae of potential brood parasites.
Project description:Carrion beetles in the genus Nicrophorus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch care only, and no care), we found that larvae receiving full care are predominantly colonized by bacteria resident in the maternal gut while larvae receiving no care are colonized with bacteria from the carcass. More importantly, larvae receiving only prehatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in Nicrophorus vespilloides and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.IMPORTANCE Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle Nicrophorus vespilloides This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses, where they are exposed to high densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation but are recolonized apparently from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further suggest that competitive interactions mediate the bacterial composition of Nicrophorus larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.
Project description: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.
Project description:Models of "plasticity-first" evolution are attractive because they explain the rapid evolution of new complex adaptations. Nevertheless, it is unclear whether plasticity can facilitate rapid microevolutionary change between diverging populations. Here, we show how plasticity may have generated adaptive differences in fecundity between neighboring wild populations of burying beetles Nicrophorus vespilloides. These populations occupy distinct Cambridgeshire woodlands that are just 2.5 km apart and that probably originated from a common ancestral population about 1000-4000 years ago. We find that populations are divergently adapted to breed on differently sized carrion. Adaptive differences in clutch size and egg size are associated with divergence at loci connected with oogenesis. The populations differ specifically in the elevation of the reaction norm linking clutch size to carrion size (i.e., genetic accommodation), and in the likelihood that surplus offspring will be lost after hatching. We suggest that these two processes may have facilitated rapid local adaptation on a fine-grained spatial scale.
Project description: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.
Project description:Sibling rivalry is commonplace within animal families, yet offspring can also work together to promote each other's fitness. Here we show that the extent of parental care can determine whether siblings evolve to compete or to cooperate. Our experiments focus on the burying beetle Nicrophorus vespilloides, which naturally provides variable levels of care to its larvae. We evolved replicate populations of burying beetles under two different regimes of parental care: Some populations were allowed to supply posthatching care to their young (Full Care), while others were not (No Care). After 22 generations of experimental evolution, we found that No Care larvae had evolved to be more cooperative, whereas Full Care larvae were more competitive. Greater levels of cooperation among larvae compensated for the fitness costs caused by parental absence, whereas parental care fully compensated for the fitness costs of sibling rivalry. We dissected the evolutionary mechanisms underlying these responses by measuring indirect genetic effects (IGEs) that occur when different sibling social environments induce the expression of more cooperative (or more competitive) behavior in focal larvae. We found that indirect genetic effects create a tipping point in the evolution of larval social behavior. Once the majority of offspring in a brood start to express cooperative (or competitive) behavior, they induce greater levels of cooperation (or competition) in their siblings. The resulting positive feedback loops rapidly lock larvae into evolving greater levels of cooperation in the absence of parental care and greater levels of rivalry when parents provide care.
Project description:The fitness and virulence of parasites is often determined by how many resources they can wrangle out of their hosts. Host defenses that help to keep resources from the parasites will then reduce virulence and parasite fitness. Here, we study whether host brood care and brood size regulation can protect host fitness and harm a parasite. We use the biparental brood-caring burying beetle Nicrophorus vespilloides and its phoretic Poecilochirus carabi mites as a model. Since paternal brood care does not seem to benefit the offspring in a clean laboratory setting, the male presence has been suggested to strengthen the defense against parasites. We manipulated male presence and found no effect on the fitness of the parasitic mites or the beetle offspring. We further manipulated beetle brood size and found larger broods to reduce parasite fitness. The specific pattern we observed suggests that beetle larvae are strong competitors and consume the carrion resource before all parasites develop. They thus starve the parasites. These results shed new light on the observation that the parasites appear to reduce host brood size early on-potentially to avert later competition their offspring might have to face.
Project description:The evolution of elaborate forms of parental care is an important topic in behavioral ecology, yet the factors shaping the evolution of complex suites of parental and offspring traits are poorly understood. Here, we use a multivariate quantitative genetic approach to study phenotypic and genetic correlations between parental and offspring traits in the burying beetle Nicrophorus vespilloides. To this end, we recorded 2 prenatal traits (clutch size and egg size), 2 postnatal parental behaviors (direct care directed toward larvae and indirect care directed toward resource maintenance), 1 offspring behavior (begging), and 2 measures of breeding success (larval dispersal mass and number of dispersing larvae). Females breeding on larger carcasses provided less direct care but produced larger larvae than females breeding on smaller carcasses. Furthermore, there were positive phenotypic correlations between clutch size, direct, and indirect care. Both egg size and direct care were positively correlated with dispersal mass, whereas clutch size was negatively correlated with dispersal mass. Clutch size and number of dispersed larvae showed genetic variance both in terms of differences between populations of origin and significant heritabilities. However, we found no evidence of genetic variance underlying other parental or offspring traits. Our results suggest that correlations between suites of parental traits are driven by variation in individual quality rather than trade-offs, that some parental traits promote offspring growth while others increase the number of offspring produced, and that parental and offspring traits might respond slowly to selection due to low levels of additive genetic variance.