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Funder: EC | FP7 | FP7 Ideas: European Research Council (FP7 Ideas); Id: 100011199; Grant(s): 310785, Parental care can be partitioned into traits that involve direct engagement with offspring and traits that are expressed as an extended phenotype and influence the developmental environment, such as constructing a nursery. Here, we use experimental evolution to test whether parents can evolve modifications in nursery construction when they are experimentally prevented from supplying care directly to offspring. We exposed replicate experimental populations of burying beetles (Nicrophorus vespilloides) to different regimes of posthatching care by allowing larvae to develop in the presence (Full Care) or absence of parents (No Care). After only 13 generations of experimental evolution, we found an adaptive evolutionary increase in the pace at which parents in the No Care populations converted a dead body into a carrion nest for larvae. Cross-fostering experiments further revealed that No Care larvae performed better on a carrion nest prepared by No Care parents than did Full Care larvae. We conclude that parents construct the nursery environment in relation to their effectiveness at supplying care directly, after offspring are born. When direct care is prevented entirely, they evolve to make compensatory adjustments to the nursery in which their young will develop. The rapid evolutionary change observed in our experiments suggests there is considerable standing genetic variation for parental care traits in natural burying beetle populations-for reasons that remain unclear.

Recent studies have shown that intraspecific patterns of phenotypic plasticity can mirror patterns of evolutionary diversification among species. This appears to be the case in Nicrophorus beetles. Within species, body size is positively correlated with the size of carrion used to provision larvae and parental performance. Likewise, among species, variation in body size influences whether species exploit smaller or larger carrion and the extent to which larvae depend on parental care. However, it is unclear whether developmental plasticity in response to carcass size, parental care, or both underlie transitions to new carcass niches. We examined this by testing whether variation in the conditions experienced by Nicrophorus vespilloides larvae influenced their ability to breed efficiently upon differently sized carcasses as adults. We found that the conditions experienced by larvae during development played a critical role in determining their ability to use large carcasses effectively as adults. Specifically, individuals that developed with parental care and on large carcasses were best able to convert the resources on a large carcass into offspring when breeding themselves. Our results suggest that parentally induced plasticity can be important in the initial stages of niche expansion.

Significance The evolution of sibling rivalry is a classic problem in behavioral ecology. Our approach of observing the experimental evolution of sibling interactions in real time reveals three key insights. First, when parents provide parental care, siblings evolve to compete. Parental care compensates for the costs of sibling rivalry. Second, when parents do not supply care, siblings evolve to cooperate. Sibling cooperation compensates for the loss of parental care. Third, rapid evolutionary switching between sibling rivalry and sibling cooperation is possible because siblings induce greater levels of rivalry (or cooperation) in each other. This generates positive evolutionary feedback, rapidly locking larvae into evolving greater levels of competition (or cooperation) in the presence (or absence) of parental care., 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.

Conspicuous coloration is an important subject in social communication and animal behavior, and it can provide valuable insight into the role of visual signals in social selection. However, animal coloration can be plastic and affected by abiotic factors such as temperature, making its quantification problematic. In such cases, careful consideration is required so that metric choices are consistent across environments and least sensitive to abiotic factors. A detailed assessment of plastic trait in response to environmental conditions could help identify more robust methods for quantifying color. Temperature affects sexual ornamentation of eastern fence lizards, Sceloporus undulatus, with ventral coloration shifting from green to blue hues as temperatures rise, making the calculation of saturation (color purity) difficult under conditions where temperatures vary. We aimed to characterize how abiotic factors influence phenotypic expression and to identify a metric for quantifying animal color that is either independent from temperature (ideally) or best conserves individual's ranks. We compared the rates of change in saturation across two temperature treatments using seven metrics: three that are based on fixed spectral ranges (with two of them designed by us specifically for this system) and three that track the expressed hue (with one of them designed by us to circumvent spurious results in unornamented individuals). We also applied a lizard visual sensitivity model to understand how temperature-induced color changes may be perceived by conspecifics. We show that the rate of change in saturation between two temperatures is inconsistent across individuals, increasing at a higher rate in individuals with higher baseline saturation at lower temperatures. In addition, the relative color rank of individuals in a population varies with the temperature standardized by the investigator, but more so for some metrics than others. While we were unable to completely eliminate the effect of temperature, current tools for quantifying color allowed us to use spectral data to estimate saturation in a variety of ways and to largely preserve saturation ranks of individuals across temperatures while avoiding erroneous color scores. We describe our approaches and suggest best-practices for quantifying and interpreting color, particularly in cases where color changes in response to environmental factors.

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., The amount and predictability of parental care may influence the evolution of offspring traits. Here, the authors experimentally evolve burying beetles at different levels of parental care and find smaller mandibles and lower self-sufficiency in populations with more care.

Interactions among siblings are finely balanced between rivalry and cooperation, but the factors that tip the balance towards cooperation are incompletely understood. Previous observations of insect species suggest that (i) sibling cooperation is more likely when siblings hatch at the same time, and (ii) this is more common when parents provide little to no care. In this paper, we tested these ideas experimentally with the burying beetle, Nicrophorus vespilloides . Burying beetles convert the body of a small dead vertebrate into an edible nest for their larvae, and provision and guard their young after hatching. In our first experiment, we simulated synchronous or asynchronous hatching by adding larvae at different intervals to the carrion-breeding resource. We found that ‘synchronously’ hatched broods survived better than ‘asynchronously’ hatched broods, probably because ‘synchronous hatching’ generated larger teams of larvae, that together worked more effectively to penetrate the carrion nest and feed upon it. In our second experiment, we measured the synchronicity of hatching in experimental populations that had evolved for 22 generations without any post-hatching care, and control populations that had evolved in parallel with post-hatching care. We found that larvae were more likely to hatch earlier, and at the same time as their broodmates, in the experimental populations that evolved without post-hatching care. We suggest that synchronous hatching enables offspring to help each other when parents are not present to provide care. However, we also suggest that greater levels of cooperation among siblings cannot compensate fully for the loss of parental care.

Several recent hypotheses suggest that parental care can influence the extent of phenotypic variation within populations; however, there have been few tests of these ideas. We exploited the facultative nature of posthatching parental care in the burying beetle, Nicrophorus vespilloides, to test whether parental care influences the expression of phenotypic variation in an important fitness trait (body size). We found that parental care and brood size (which influences sibling competition) had positive and independent effects on variation in body size. First, the mean coefficient of variation (CV) of body size was significantly greater in broods that received care than in those that did not. Second, CV body size increased with brood size in both parental care treatments. These results are not consistent with predictions from recent hypotheses that predict parental care will reduce phenotypic variation among siblings. The positive effects of parental care and brood size on phenotypic variation that we observed are likely due to sibling competition for access to provisioning parents and competition for limiting resources contained in the breeding carcass. Our results suggest that future theory linking parental care to the generation and maintenance of phenotypic variation must integrate the nature of interactions among family members.

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. DOI: http://dx.doi.org/10.7554/eLife.07340.001, eLife digest The burying beetle is an unusual insect in that both the father and the mother take care of their young larvae. They do this by providing food in the form of a small dead animal, such as a mouse, from which they diligently remove any fur or feathers, and by defending both the food and the larvae from rivals. These actions reduce the fitness of the parents, which can be estimated by measuring by how long they survive after caring for their brood. They also increase the health of the larvae, as measured by how large the larvae are when they move away from the carcass to pupate. Kilner et al. wanted to know how the parenting received by larvae affects their behaviour when they grow up and have their own offspring. Larvae were given varying amounts of care, ranging from none at all to five days (which is the typical length of the larval stage for burying beetles). Larvae that received little or no care grew up to become low-quality parents, whereas those that received lots of care became high-quality parents. A low-quality parent is, by definition, a parent that becomes less fit as a result of rearing offspring; a high-quality parent providing the same amount of care would not suffer such a large reduction in its fitness. Each of the female beetles from this first experiment was then mated with a high-quality male and together they took care of their offspring. Kilner et al. observed that the fathers lived longer when they were paired with high-quality mothers than they did when they were paired with lower quality mothers. This happened because the lower quality mothers effectively exploited the fathers, forcing them to do more of the parenting. Although the males gained by raising healthy larvae, they paid a price by dying at a younger age. Results from these insect experiments are not directly linked to human behaviour, but they might tell us why animals of other species are generally so careful to choose a mate that matches them in quality. In this way, they can avoid being exploited when the pair work together to raise young. In future, Kilner et al. will investigate how beetles adjust their parenting effort in response to the effort put in by their partner: can they estimate parental quality directly, or do they simply observe how much care the other partner is providing? DOI: http://dx.doi.org/10.7554/eLife.07340.002

Parents of many species provision their young, and the extent of parental provisioning constitutes a major component of the offspring's social environment. Thus, a change in parental provisioning can alter selection on offspring, resulting in the coevolution of parental and offspring traits. Although this reasoning is central to our evolutionary understanding of family life, there is little direct evidence that selection by parents causes evolutionary change in their offspring. Here we use experimental evolution to examine how populations of burying beetles adapt to a change in posthatching parental provisioning. We measured the performance of larvae descended from lab populations that had been maintained with and without posthatching parental care (Full Care and No Care populations). We found that adaptation to the absence of posthatching care led to rapid and consistent changes in larval survival in the absence of care. Specifically, larvae from No Care populations had higher survival in the absence of care than larvae from Full Care populations. Other measures of larval performance, such as the ability of larvae to consume a breeding carcass and larval mass at dispersal, did not differ between the Full Care and No Care populations. Nevertheless, our results show that populations can adapt rapidly to a change in the extent of parental care and that experimental evolution can be used to study such adaptation.

Cryptic evolution occurs when evolutionary change is masked by concurrent environmental change. In most cases, evolutionary changes in the phenotype are masked by changing abiotic factors. However, evolutionary change in one trait might also be masked by evolutionary change in another trait, a phenomenon referred to as evolutionary environmental deterioration. Nevertheless, detecting this second type of cryptic evolution is challenging and there are few compelling examples. Here, we describe a likely case of evolutionary environmental deterioration occurring in experimental burying beetle ( Nicrophorus vespilloides ) populations that are adapting to a novel social environment that lacks post-hatching parental care. We found that populations rapidly adapted to the removal of post-hatching parental care. This adaptation involved clear increases in breeding success and larval density (number of dispersing larvae produced per gram of breeding carcass), which in turn masked a concurrent increase in the mean larval mass across generations. This cryptic increase in larval mass was accomplished through a change in the reaction norm that relates mean larval mass to larval density. Our results suggest that cryptic evolution might be commonplace in animal families, because evolving trophic and social interactions can potentially mask evolutionary change in other traits, like body size.

Studies of siblings have focused mainly on their competitive interactions and to a lesser extent on their cooperation. However, competition and cooperation are at opposite ends on a continuum of possible interactions and the nature of these interactions may be flexible with ecological factors tipping the balance toward competition in some environments and cooperation in others. Here we show that the presence of parental care and the density of larvae on the breeding carcass change the outcome of sibling interactions in burying beetle broods. With full parental care there was a strong negative relationship between larval density and larval mass, consistent with sibling competition for resources. In the absence of care, initial increases in larval density had beneficial effects on larval mass but further increases in larval density reduced larval mass. This likely reflects a density-dependent shift between cooperation and competition. In a second experiment, we manipulated larval density and removed parental care. We found that the ability of larvae to penetrate the breeding carcass increased with larval density and that feeding within the carcass resulted in heavier larvae than feeding outside the carcass. However, larval density did not influence carcass decay.