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Principles of social evolution have long been used retrospectively to interpret social interactions, but have less commonly been applied predictively to inform conservation and animal husbandry strategies. We investigate whether differences in developmental environment, facilitated by divergent social conditions, can predict resilience to environmental change. Upon exposure to harsh novel environments, populations that previously experienced more benign social environments are predicted either to suffer fitness losses (the "mutation load hypothesis" and "selection filter hypothesis") or maintain fitness (the "beneficial mutation hypothesis"). We tested these contrasting predictions using populations of burying beetles Nicrophorus vespilloides we had evolved experimentally for 45 generations under contrasting social environments by manipulating the supply of post-hatching parental care. We exposed sexually immature adults from each population to varying heat stress and measured the effect on survival and reproduction. The greater the level of parental care previously experienced by a population, the better its survival under heat stress during sexual maturation. Although this is consistent with the "beneficial mutation hypothesis," it is also possible that populations that had evolved without post-hatching care were simply more prone to dying during maturation, regardless of their thermal environment. Overall, we suggest that stochastic genetic variation, probably due to founder effects, had a stronger influence on resilience. We discuss the implications for translocation and captive breeding programs. [ABSTRACT FROM AUTHOR]

Through the effort required to construct them, the microenvironmental conditions they impose on the family and their indirect influence on posthatching care, nests play a key role in influencing family life. We combined experimental evolution with cross-fostering experiments on laboratory populations of Nicrophorus vespilloides to investigate three ways in which the nest can contribute more broadly to parental investment. We used replicate populations of N. vespilloides that had evolved for 42 generations under contrasting regimes of care. Populations were either able to supply posthatching care ('Full Care') or prevented from supplying any posthatching care ('No Care'). Research on these populations has previously shown that the No Care populations evolved to build rounder nests, more rapidly, by Generation 14. Here we found (1) larvae raised by Full Care parents on nests prepared by parents from the No Care population did not attain a higher mass by the end of larval development than larvae in other treatments. However, we did discover that (2) cross-fostering nests between families consistently reduced larval mass, and to a similar extent whether nests were cross-fostered between or within the populations. We suggest that cross-fostering disrupted the chemical environment on and around the nest since we found no evidence that (3) nests mediate interactions between males and females. The duration of paternal care was consistently shorter than the duration of maternal care, and even shorter for males from the No Care populations than males from the Full Care populations. Nevertheless, the duration of male care did not predict variation in duration of female care. In short, although the nest is the substrate for burying beetle family life, we found little evidence that it had evolved divergently in our experimental populations to influence parental investment. • Do nests contribute to offspring performance, independent of posthatching care? • We evolved lab populations of burying beetles with and without posthatching care. • Brood performance was reduced when nests were switched between families. • Switching nests between populations did not worsen brood performance. • Chemical or microbial cues might cause broods to perform best in their home nest. [ABSTRACT FROM AUTHOR]

Cooperative social behaviors, such as parental care, have long been hypothesized to relax selection leading to the accumulation of genetic variation in populations. Although the idea has been discussed for decades, there has been relatively little experimental work to investigate how social behavior contributes to genetic variation in populations. Here, we investigate how parental care can shape molecular genetic variation in the subsocial insect, Nicrophorus vespilloides. Using whole-genome sequencing of populations that had evolved in the presence or absence of parental care for 30 generations, we show that parental care maintains levels of standing genetic variation. In contrast, under a harsh environment without care, strong directional selection caused a reduction in genetic variation. Furthermore, we show that adaptation to the loss of care is associated with genetic divergence between populations at loci related to stress, morphological development, and transcriptional regulation. These data reveal how social behavior is linked to the genetic processes that shape and maintain genetic diversity within populations, and provides rare empirical evidence for an old hypothesis. Lay Summary: Social behaviors, such as parental care, have long been hypothesized to result in the accumulation of genetic variation in populations. Here, we investigate how parental care can shape molecular genetic variation in a species that performs biparental care, Nicrophorus vespilloides. Using genome sequencing of populations that had evolved in the presence or absence of parental care for 30 generations, we show that parental care maintains levels of standing genetic variation. In contrast, under a harsh environment without care, populations lost genetic variation. Furthermore, we show that adaptation to the loss of care is associated with genetic divergence between populations at genes related to stress, morphological development, and transcriptional regulation. These data reveal how social behavior is linked to the genetic processes that shape and maintain genetic diversity within populations. [ABSTRACT FROM AUTHOR]

Phenotypic plasticity enables animals to adjust their behavior flexibly to their social environment—sometimes through the expression of adaptive traits that have not been exhibited for several generations. We investigated how long social adaptations can usefully persist when they are not routinely expressed, by using experimental evolution to document the loss of social traits associated with the supply and demand of parental care. We allowed populations of burying beetles Nicrophorus vespilloides to evolve in two different social environments for 48 generations in the lab. In "Full Care" populations, traits associated with the supply and demand of parental care were expressed at every generation, whereas in "No Care" populations we prevented expression of these traits experimentally. We then revived trait expression in the No Care populations at generations 24, 43, and 48 by allowing parents to supply post-hatching care and compared these social traits with those expressed by the Full Care populations. We found that offspring demands for care and male provision of care in the No Care populations were lost sooner than female provision of care. We suggest that this reflects differences in the strength of selection for the expression of alternative traits in offspring, males and females, which can enhance fitness when post-hatching care is disrupted. [ABSTRACT FROM AUTHOR]

The overproduction of offspring is commonly associated with high hatching failure and a mechanism for dispensing with surplus young. We used experimental evolution of burying beetle populations Nicrophorus vespilloides to determine causality in these correlations. We asked does eliminating the mechanism for killing "spare" offspring cause the evolution of a more restrained clutch size and consequently select for reduced hatching failure? N. vespilloides typically overproduces eggs but kills 1st instar larvae through partial filial cannibalism during brood care. We established replicate evolving populations that either could practice filial cannibalism (Full Care) or could not, by removing parents before their young hatched (No Care). After 20+ generations of experimental evolution, we measured clutch size and hatching success. We found that No Care females produced fewer eggs than Full Care females when allowed to breed on a small corpse, a finding not explained by differences in female quality. On larger corpses, females from both populations laid similar numbers of eggs. Furthermore, hatching success was greater in the No Care populations on small corpses. Our results suggest that the adaptive overproduction of offspring depends on a mechanism for eliminating surplus young and that killing offspring, in turn, relaxes selection against hatching failure. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

It is often assumed that there is a positive relationship between egg size and offspring fitness. However, recent studies have suggested that egg size has a greater effect on offspring fitness in low-quality environments than in high-quality environments. Such observations suggest that mothers may compensate for poor posthatching environments by increasing egg size. In this paper we test whether there is a limit on the extent to which increased egg size can compensate for the removal of posthatching parental care in the burying beetle, Nicrophorus vespilloides. Previous experiments with N. vespilloides suggest that an increased egg size can compensate for a relatively poor environment after hatching. Here, we phenotypically engineered female N. vespilloides to produce large or small eggs by varying the amount of time they were allowed to feed on the carcass as larvae. We then tested whether differences between these groups in egg size translated into differences in larval performance in a harsh postnatal environment that excluded parental care. We found that females engineered to produce large eggs did not have higher breeding success, and nor did they produce larger larvae than females engineered to produce small eggs. These results suggest that there is a limit on the extent to which increased maternal investment in egg size can compensate for a poor posthatching environment. We discuss the implication of our results for a recent study showing that experimental N. vespilloides populations can adapt rapidly to the absence of posthatching parental care. [ABSTRACT FROM AUTHOR]

Parents play a key role in determining the phenotype of their offspring. However, relatively few studies have investigated whether parents can change their offspring's behaviour in a sustained way that persists into adulthood. With experiments on the burying beetle, Nicrophorus vespilloides , we investigated how the developmental environment created by parents affects their offspring's wing morphology in adulthood, and the correlated effects on adult flight behaviour. Burying beetles exhibit complex biparental care, but offspring can survive without parental provisioning. By removing parents just prior to hatching, while holding the nutritional environment constant, we investigated the downstream consequences for offspring morphology and behaviour. Larvae that developed in the absence of their parents had relatively long and more slender wings than those that developed in their parents' presence. Flight mill tests revealed that flight performance was dependent on the presence of parents during development but not on wing shape. Our results demonstrate that parents have long-lasting effects on the behaviour of their offspring, by influencing the morphology and flight behaviour of their young even after they have matured into adults. [ABSTRACT FROM AUTHOR]

Animal behavior, physiology, and fitness are influenced by materials transferred between conspecifics (e.g., milk or ejaculate), even in solitary taxa. Such socially transferred materials are currently studied separately, without acknowledgment that they are instigators of evolutionary change and potent mechanisms for indirect genetic effects. Recent methodological advances allow the linkage of socially transferred gene products to their physiological, behavioral, and fitness impacts, yet such integrative approaches are rarely used. This conceptual framing and classification of socially transferred materials bridges proximate and ultimate scales and connects molecular biology to evolution. The concept of socially transferred materials has the potential to bring about transformative innovation in fundamental research and also in applied fields, such as medicine and agriculture. 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. [ABSTRACT FROM AUTHOR]