Offspring dependence on parental care and the role of parental transfer of oral fluids in burying beetles.

BACKGROUND: Immature stages of many animals can forage and feed on their own, whereas others depend on their parents' assistance to obtain or process food. But how does such dependency evolve, and which offspring and parental traits are involved? Burying beetles (Nicrophorus) provide extensive biparental care, including food provisioning to their offspring. Interestingly, there is substantial variation in the reliance of offspring on post-hatching care among species. Here, we examine the proximate mechanisms underlying offspring dependence, focusing on the larvae of N. orbicollis, which are not able to survive in the absence of parents. We specifically asked whether the high offspring dependence is caused by (1) a low starvation tolerance, (2) a low ability to self-feed or (3) the need to obtain parental oral fluids. Finally, we determined how much care (i.e. duration of care) they require to be able to survive. RESULTS: We demonstrate that N. orbicollis larvae are not characterized by a lower starvation tolerance than larvae of the more independent species. Hatchlings of N. orbicollis are generally able to self-feed, but the efficiency depends on the kind of food presented and differs from the more independent species. Further, we show that even when providing highly dependent N. orbicollis larvae with easy ingestible liquefied mice carrion, only few of them survived to pupation. However, adding parental oral fluids significantly increased their survival rate. Finally, we demonstrate that survival and growth of dependent N. orbicollis larvae is increased greatly by only a few hours of parental care. CONCLUSIONS: Considering the fact that larvae of other burying beetle species are able to survive in the absence of care, the high dependence of N. orbicollis larvae is puzzling. Even though they have not lost the ability to self-feed, an easily digestible, liquefied carrion meal is not sufficient to ensure their survival. However, our results indicate that the transfer of parental oral fluids is an essential component of care. In the majority of mammals, offspring rely on the exchange of fluids (i.e. milk) to survive, and our findings suggest that even in subsocial insects, such as burying beetles, parental fluids can significantly affect offspring survival.

Harsh nutritional environment has positive and negative consequences for family living in a burying beetle.

Harsh environmental conditions in form of low food availability for both offspring and parents alike can affect breeding behavior and success. There has been evidence that food scarce environments can induce competition between family members, and this might be intensified when parents are caring as a pair and not alone. On the other hand, it is possible that a harsh, food-poor environment could also promote cooperative behaviors within a family, leading, for example, to a higher breeding success of pairs than of single parents. We studied the influence of a harsh nutritional environment on the fitness outcome of family living in the burying beetle Nicrophorus vespilloides. These beetles use vertebrate carcasses for reproduction. We manipulated food availability on two levels: before and during breeding. We then compared the effect of these manipulations in broods with either single females or biparentally breeding males and females. We show that pairs of beetles that experienced a food-poor environment before breeding consumed a higher quantity of the carcass than well-fed pairs or single females. Nevertheless, they were more successful in raising a brood with higher larval survival compared to pairs that did not experience a food shortage before breeding. We also show that food availability during breeding and social condition had independent effects on the mass of the broods raised, with lighter broods in biparental families than in uniparental ones and on smaller carcasses. Our study thus indicates that a harsh nutritional environment can increase both cooperative as well as competitive interactions between family members. Moreover, our results suggest that it can either hamper or drive the formation of a family because parents choose to restrain reproductive investment in a current brood or are encouraged to breed in a food-poor environment, depending on former experiences and their own nutritional status.

Parent-offspring conflict and its outcome under uni-and biparental care.

Conflicts over parental investment are predicted to be common among family members, especially between parents and their offspring. Parent-offspring conflict has been studied in many brood-caring organisms, but whether its outcome is closer to the parental or offspring optimum is usually unknown, as is whether the presence of a second parent, a caring male partner, can affect the outcome. Here, we manipulated the initial brood size of single and paired female burying beetles to examine how many offspring are necessary to maintain parental care in the current brood. We found that mothers continued to invest in small broods even if their reproductive output would have been higher if they had discontinued their care and produced a second brood instead. Consequently, our data suggests that the offspring have the upper hand in the conflict. However, our results further show that paired females laid a second egg clutch more often and produced more offspring than single females, suggesting that the presence of a male partner shifts the conflict outcome towards the parental optimum. This latter result not only is a novel aspect of parent-offspring theory, but also represents an additional factor that might explain the evolution of biparental care.

Differences in sibling cooperation in presence and absence of parental care in a genus with interspecific variation in offspring dependence.

The widely spread evolutionary strategy of parental care is considered an important driver of social evolution. Although offspring were long thought to primarily interact competitively, recent studies revealed the potential importance of sibling cooperation. Theories suggest that the degree of cooperation in offspring interactions depends on the degree of offspring dependence on parental care: offspring unable to forage on their own should compete more, whereas more independent juveniles may increase the degree of cooperation. In this study, we tested the occurrence of sibling cooperation in the absence of posthatching care in several burying beetle species exhibiting varying degrees of offspring dependence. To this end, we measured larval growth rate and survival in the presence and absence of prehatching care using different brood sizes. We found that sibling cooperation cannot be exclusively explained by offspring dependence on parental care. Although only species with more independent larvae cooperated when receiving prehatching care, larval cooperation occurred across species in the absence of care. The latter result suggests that sibling cooperation was already present in an early ancestor of the genus Nicrophorus. Overall, these findings give important insights into the transition from facultative to obligate family life.