From facultative to obligatory parental care: Interspecific variation in offspring dependency on post-hatching care in burying beetles.
ABSTRACT: Studies on the evolution of parental care have focused primarily on the costs and benefits of parental care and the life-history attributes that favour it. However, once care evolves, offspring in some taxa appear to become increasingly dependent on their parents. Although offspring dependency is a central theme in family life, the evolutionary dynamics leading to it are not fully understood. Beetles of the genus Nicrophorus are well known for their elaborate biparental care, including provisioning of their young. By manipulating the occurrence of pre- or post-hatching care, we show that the offspring of three burying beetle species, N. orbicollis, N. pustulatus, and N. vespilloides, show striking variation in their reliance on parental care. Our results demonstrate that this variation within one genus arises through a differential dependency of larvae on parental feeding, but not on pre-hatching care. In N. pustulatus, larvae appear to be nutritionally independent of their parents, but in N. orbicollis, larvae do not survive in the absence of parental feeding. We consider evolutionary scenarios by which nutritional dependency may have evolved, highlighting the role of brood size regulation via infanticide in this genus.
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:Background:In species with parental care, there is striking variation in offspring dependence at birth, ranging from feeding independence to complete dependency on parents for nutrition. Frequently, highly dependent offspring further evolve reductions or alterations of morphological traits that would otherwise promote self-sufficiency. Here, we examine evidence for morphological evolution associated with dependence in burying beetles (Nicrophorus spp.), in which dependence upon parents appears to have several independent origins. In many species, precocial first instar larvae can survive without parenting, but several altricial species die at this stage on their own. We focused specifically on the mandibles, which are expected to be related to feeding ability and therefore independence from parents. Results:We find no evidence that the size of the mandible is related to dependence on parents. However, we do find a developmental and phylogenetic correlation between independence and the presence of serrations on the inner edge of the mandible. Mandibles of independent species bear serrations at hatching, whereas dependent species hatch with smooth mandibles, only developing serrations in the second instar when these larvae gain the ability to survive on their own. Phylogenetic evidence suggests that serrations coincide with independence repeatedly. We note a single exception to this trend, a beetle with a serrated mandible that cannot survive without parents. However, this exception occurs in a species that has recently evolved the loss of independence. Conclusions:We argue that the absence of mandible serrations occurs due to alternative selection pressures incurred in larvae dependent upon parents to survive. We suggest that this may have led to a variable function for mandibles, perhaps related to increased competitive ability among siblings or increased efficiency in receiving nutrition from parents. Furthermore, we propose that the phylogenetic pattern we see is consistent with the long-held evolutionary hypothesis that evolutionary change in behavior and physiology precede morphological change.
Project description:The commensal microbiota is a key modulator of animal fitness, but little is known about the extent to which the parental microbiota influences fitness-related traits of future generations. We addressed this gap by manipulating the parental microbiota of a polyphagous fruit fly (Bactrocera tryoni) and measuring offspring developmental traits, body composition, and fecundity. We generated three parental microbiota treatments where parents had a microbiota that was non-manipulated (control), removed (axenic), or removed-and-reintroduced (reinoculation). We found that the percentage of egg hatching, of pupal production, and body weight of larvae and adult females were lower in offspring of axenic parents compared to that of non-axenic parents. The percentage of partially emerged adults was higher, and fecundity of adult females was lower in offspring of axenic parents relative to offspring of control and reinoculated parents. There was no significant effect of parental microbiota manipulation on offspring developmental time or lipid reserve. Our results reveal transgenerational effects of the parental commensal microbiota on different aspects of offspring life-history traits, thereby providing a better understanding of the long-lasting effects of host-microbe interactions.
Project description: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.
Project description:A growing body of studies is showing that offspring telomere length (TL) can be influenced by the age of their parents. Such a relationship might be explained by variation in TL at conception (gamete effect) and/or by alteration of early growth conditions in species providing parental care. In a long-lived bird with bi-parental care, the Alpine swift (Apus melba), we exchanged an uneven number of 2 to 4-day-old nestlings between pairs as part of a brood size manipulation. Nestling TL was measured at 50 days after hatching, which allowed investigation of the influence of the age of both their biological and foster parents on offspring TL, after controlling for the manipulation. Nestling TL was negatively related to the age of their biological father and foster mother. Nestling TL did not differ between enlarged and reduced broods. These findings suggest that offspring from older males were fertilized by gametes with shorter telomeres, presumably due to a greater cell division history or a longer accumulation of damage, and that older females may have provided poorer parental care to their offspring.
Project description:Bi-parental care is very common in birds, occurring in over 90% of species, and is expected to evolve whenever the benefits of enhanced offspring survival exceed the costs to both parents of providing care. In altricial species, where the nestlings are entirely dependent on the parents for providing food until fledging, reproductive success is related to the capacity of the parents to provision the offspring at the nest. The degree to which parents synchronise their visits to the nest is rarely considered by studies of bi-parental care, and yet may be an important component of parental care, affecting the outcome of the reproductive attempt, and the dynamics of sexual conflict between the parents. Here we studied this aspect of parental care in the long-tailed finch (Poephila acuticauda), a socially monogamous estrildid finch. We monitored parental nest visit rates and the degree of parental visit synchrony, and assessed their effects on reproductive success (e.g., brood size, number of offspring fledged and nestling growth). The frequency of nest visits in a day was low in this species (<1 visit/h), but there was a high level of synchrony by the two partners with 73% of visits made together. There was a correlation between the proportion of visits that were made by the pair together and the size of the brood at hatching, although it was not related to the number of fledglings a pair produced, or the quality of those offspring. We suggest that nest visit synchrony may primarily be driven by the benefit of parents being together whilst foraging away from the nest, or may reduce nest predation by reducing the level of activity around the nest throughout the day.
Project description: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.
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: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:Optimal sex allocation is frequency-dependent, but senescence may cause behaviour at old age to be suboptimal. We investigated whether sex allocation changes with parental age, using 16 years of data comprising more than 2500 molecularly sexed offspring of more than 600 known-age parents in common terns (Sterna hirundo), slightly sexually size-dimorphic seabirds. We decomposed parental age effects into within-individual change and sex allocation-associated selective (dis)appearance. Individual parents did not differ consistently in sex allocation, but offspring sex ratios at fledging changed from female- to male-biased as parents aged. Sex ratios at hatching were not related to parental age, suggesting sons to outperform daughters after hatching in broods of old parents. Our results call for the integration of sex allocation theory with theory on ageing and demography, as a change in sex allocation with age per se will cause the age structure of a population to affect the frequency-dependent benefits and the age-specific strength of selection on sex allocation.