For centuries, European culture has been enriched by depictions in art and literature of the diverse ways in which parents can exert a long-lasting influence on their children. We now know that animal parents can have similarly lingering effects on their offspring and a relatively new and growing area of research in evolutionary biology sets out to understand the causes and consequences of these influences. Formally known as ‘parental effects’, and defined as non-genetic influences of the parent on their young, the phenomenon is of particular interest because it can potentially speed up the pace of evolutionary change that allows animals to adapt to changing environments. This may prove vital for the continued survival of animal populations whose habitats are undergoing rapid man-made alterations.

Recent research in this area has revealed two general ways in which so-called parental effects might facilitate evolution. They can influence offspring fitness, promoting some individuals while dooming others. And they can potentially provide a mechanism for non-genetic inheritance. For example, individuals hatching from large eggs might then be more likely to produce large eggs themselves upon reaching maturity. Parental effects that cascade across the generations like this can accelerate the pace at which an adaptation for a new environment spreads through the population.

In this study, we were interested specifically in understanding how parental effects might modulate the fitness gained from particular acts of animal behaviour. An animal’s behaviour is one of the first traits to change and evolve when it enters a novel environment, and we wanted to know how parents might contribute to this process. We chose parental care as our behaviour of interest, because its adaptive value can readily be assessed by balancing the fitness benefits gained (by assessing offspring performance) against any fitness costs incurred by the parent from carrying out parental care (by assessing parental performance after reproduction). We wanted to know (i) how parental effects might change the fitness costs and benefits associated with parental care for any given individual, and (ii) whether handicapping individuals in this way might have associated fitness consequences for their social partner, with whom they raise young.

Our experiments exploited the unusual natural history of the burying beetle, Nicrophorus vespilloides. Like other Nicrophorus beetles, this species uses the carcass of a small vertebrate for reproduction. It exhibits elaborate biparental care, though one parent (of either sex) can raise offspring singlehandedly. Parents prepare the carcass for reproduction by stripping it of fur or feathers, rolling the flesh into a ball and interring it in a shallow grave. There the corpse becomes an edible nest for the larvae, which feed themselves upon the flesh and are, additionally, fed from time to time by the parents. Within a week of hatching, just a few bones remain of the carcass, the parents fly off in search of new mating opportunities and the larvae crawl away to pupate in the soil. Roughly five weeks later, they are sexually mature adults and the life cycle begins again. In our previous work, we discovered that we could remove parents at any stage from just prior to hatching to larval dispersal and the larvae would survive. This gave us a way to manipulate the magnitude of the parental effect experienced by offspring – by changing the extent of care they received. The short generation time (outlined above) meant that we could easily track the consequences when the larvae matured and exhibited parental behaviour themselves, to see how care supplied in one generation influenced the supply ofcare in the next.

Our experiments showed that adults which received low levels of care as larvae were less successful at raising larger broods and suffered greater mortality afterwards: they were low-quality parents. Well-nourished offspring, conversely, matured into high-quality parents. Furthermore, when raising offspring with higher-quality parents, low-quality individuals caused their partners to suffer raised levels of mortality following reproduction, presumably because they had to work harder to compensate for the inferior partner’s shortcomings.

The evolution of new adaptive behaviour depends both on a mechanism for inheritance of behavioural traits from generation to generation and on the net fitness gained by performing that behaviour. Our study shows that parental effects not only influence the inheritance of a behavioural trait (because, for example, well-cared for larvae mature into high-quality parents), but that also they alter the fitness gains associated with that behaviour, with knock-on fitness consequences for their social partner.

Thus, our experiment indicates how parental effects can potentially provide a mechanism for the rapid evolution of new adaptive social behaviour in the face of environmental change.

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