Among-individual variation in behavioral plasticity—the modification of behavior in response to changes in environment experienced by individuals—is increasingly recognized as an important, but relatively poorly understood, feature of organisms that facilitates adaptation to environmental change. It is expected to evolve when there is rapidly fluctuating or directional environmental change during the lifetime of individuals. This is particularly likely to occur in the context of reproductive behaviors, when the outcomes of unpredictable social interactions with other individuals during mating and parental care determine how selection acts on males and females and mating systems evolve. To better understand patterns of mating and parental care and organismal adaptation to environmental change, we need to know why there is so much variation in behavioral plasticity between and within species. Here we address this question using burying beetles as a model. Burying beetles have unusually variable, facultatively expressed, modes of parental care and variation between the sexes and among individuals in the plasticity of reproductive behaviors. We present evidence to show that variation in male plasticity of mating behavior is a key driver of the evolution of patterns of parental care in Nicrophorus vespilloides burying beetles. More generally, we conclude that behavioral plasticity in burying beetles, and likely other taxa, has evolved as a consequence of a resource requirement bottle-neck (niche specialization) in combination with highly unpredictable availability of such suitable resources and the social unpredictability that arises as a result: constraint is the mother of plastic invention.

Sexual conflict occurs when selection to maximize fitness in one sex does so at the expense of the other sex. In the burying beetle Nicrophorus vespilloides, repeated mating provides assurance of paternity at a direct cost to female reproductive productivity. To reduce this cost, females could choose males with low repeated mating rates or smaller, servile males. We tested this by offering females a dichotomous choice between males from lines selected for high or low mating rate. Each female was then allocated her preferred or non-preferred male to breed. Females showed no preference for males based on whether they came from lines selected for high or low mating rates. Pairs containing males from high mating rate lines copulated more often than those with low line males but there was a negative relationship between female size and number of times she mated with a non-preferred male. When females bred with their preferred male the number of offspring reared increased with female size but there was no such increase when breeding with non-preferred males. Females thus benefited from being choosy, but this was not directly attributable to avoidance of costly male repeated mating.

Male and female genital morphology varies widely across many taxa, and even among populations. Disentangling potential sources of selection on genital morphology is problematic because each sex is predicted to respond to adaptations in the other due to reproductive conflicts of interest. To test how variation in this sexual conflict trait relates to variation in genital morphology we used our previously developed artificial selection lines for high and low repeated mating rates. We selected for high and low repeated mating rates using monogamous pairings to eliminate contemporaneous female choice and male-male competition. Male and female genital shape responded rapidly to selection on repeated mating rate. High and low mating rate lines diverged from control lines after only 10 generations of selection. We also detected significant patterns of male and female genital shape coevolution among selection regimes. We argue that because our selection lines differ in sexual conflict, these results support the hypothesis that sexually antagonistic coevolution can drive the rapid divergence of genital morphology. The greatest divergence in morphology corresponded with lines in which the resolution of sexual conflict over mating rate was biased in favor of male interests.

Male parents face a choice: should they invest more in caring for offspring or in attempting to mate with other females? the most profitable course depends on the intensity of competition for mates, which is likely to vary with the population sex ratio. However, the balance of pay-offs may vary among individual males depending on their competitive prowess or attractiveness. We tested the prediction that sex ratio and size of the resource holding male provide cues regarding the level of mating competition prior to breeding and therefore influence the duration of a male's biparental caring in association with a female. Male burying beetles, Nicrophorus vespilloides were reared, post-eclosion, in groups that differed in sex ratio. Experimental males were subsequently translocated to the wild, provided with a breeding resource (carcass) and filmed. We found no evidence that sex ratio cues prior to breeding affected future parental care behaviour but males that experienced male-biased sex ratios took longer to attract wild mating partners. Smaller males attracted a higher proportion of females than did larger males, securing significantly more monogamous breeding associations as a result. Smaller males thus avoided competitive male-male encounters more often than larger males. This has potential benefits for their female partners who avoid both intrasexual competition and direct costs of higher mating frequency associated with competing males.

Male parents spend less time caring than females in many species with biparental care. The traditional explanation for this pattern is that males have lower confidence of parentage, so they desert earlier in favour of pursuing other mating opportunities. However, one recent alternative hypothesis is that prolonged male parental care might also evolve if staying to care actively improves paternity. If this is the case, an increase in reproductive competition should be associated with increased paternal care. To test this prediction, we manipulated the level of reproductive competition experienced by burying beetles, Nicrophorus vespilloides (Herbst, 1783). We found that caregiving males stayed for longer and mated more frequently with their partner when reproductive competition was greater. Reproductive productivity did not increase when males extended care. Our findings provide support for the increased paternity hypothesis. Extended duration of parental care may be a male tactic both protecting investment (in the current brood) and maximizing paternity (in subsequent brood(s) via female stored sperm) even if this fails to maximize current reproductive productivity and creates conflict of interest with their mate via costs associated with increased mating frequency.

Good early nutritional conditions may confer a lasting fitness advantage over individuals suffering poor early conditions (a 'silver spoon' effect). Alternatively, if early conditions predict the likely adult environment, adaptive plastic responses might maximize individual performance when developmental and adult conditions match (environmental-matching effect). Here, we test for silver spoon and environmental-matching effects by manipulating the early nutritional environment of Nicrophorus vespilloides burying beetles. We manipulated nutrition during two specific early developmental windows: the larval environment and the post-eclosion environment. We then tested contest success in relation to variation in adult social environmental quality experienced (defined according to whether contest opponents were smaller (good environment) or larger (poor environment) than the focal individual). Variation in the larval environment influenced adult body size but not contest success per se for a given adult social environment experienced (an 'indirect' silver spoon effect). Variation in post-eclosion environment affected contest success dependent on the quality of the adult environment experienced (a context-dependent 'direct' silver spoon effect). By contrast, there was no evidence for environmental-matching. The results demonstrate the importance of social environmental context in determining how variation in nutrition in early life affects success as an adult.

Food availability can be unpredictable. When food becomes more abundant following a period of low food availability, developing larvae or juveniles often allocate resources preferentially towards increasing growth. This has important long-term effects on adult phenotypes and longevity. Despite the importance of strategic resource allocation during early development, few studies have examined how changes in resource availability during other windows of development affect reproductive strategies and fitness independent of growth. We manipulated food availability in a burying beetle, Nicrophorus vespilloides, during a subadult period of sexual maturation when individuals cannot increase structural size but are still undergoing reproductive maturation. In contrast to the trade-offs during larval or juvenile growth, beetles that experienced delayed feeding during reproductive maturation allocated resources preferentially towards maintaining both reproductive function and longevity. In both sexes, delayed feeding beetles were much less successful in competition for carcasses. However, delayed feeding males and females provided similar amounts of parental care and did not differ in reproductive success or longevity. These results indicate that the nutritional environment experienced during a key developmental window may be an important determinant of the expression of alternative reproductive strategies in adulthood, independent of body size. © 2013 British Ecological Society.