Having a better home range does not reduce the cost of reproduction in Soay sheep.

A cost of reproduction may not be observable in the presence of environmental or individual heterogeneity because they affect the resources available to individuals. Individual space use is critical in determining both the resources available to individuals and the exposure to factors that mediate the value of these resources (e.g. competition and parasitism). Despite this, there has, to our knowledge, been little research to understand how between-individual differences in resource acquisition, caused by variation in space use, interact with environmental variation occurring at the population scale to influence estimates of the cost of reproduction in natural populations. We used long-term data from the St. Kilda Soay sheep population to understand how differences in age, relative home range quality, and average adult body mass, interacted with annual variation in population density and winter North Atlantic Oscillation index to influence over-winter survival and reproduction in the subsequent year, for females that had invested into reproduction to varying degrees. Our results suggest that Soay sheep females experience costs both in terms of future survival and future reproduction. However, we found little evidence that estimated costs of reproduction vary depending on relative home range quality. There are several possible causes for the lack of a relationship between relative home range quality and our estimate of the costs experienced by females. These include the potential for a correlation between relative home range quality and reproductive allocation to mask a relationship between home range quality and reproductive costs, as well as the potential for the benefit of higher quality home ranges being offset by higher densities. Nevertheless, our results raise questions regarding the presence or context-dependence of relationships between resource access and the estimated cost of reproduction.

Resource allocation is determined by both parents and offspring in a burying beetle.

Parents and offspring have different optima for the level of parental resource allocation and the timing of nutritional independence. Theoretical models assume that either parents or offspring control the allocation of resources within a brood; however, control may also be mutual. Here, we investigate whether the resolution of parent-offspring conflict is biased towards cues from either the parents' or the offspring's behaviour, or whether the conflict is under mutual control. Importantly, we considered potential shifts in the power continuum over the entire period of juvenile dependency. The burying beetle Nicrophorus vespilloides parents provision food for the larvae, and the larvae solicit food from their parents with conspicuous begging displays. Both parental and larval behaviours change as larvae age. We repeatedly manipulated the age of the brood females care for, thereby creating mismatch between the age of the foster brood and expected age of the brood from the female parent's perspective, over the period of dependency in juvenile development. We found that females adjusted the total amount of provisioning based on the actual age of the brood. However, both the parent and the offspring influenced the levels of food provisioning, which followed neither the expected age of the brood from the parent's perspective nor offspring age. Our results suggest that there is mutual control over parental care, thus contradicting the dichotomous view of control over parental care. We suggest that the mutual influence of both parents and the offspring should be taken into account in development of future theory, as well as empirical studies.

Effects of inbreeding on behavioural plasticity of parent-offspring interactions in a burying beetle.

Inbreeding depression is defined as a fitness decline in progeny resulting from mating between related individuals, the severity of which may vary across environmental conditions. Such inbreeding-by-environment interactions might reflect that inbred individuals have a lower capacity for adjusting their phenotype to match different environmental conditions better, as shown in prior studies on developmental plasticity. Behavioural plasticity is more flexible than developmental plasticity because it is reversible and relatively quick, but little is known about its sensitivity to inbreeding. Here, we investigate effects of inbreeding on behavioural plasticity in the context of parent-offspring interactions in the burying beetle Nicrophorus vespilloides. Larvae increase begging with the level of hunger, and parents increase their level of care when brood sizes increase. Here, we find that inbreeding increased behavioural plasticity in larvae: inbred larvae reduced their time spent associating with a parent in response to the length of food deprivation more than outbred larvae. However, inbreeding had no effect on the behavioural plasticity of offspring begging or any parental behaviour. Overall, our results show that inbreeding can increase behavioural plasticity. We suggest that inbreeding-by-environment interactions might arise when inbreeding is associated with too little or too much plasticity in response to changing environmental conditions.

Females adjust maternal hormone concentration in eggs according to male condition in a burying beetle.

In birds and other vertebrates, there is good evidence that females adjust the allocation of hormones in their eggs in response to prenatal environmental conditions, such as food availability or male phenotype, with profound consequences for life history traits of offspring. In insects, there is also evidence that females deposit juvenile hormones (JH) and ecdysteroids (ESH) in their eggs, hormones that play a key role in regulating offspring growth and metamorphosis. However, it is unclear whether females adjust their hormonal deposition in eggs in response to prenatal environmental conditions. Here we address this gap by conducting an experiment on the burying beetle Nicrophorus vespilloides, in which we manipulated the presence of the male parent and the size of the carcass used for breeding at the time of laying. We also tested for effects of the condition (i.e., body mass) of the parents. We then recorded subsequent effects on JH and ESH concentrations in the eggs. We found no evidence for an effect of these prenatal environmental conditions (male presence and carcass size) on hormonal concentration in the eggs. However, we found that females reduced their deposition of JH when mated with heavier males. This finding is consistent with negative differential allocation of maternal hormones in response to variation in the body mass of the male parent. We encourage further work to investigate the role of maternally derived hormones in insect eggs.

Increased allocation to reproduction reduces future competitive ability in a burying beetle.

The existence of a trade-off between current and future reproduction is a fundamental prediction of life history theory. Support for this prediction comes from brood size manipulations, showing that caring for enlarged broods often reduces the parent's future survival or fecundity. However, in many species, individuals must invest in competing for the resources required for future reproduction. Thus, a neglected aspect of this trade-off is that increased allocation to current reproduction may reduce an individual's future competitive ability. We tested this prediction in the burying beetle, Nicrophorus vespilloides, a species where parents care for their offspring and where there is fierce competition for resources used for breeding. We manipulated reproductive effort by providing females with either a small brood of 10 larvae or a large brood of 40 larvae and compared the ability of these females, and virgin females that had no prior access to a carcass, to compete for a second carcass against a virgin competitor. We found that increased allocation to current reproduction reduced future competitive ability, as females that had cared for a small brood were more successful when competing for a second carcass against a virgin competitor than females that had cared for a large brood. In addition, the costs of reproduction were offset by the benefits of feeding from the carcass during an initial breeding attempt, as females that had cared for a small brood were better competitors than virgin females that had no prior access to a carcass, whilst females that had cared for a large brood were similar in competitive ability to virgin females. Our results add to our understanding of the trade-off between current and future reproduction by showing that this trade-off can manifest through differences in future competitive ability and that direct benefits of reproduction can offset some of these costs.

Females manipulate behavior of caring males via prenatal maternal effects.

In species with biparental care, there is sexual conflict as each parent is under selection to minimize its personal effort by shifting as much as possible of the workload over to the other parent. Most theoretical and empirical work on the resolution of this conflict has focused on strategies used by both parents, such as negotiation. However, because females produce the eggs, this might afford females with an ability to manipulate male behavior via maternal effects that alter offspring phenotypes. To test this hypothesis, we manipulated the prenatal conditions (i.e., presence or absence of the male), performed a cross-fostering experiment, and monitored the subsequent effects of prenatal conditions on offspring and parental performance in the burying beetle Nicrophorus vespilloides We found that offspring were smaller at hatching when females laid eggs in presence of a male, suggesting that females invest less in eggs when expecting male assistance. Furthermore, broods laid in the presence of a male gained more weight during parental care, and they did so at the expense of male weight gain. Contrary to our expectations, males cared less for broods laid in the presence of a male. Our results provide experimental evidence that females can alter male behavior during breeding by adjusting maternal effects according to prenatal conditions. However, rather than increasing the male's parental effort, females appeared to suppress the male's food consumption, thereby leaving more food for their brood.

Effects of variation in resource acquisition during different stages of the life cycle on life-history traits and trade-offs in a burying beetle.

Individual variation in resource acquisition should have consequences for life-history traits and trade-offs between them because such variation determines how many resources can be allocated to different life-history functions, such as growth, survival and reproduction. Since resource acquisition can vary across an individual's life cycle, the consequences for life-history traits and trade-offs may depend on when during the life cycle resources are limited. We tested for differential and/or interactive effects of variation in resource acquisition in the burying beetle Nicrophorus vespilloides. We designed an experiment in which individuals acquired high or low amounts of resources across three stages of the life cycle: larval development, prior to breeding and the onset of breeding in a fully crossed design. Resource acquisition during larval development and prior to breeding affected egg size and offspring survival, respectively. Meanwhile, resource acquisition at the onset of breeding affected size and number of both eggs and offspring. In addition, there were interactive effects between resource acquisition at different stages on egg size and offspring survival. However, only when females acquired few resources at the onset of breeding was there evidence for a trade-off between offspring size and number. Our results demonstrate that individual variation in resource acquisition during different stages of the life cycle has important consequences for life-history traits but limited effects on trade-offs. This suggests that in species that acquire a fixed-sized resource at the onset of breeding, the size of this resource has larger effects on life-history trade-offs than resources acquired at earlier stages.

Interplay between age-based competitive asymmetries within the brood and direct competition between inbred and outbred offspring in a burying beetle.

Theory suggests that intraspecific competition associated with direct competition between inbred and outbred individuals should be an important determinant of the severity of inbreeding depression. The reason is that, if outbred individuals are stronger competitors than inbred ones, direct competition should have a disproportionate effect on the fitness of inbred individuals. However, an individual's competitive ability is not only determined by its inbreeding status but also by competitive asymmetries that are independent of an individual's inbreeding status. When this is the case, such competitive asymmetries may shape the outcome of direct competition between inbred and outbred individuals. Here, we investigate the interface between age-based competitive asymmetries within broods and direct competition between inbred and outbred offspring in the burying beetle Nicrophorus vespilloides. We found that inbred offspring had lower survival than outbred ones confirming that there was inbreeding depression. Furthermore, seniors (older larvae) grew to a larger size and had higher survival than juniors (younger larvae), confirming that there were age-based competitive asymmetries. Nevertheless, there was no evidence that direct competition between inbred and outbred larvae exacerbated inbreeding depression, no evidence that inbreeding depression was more severe in juniors and no evidence that inbred juniors suffered disproportionately due to competition from outbred seniors. Our results suggest that direct competition between inbred and outbred individuals does not necessarily exacerbate inbreeding depression and that inbred individuals are not always more sensitive to poor and stressful conditions than outbred ones.

Effects of Offspring and Parental Inbreeding on Parent-Offspring Communication.

There is mounting evidence that inbreeding can have complex effects on social interactions among inbred and outbred individuals. Here, we investigate effects of offspring and maternal inbreeding on parent-offspring communication in the burying beetle Nicrophorus vespilloides. We find effects of the interaction between offspring and maternal inbreeding on maternal behavior. Outbred females provided more direct care toward inbred larvae, while inbred females provided similar levels of direct care toward inbred and outbred larvae. Furthermore, we find direct and indirect effects of offspring inbreeding on offspring begging and maternal behavior, respectively. Inbred larvae spent less time begging than outbred larvae, and (outbred) females provided more direct care and less indirect care toward inbred larvae. Finally, we find effects of the interaction between offspring and maternal inbreeding on larval body mass. Inbred and outbred offspring grew to a similar size when the female was outbred, while inbred offspring were of a smaller size when the female was inbred. Our results suggest that outbred females provided more care toward inbred offspring to compensate for their poor genetic quality. Our study advances our understanding of inbreeding by showing that inbreeding can have direct effects on the behavior of inbred individuals and indirect effects on the behavior of outbred individuals and that indirect effects on outbred individuals may in turn influence the fitness of inbred individuals.

Inbred burying beetles suffer fitness costs from making poor decisions.

There is growing interest in how environmental conditions, such as resource availability, can modify the severity of inbreeding depression. However, little is known about whether inbreeding depression is also associated with differences in individual decision-making. For example, decisions about how many offspring to produce are often based upon the prevailing environmental conditions, such as resource availability, and getting these decisions wrong may have important fitness consequences for both parents and offspring. We tested for effects of inbreeding on individual decision-making in the burying beetle Nicrophorus vespilloides, which uses the size of a carrion resource to make decisions about number of offspring. Both inbred and outbred females adjusted their initial decisions about number of eggs to lay based on carcass size. However, when we forced individuals to update this initial decision by providing them with a different-sized carcass partway through reproduction, inbred females failed to update their decision about how many larvae to cull. Consequently, inbred females reared too many larvae, resulting in negative fitness consequences in the form of smaller offspring and reduced female post-reproductive condition. Our study provides novel insights into the effects of inbreeding by showing that poor decision-making by inbred individuals can negatively affect fitness.

Biparental care is more than the sum of its parts: experimental evidence for synergistic effects on offspring fitness.

Despite an extensive body of theoretical and empirical literature on biparental cooperation, it is still unclear whether offspring fare equally, better or worse when receiving care by two parents versus a single parent. Some models predict that parents should withhold the amount of care they provide due to sexual conflict, thereby shifting as much of the workload as possible to their partner. This conflict should lead to offspring faring worse with two parents. Yet, other models predict that when parents care for their offspring together, their individual contributions can have synergistic (more than additive) effects on offspring fitness. Under this scenario, biparental cooperation should lead to offspring faring better with two parents. We address this fundamental question using a unique experimental design where we compared offspring fitness when the two parents worked together (biparental treatment) and when they worked separately (uniparental treatment), while keeping constant the amount of resources and number of offspring per parent across treatments. This made it possible to directly compare the biparental treatment to the sum of the male and female contributions in the uniparental treatment. Our main finding was that offspring grew larger and were more likely to survive to adulthood when reared by both parents than a single parent. This is the first empirical evidence for a synergistic effect of biparental cooperation on offspring fitness and could provide novel insights into the conditions favouring the evolution of biparental cooperation.

Flexible parents: joint effects of handicapping and brood size manipulation on female parental care in Nicrophorus vespilloides.

Parental care is highly variable, reflecting that parents make flexible decisions in response to variation in the cost of care to themselves and the benefit to their offspring. Much of the evidence that parents respond to such variation derives from handicapping and brood size manipulations, the separate effects of which are well understood. However, little is known about their joint effects. Here, we fill this gap by conducting a joint handicapping and brood size manipulation in the burying beetle Nicrophorus vespilloides. We handicapped half of the females by attaching a lead weight to their pronotum, leaving the remaining females as controls. We also manipulated brood size by providing each female with 5, 20 or 40 larvae. In contrast to what we predicted, handicapped females spent more time provisioning food than controls. We also found that handicapped females spent more time consuming carrion. Furthermore, handicapped females spent a similar amount of time consuming carrion regardless of brood size, whereas controls spent more time consuming carrion as brood increased. Females spent more time provisioning food towards larger broods, and females were more likely to engage in carrion consumption when caring for larger broods. We conclude that females respond to both handicapping and brood size manipulations, but these responses are largely independent of each other. Overall, our results suggest that handicapping might lead to a higher investment into current reproduction and that it might be associated with compensatory responses that negate the detrimental impact of higher cost of care in handicapped parents.

Differential effects of offspring and maternal inbreeding on egg laying and offspring performance in the burying beetle Nicrophorus vespilloides.

We investigate the effect of offspring and maternal inbreeding on maternal and offspring traits associated with early offspring fitness in the burying beetle Nicrophorus vespilloides. We conducted two experiments. In the first experiment, we manipulated maternal inbreeding only (keeping offspring outbred) by generating mothers that were outbred, moderately inbred or highly inbred. Meanwhile, in the second experiment, we manipulated offspring inbreeding only (keeping females outbred) by generating offspring that were outbred, moderately inbred or highly inbred. In both experiments, we monitored subsequent effects on breeding success (number of larvae), maternal traits (clutch size, delay until laying, laying skew, laying spread and egg size) and offspring traits (hatching success, larval survival, duration of larval development and average larval mass). Maternal inbreeding reduced breeding success, and this effect was mediated through lower hatching success and greater larval mortality. Furthermore, inbred mothers produced clutches where egg laying was less skewed towards the early part of laying than outbred females. This reduction in the skew in egg laying is beneficial for larval survival, suggesting that inbred females adjusted their laying patterns facultatively, thereby partially compensating for the detrimental effects of maternal inbreeding on offspring. Finally, we found evidence of a nonlinear effect of offspring inbreeding coefficient on number of larvae dispersing. Offspring inbreeding affected larval survival and larval development time but also unexpectedly affected maternal traits (clutch size and delay until laying), suggesting that females adjust clutch size and the delay until laying in response to being related to their mate.

Parental care buffers against inbreeding depression in burying beetles.

When relatives mate, their inbred offspring often suffer a reduction in fitness-related traits known as "inbreeding depression." There is mounting evidence that inbreeding depression can be exacerbated by environmental stresses such as starvation, predation, parasitism, and competition. Parental care may play an important role as a buffer against inbreeding depression in the offspring by alleviating these environmental stresses. Here, we examine the effect of parental care on the fitness costs of inbreeding in the burying beetle Nicrophorus vespilloides, an insect with facultative parental care. We used a 2 × 2 factorial design with the following factors: (i) the presence or absence of a caring female parent during larval development and (ii) inbred or outbred offspring. We examined the joint influence of maternal care and inbreeding status on fitness-related offspring traits to test the hypothesis that maternal care improves the performance of inbred offspring more than that of outbred offspring. Indeed, the female's presence led to a higher increase in larval survival in inbred than in outbred broods. Receiving care at the larval stage also increased the lifespan of inbred but not outbred adults, suggesting that the beneficial buffering effects of maternal care can persist long after the offspring have become independent. Our results show that parental care has the potential to moderate the severity of inbreeding depression, which in turn may favor inbreeding tolerance and influence the evolution of mating systems and other inbreeding-avoidance mechanisms.

Intraspecific Competition and Inbreeding Depression: Increased Competitive Effort by Inbred Males Is Costly to Outbred Opponents.

A recent theoretical model suggests that intraspecific competition is an important determinant of the severity of inbreeding depression. The reason for this is that intraspecific competition is density dependent, leading to a stronger negative effect on inbred individuals if they are weaker competitors than outbred ones. In support of this prediction, previous empirical work shows that inbred individuals are weaker competitors than outbred ones and that intraspecific competition often exacerbates inbreeding depression. Here, we report an experiment on the burying beetle Nicrophorus vespilloides, in which we recorded the outcome of competition over a small vertebrate carcass between an inbred or outbred male resident caring for a brood and a size-matched inbred or outbred male intruder. We found that inbred males were more successful as intruders in taking over a carcass from a male resident and were injured more frequently as either residents or intruders. Furthermore, inbred males gained less mass during the breeding attempt and had a shorter adult life span than outbred males. Finally, successful resident males reared a substantially smaller brood comprised of lighter larvae when the intruder was inbred than when it was outbred. Our results shows that inbred males increased their competitive effort, thus contradicting previous work suggesting that inbred males are weaker competitors. Furthermore, our results shows that inbred intruders impose a greater cost to resident males, suggesting that outbred individuals can suffer fitness costs as a result of competition with inbred ones.

Effects of Prior Contest Experience and Contest Outcome on Female Reproductive Decisions and Offspring Fitness.

Winning or losing a prior contest can influence the outcome of future contests, but it might also alter subsequent reproductive decisions. For example, losers may increase their investment in the current breeding attempt if losing a contest indicates limited prospects for future breeding. Using the burying beetle Nicrophorus vespilloides, we tested whether females adjust their prehatching and posthatching reproductive effort after winning or losing a contest with a same-sex conspecific. Burying beetles breed on carcasses of small vertebrates for which there is fierce intrasexual competition. We found no evidence that winning or losing a contest influenced reproductive investment decisions in this species. Instead, we show that a female's prior contest experience (regardless of its outcome) influenced the amount of posthatching care provided, with downstream consequences for the female's reproductive output; both winners and losers spent more time provisioning food to their offspring and produced larger broods than females with no contest experience. We discuss the wider implications of our findings and present a conceptual model linking contest-mediated adjustments in parental investment to population-level processes. We propose that the frequency of intraspecific contests could both influence and be influenced by population dynamics in species where contest experience influences the size and/or number of offspring produced.

Maternal effects alter the severity of inbreeding depression in the offspring.

A maternal effect is a causal influence of the maternal phenotype on the offspring phenotype over and above any direct effects of genes. There is abundant evidence that maternal effects can have a major impact on offspring fitness. Yet, no previous study has investigated the potential role of maternal effects in influencing the severity of inbreeding depression in the offspring. Inbreeding depression is a reduction in the fitness of inbred offspring relative to outbred offspring. Here, we tested whether maternal effects due to body size alter the magnitude of inbreeding depression in the burying beetle Nicrophorus vespilloides We found that inbreeding depression in larval survival was more severe for offspring of large females than offspring of small females. This might be due to differences in how small and large females invest in an inbred brood because of their different prospects for future breeding opportunities. To our knowledge, this is the first evidence for a causal effect of the maternal phenotype on the severity of inbreeding depression in the offspring. In natural populations that are subject to inbreeding, maternal effects may drive variation in inbreeding depression and therefore contribute to variation in the strength and direction of selection for inbreeding avoidance.

Complex effects of inbreeding on biparental cooperation.

There is mounting evidence that inbreeding can have detrimental effects on the fitness of outbred individuals that interact with or depend on inbred individuals. However, little is currently known about the behavioral mechanisms by which interactions with inbred individuals induce fitness costs in outbred individuals. Here, we study effects of inbreeding on the behavioral dynamics of biparental cooperation in the burying beetle Nicrophorus vespilloides. To this end, we used a two-by-two factorial design, in which an inbred or outbred female was mated to an inbred or an outbred male and tested for effects on cooperation between male and female parents providing care for their joint offspring. We found no evidence that inbred parents provided less care than outbred parents. Nevertheless, partners of inbred parents increased the amount of care they provided, leading to overcompensation. Our study shows that inbreeding can have strong and complex effects on the behavioral dynamics of biparental cooperation and that these effects are mediated mainly through changes in the partner's behavior. We suggest that similar effects of inbreeding on outbred individuals may extend to other social contexts, such as cooperative breeding and mating.

Flexible females: nutritional state influences biparental cooperation in a burying beetle.

In species that provide biparental care, there is a sexual conflict between parents over how much each should contribute toward caring for their joint offspring. Theoretical models for the resolution of this conflict through behavioral negotiation between parents assume that parents cannot assess their partner's state directly but do so indirectly by monitoring their partner's contribution. Here, we test whether parents can assess their partner's state directly by investigating the effect of nutritional state on cooperation between parents in the burying beetle Nicrophorus vespilloides. We used a two-by-two factorial design, in which a well-fed or food-deprived female was paired with a well-fed or food-deprived male. We found that females adjusted their level of care in response to both their own nutritional state and that of their partner and that these decisions were independent of their partner's contribution. We found no evidence that males responded directly to the nutritional state. Males instead responded indirectly based on the contribution of their partner. Our results suggest that parents are able to assess the state of their partner, in contrast to what has been assumed, and that these assessments play an important role in the mediation of sexual conflict between caring parents.

Revisiting the ecology and evolution of burying beetle behavior (Staphylinidae: Silphinae).

Investigating fundamental processes in biology requires the ability to ground broad questions in species-specific natural history. This is particularly true in the study of behavior because an organism's experience of the environment will influence the expression of behavior and the opportunity for selection. Here, we provide a review of the natural history and behavior of burying beetles of the genus Nicrophorus to provide the groundwork for comparative work that showcases their remarkable behavioral and ecological diversity. Burying beetles have long fascinated scientists because of their well-developed parenting behavior, exhibiting extended post-hatching care of offspring that varies extensively within and across taxa. Despite the burgeoning success of burying beetles as a model system for the study of behavioral evolution, there has not been a review of their behavior, ecology, and evolution in over 25 years. To address this gap, we leverage a developing community of researchers who have contributed to a detailed knowledge of burying beetles to highlight the utility of Nicrophorus for investigating the causes and consequences of social and behavioral evolution.