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Selection, inheritance, and the evolution of parent-offspring interactions
Very few studies have examined parent-offspring interactions from a quantitative genetic perspective. We used a cross-fostering design and measured genetic correlations and components of social selection arising from two parental and two offspring behaviors in the burying beetle Nicrophorus vespilloides. Genetic correlations were assessed by examining behavior of relatives independent of common social influences. We found positive genetic correlations between all pairs of behaviors, including between parent and offspring behaviors. Patterns of selection were assessed by standardized performance and selection gradients. Parental provisioning had positive effects on offspring performance and fitness, while remaining near the larvae without feeding them had negative effects. Begging had positive effects on offspring performance and fitness, while increased competition among siblings had negative effects. Coadaptations between parenting and offspring behavior appear to be maintained by genetic correlations and functional trade-offs; parents that feed their offspring more also spend more time in the area where they can forage for themselves. Families with high levels of begging have high levels of sibling competition. Integrating information from genetics and selection thus provides a general explanation for why variation persists in seemingly beneficial traits expressed in parent-offspring interactions and illustrates why it is important to measure functionally related suites of behaviors
Coadaptation of prenatal and postnatal maternal effects
In a wide variety of species, a female's age of first reproduction influences offspring size and survival, suggesting that there exists an optimal timing of reproduction. Mothers in many species also influence offspring size and survival after birth through variation in parental care. We experimentally separated these effects in the burying beetle Nicrophorus vespilloides to test for coadaptation between prenatal and postnatal maternal effects associated with age at first reproduction. Females that reproduced early produced offspring with lower birth weight. The amount of parental care depended on the age of first reproduction of the caretaker, as did the extent of offspring begging. As predicted for a coadaptation of maternal effects, prenatal and postnatal effects were opposite for different-aged mothers, and larval weight gain and survival was greatest when the age of the caretaker and birth mother matched. Thus, prenatal effects intrinsically associated with age of first reproduction can be ameliorated by innate plasticity in postnatal care. A coadaptation of prenatal and postnatal maternal effects may evolve to allow variable timing of the first reproductive attempt. Such a coadaptation might be particularly valuable when females are constrained from reproducing at an optimal age, as, for example, in species that breed on scarce and unpredictable resources
Data from: 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.Pilakouta, Natalie; Smiseth, Per T. (2016), Data from: Maternal effects alter the severity of inbreeding depression in the offspring, Dryad, Dataset, https://doi.org/10.5061/dryad.r754
Data from: Flexible females: nutritional state influences biparental cooperation in a burying beetle
In species that provide biparental care, there is sexual conflict between parents over how much each should contribute towards 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 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.Lambert, Georgia A.; Smiseth, Per T. (2024). Data from: Flexible females: nutritional state influences biparental cooperation in a burying beetle [Dataset]. Dryad. https://doi.org/10.5061/dryad.s7h44j1f
Data from: Asynchronous hatching provides females with a means for increasing male care but incurs a cost by reducing offspring fitness
In species with biparental care, sexual conflict occurs because the benefit of care depends on the total amount of care provided by the two parents while the cost of care depends on each parent’s own contribution. Asynchronous hatching may play a role in mediating the resolution of this conflict over parental care. The sexual conflict hypothesis for the evolution of asynchronous hatching suggests that females adjust hatching patterns in order to increase male parental effort relative to female effort. We tested this hypothesis in the burying beetle Nicrophorus vespilloides by setting up experimental broods with three different hatching patterns: synchronous, asynchronous and highly asynchronous broods. As predicted, we found that males provided care for longer in asynchronous broods whereas the opposite was true of females. However, we did not find any benefit to females of reducing their duration of care in terms of increased lifespan or reduced mass loss during breeding. We found substantial negative effects of hatching asynchrony on offspring fitness as larval mass was lower and fewer larvae survived to dispersal in highly asynchronous broods compared to synchronous or asynchronous broods. Our results suggest that, even though females can increase male parental effort by hatching their broods more asynchronously, females pay a substantial cost from doing so in terms of reducing offspring growth and survival. Thus, females should be under selection to produce a hatching pattern that provides the best possible trade-off between the benefits of increased male parental effort and the costs due to reduced offspring fitness.Ford, Lucy E.; Smiseth, Per T. (2015), Data from: Asynchronous hatching provides females with a means for increasing male care but incurs a cost by reducing offspring fitness, Dryad, Dataset, https://doi.org/10.5061/dryad.sm1g
Data from: 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, while 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 brood. 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.Ratz, Tom; Smiseth, Per T. (2018), Data from: Flexible parents: joint effects of handicapping and brood size manipulation on female parental care in Nicrophorus vespilloides, Dryad, Dataset, https://doi.org/10.5061/dryad.p208f1
Data from: Intergenerational effects of inbreeding in Nicrophorus vespilloides: offspring suffer fitness costs when either they or their parents are inbred
Inbreeding depression is the reduction in fitness caused by mating between related individuals. Inbreeding is expected to cause a reduction in offspring fitness when the offspring themselves are inbred, but outbred individuals may also suffer a reduction in fitness when they depend on care from inbred parents. At present, little is known about the significance of such intergenerational effects of inbreeding. Here, we report two experiments on the burying beetle Nicrophorus vespilloides, an insect with elaborate parental care, in which we investigated inbreeding depression in offspring when either the offspring themselves or their parents were inbred. We found substantial inbreeding depression when offspring were inbred, including reductions in hatching success of inbred eggs and survival of inbred offspring. We also found substantial inbreeding depression when parents were inbred, including reductions in hatching success of eggs produced by inbred parents and survival of outbred offspring that received care from inbred parents. Our results suggest that intergenerational effects of inbreeding can have substantial fitness costs to offspring, and that future studies need to incorporate such costs to obtain accurate estimates of inbreeding depression.Mattey, Sarah N.; Strutt, Luke; Smiseth, Per T. (2012), Data from: Intergenerational effects of inbreeding in Nicrophorus vespilloides: offspring suffer fitness costs when either they or their parents are inbred, Dryad, Dataset, https://doi.org/10.5061/dryad.db40
Data from: State-dependent cooperation in burying beetles: parents adjust their contribution towards care based on both their own and their partner’s size
Handicapping experiments on species with biparental care show that a focal parent increases its contribution when its partner is handicapped. Such results are interpreted as evidence for negotiation, whereby each parent adjusts its amount of care to that of its partner. However, it is currently unclear whether the focal parent responds to a change in its handicapped partner's behaviour or state. To address this gap, we conducted an experiment on the burying beetle Nicrophorus vespilloides where we first experimentally generated different-sized male and female parents by varying the duration of larval development. We then used a 2×2 factorial design in which a small or large male was paired with a small or large female. Small females provided less direct care (food provisioning and interactions with larvae) than large females, and males and females provided less direct care when paired with a small partner. Thus, the focal parent adjusted its contribution towards care based on both its own state and that of its partner. There was evidence for negotiation between the two parents as the focal parent adjusted its contribution based on the amount of care by its partner. However, there was no evidence that negotiation accounted for how the focal parent responded to its partner's size. Our results have important implications for our understanding of biparental cooperation as they show that each parent not only adjusts its contribution based on the amount of care provided by its partner but also based on its own state and its partner's state.Pilakouta, Natalia; Richardson, Jon; Smiseth, Per T. (2015), Data from: State-dependent cooperation in burying beetles: parents adjust their contribution towards care based on both their own and their partner’s size, Dryad, Dataset, https://doi.org/10.5061/dryad.7nj7
Data from: Sibling competition does not exacerbate inbreeding depression in the burying beetle Nicrophorus vespilloides
Inbreeding results from matings between relatives and can cause a reduction in offspring fitness, known as inbreeding depression. Previous work has shown that a wide range of environmental stresses, such as extreme temperatures, starvation, and parasitism, can exacerbate inbreeding depression. It has recently been argued that stresses due to intraspecific competition should have a stronger effect on the severity of inbreeding depression than stresses due to harsh physical conditions. Here, we tested whether an increase in the intensity of sibling competition can exacerbate inbreeding depression in the burying beetle Nicrophorus vespilloides. We used a 2×3 factorial design with offspring inbreeding status (outbred or inbred) and brood size (5, 20, or 40 larvae) as the two factors. We found a main effect of inbreeding status, as inbred larvae had lower survival than outbred larvae, and a main effect of brood size, as larvae in large broods had lower survival and mass than larvae in medium-sized broods. However, there was no effect of the interaction between inbreeding status and brood size, suggesting that sibling competition did not influence the severity of inbreeding depression. Since we focused on sibling competition within homogeneous broods of either inbred or outbred larvae, we cannot rule out possible effects of sibling competition on inbreeding depression in mixed paternity broods comprising of both inbred and outbred offspring. More information on whether and when sibling competition might influence the expression of inbreeding depression can help advance our understanding of the causes underlying variation in the severity of inbreeding depression.Pilakouta, Natalie; Sieber, Daniel J.; Smiseth, Per T. (2016), Data from: Sibling competition does not exacerbate inbreeding depression in the burying beetle Nicrophorus vespilloides, Dryad, Dataset, https://doi.org/10.5061/dryad.m398
Data from: 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.Paquet, Matthieu; Smiseth, Per T. (2018), Data from: Females manipulate behavior of caring males via prenatal maternal effects, Dryad, Dataset, https://doi.org/10.5061/dryad.8424
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