Per T. Smiseth

Partial begging: an empirical model for the early evolution of offspring signalling

Species where, from birth, the offspring feed themselves in addition to begging for food from the parents can be described as ‘partially begging’. Such species provide a unique opportunity to examine the evolution of offspring begging from nonndash;signalling offspring foraging strategies. We used the partially begging burying beetle Nicrophorus vespilloides to test specific hypotheses concerning the coexistence of begging and selfndash;feeding. We first tested whether the cessation of larval begging coincided with an increase in the efficiency of selfndash;feeding. As predicted, begging ceased when the efficiency of selfndash;feeding reached the point where the larvae grew just as well without as with access to food provided by the parent. We next tested whether the transition to nutritional independence was under parental or offspring control. The parent did not change its behaviour towards the larvae over time, while the larvae changed their behaviour by reducing the time spent begging in the presence of the parent. Food allocation during the transition to nutritional independence was therefore under offspring control. Our results on partial begging provide a starting point for new theoretical models for the origin of begging. We suggest that these should be constructed as scramblendash;competition models because the offspring control food allocation.

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.

Mechanisms and fitness effects of antibacterial defences in a carrion beetle

Parents of many species care for their offspring by protecting them from a wide range of environmental hazards, including desiccation, food shortages, predators, competitors, and parasites and pathogens. Currently, little is known about the mechanisms and fitness consequences of parental defences against bacterial pathogens and competitors. Here, we combine approaches from microbiology and behavioural ecology to investigate the role and mechanistic basis of antibacterial secretions applied to carcasses by parents of the burying beetle Nicrophorus vespilloides. This species rears its larvae on vertebrate carcasses, where larvae suffer significant fitness costs due to competition with bacterial decomposers. We first confirm that anal secretions produced by parents are potently bactericidal and that their effects are specific to gram‐positive bacteria. Next, we identify the source of bacterial killing as a secreted lysozyme and show that its concentration changes throughout the breeding cycle. Finally, we show that secreted lysozyme is crucial for larval development, increasing survival by nearly two‐fold compared to offspring reared in its absence. These results demonstrate for the first time that anal secretions applied to carrion is a form of parental care and expand the mechanistic repertoire of defences used by parent insects to protect dependent offspring from microbial threats.

The evolution of repeated mating in the burying beetle, Nicrophorus vespilloides

Abstract Animals of many species accept or solicit recurring copulations with the same partner; i.e., show repeated mating. An evolutionary explanation for this excess requires that the advantages of repeated mating outweigh the costs, and that behavioral components of repeated mating are genetically influenced. There can be benefits of repeated mating for males when there is competition for fertilizations or where the opportunities for inseminating additional mates are rare or unpredictable. The benefits to females are less obvious and, depending on underlying genetic architecture, repeated mating may have evolved as a correlated response to selection on males. We investigated the evolution of repeated mating with the same partner in the burying beetle Nicrophorus vespilloides by estimating the direct and indirect fitness benefits for females and the genetics of behavior underlying repeated mating. The number of times a female mated had minimal direct and no indirect fitness benefits for females. The behavioral components of repeated mating (mating frequency and mating speed) were moderately negatively genetically correlated in males and uncorrelated in females. However, mating frequency and mating speed were strongly positively genetically correlated between males and females. Our data suggest that repeated mating by female N. vespilloides may have evolved as a correlated response to selection on male behavior rather than in response to benefits of repeated mating for females.

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.

Antimicrobial secretions and social immunity in larval burying beetles, Nicrophorus vespilloides

Offspring of many animals develop in environments in which they are exposed to high densities of potentially harmful bacteria. For example, larvae of the carrion beetle Nicrophorus vespilloides face significant challenges from the bacteria they encounter during their development on decomposing vertebrate carcasses. We tested the idea that larvae secrete antimicrobial compounds during development to defend themselves against microbial exposure. We first showed that larval secretion of active antimicrobials peaked during the early stages of development. As has been found previously for parental secretions, larval secretions were active against Gram-positive but not Gram-negative bacteria, indicating that they might be based on lysozyme-like compounds. Finally, consistent with this antibacterial activity, we showed that larval survival declined significantly when challenged with lysozyme-resistant Staphylococcus aureus but not when challenged with a lysozyme-susceptible strain of the same species. These results demonstrate that Nicrophorus larvae are not simply passive recipients of social immunity derived from their parents, but that they are active participants in its production.

Asynchronous hatching in burying beetles: a test of the peak load reduction hypothesis

The evolution of asynchronous hatching is a central yet controversial issue in evolutionary ecology and animal behaviour. Although asynchronous hatching has a widespread taxonomic distribution, past research has focused almost exclusively on altricial birds. We tested the peak load reduction hypothesis for the evolution of asynchronous hatching in the burying beetle Nicrophorus vespilloides , an insect in which parents provide their offspring with food after hatching. This hypothesis posits that caring parents benefit from asynchronous hatching because it reduces the parents maximum workload during the peak in the offsprings demand for food. To test this hypothesis, we established three types of broods, synchronous, asynchronous and highly asynchronous, with a hatching span of 0, 24 and 48xa0h, respectively, and monitored effects on brood demand and female parental care. As expected, there were sharp peaks in both brood demand and female food provisioning, and the peak in brood demand decreased as a function of increasing levels of asynchronous hatching. However, in contrast to what we expected, the peak in female food provisioning was similar regardless of the level of asynchronous hatching, and offspring survival was substantially lower in highly asynchronous broods than in synchronous or asynchronous broods. We conclude that our results provide no overall support for the peak load reduction hypothesis. Further experiments are needed to establish the adaptive benefits of asynchronous hatching in this species.

Begging and parent-offspring conflict in grey seals

Theoretical models, assuming an underlying conflict of interest between parents and offspring, suggest that begging can be an honest signal of offspring need provided that it is costly. Models on begging have been tested primarily on those birds in which parents provide care for several offspring. For these species, the underlying conflict selecting for extravagant (and apparently costly) begging displays might be sibling competition rather than parent–offspring conflict. We tested hypotheses on begging and parent–offspring conflict with the grey seal, Halichoerus grypus, as our model species, in which lactating females care for a single pup. As predicted from models of begging as an honest signal of need, pups begged at a significantly higher rate when hungry than when satiated. Furthermore, a mother was more likely to approach her pup shortly after the pup had uttered a begging call than within a randomly chosen period. We found no consistent support, however, for the assumption that there are strong conflicts of interest between mothers and pups. For example, the rate of suckling was not correlated with begging rate, suckling bouts terminated by pups were not longer than those terminated by mothers, and, although pups initiated the majority of suckling bouts, mothers did not terminate more suckling bouts than pups. These findings thus suggest that begging in species that care for a single offspring may evolve in the absence of strong parent–offspring conflict. uf6d9 2001 The Association for the Study of Animal Behaviour

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.

Negotiation between parents: does the timing of mate loss affect female compensation in Nicrophorus vespilloides?

Facultative adjustments in care are usually interpreted as a form of negotiation between the parents over how much care each should provide. Previous research on the burying beetle, Nicrophorus vespilloides, shows that males but not females appear to adjust their levels of care following negotiation. However, the importance of negotiation is likely to decrease over the course of a breeding attempt, and thus the timing of mate removal might affect the degree to which females adjust their levels of care. We therefore performed an experimental study where we removed N. vespilloides males at different intervals; before the female was provided the resources needed for breeding, 24 h after receiving resources, at the time of larval hatching, or after the parental care period. We monitored the effects on levels of female care of the offspring when parental care is at its highest. We found that the timing of male removal had a significant effect on the time females spent maintaining the carcass, but not on the time females spent providing food for the offspring or processing carrion. Our findings suggest that, in N. vespilloides, female decisions about how much care to provide involves negotiation, although the importance of negotiation decreases towards the end of breeding attempts.