Heatwaves inflict reproductive but not survival costs to male insects.

Climate change is having a dramatic effect on the environment, with rising global temperatures and more frequent extreme climatic events, such as heatwaves, that can hamper organisms' biological functions. Although it is clear that sudden and extreme temperatures can damage reproductive processes, there is limited understanding of the effects of heatwaves on male mating behaviour and reproductive success. We tested for the effects of heat stress induced by ecologically relevant heatwaves (33°C and 39°C for five consecutive days) on the mating behaviour, reproductive success, body mass and survival of male field crickets Gryllus bimaculatus, paired with untreated females. We predicted life-history and reproductive costs would increase with increasing heatwave intensity. Consistent with our expectations, males exposed to the highest heatwave temperature produced the fewest offspring, while having to increase courtship effort to successfully mate. Males also gained relatively more weight following heatwave exposure. Given that we found no difference in lifetime survival, our results suggest a potential trade-off in resource allocation between somatic maintenance and reproductive investment. Taken together, our findings indicate that sublethal effects of heatwaves could reduce the growth and persistence of animal populations by negatively impacting reproductive rates. These findings highlight the need for considering thermal ecologies, life history and behaviour to better understand the consequences of extreme climatic events on individuals and populations.

The evolution of prey-attraction strategies in spiders: the interplay between foraging and predator avoidance.

Lures and other adaptations for prey attraction are particularly interesting from an evolutionary viewpoint because they are characterized by correlational selection, involve multicomponent signals, and likely reflect a compromise between maximizing conspicuousness to prey while avoiding drawing attention of enemies and predators. Therefore, investigating the evolution of lure and prey-attraction adaptations can help us understand a larger set of traits governing interactions among organisms. We review the literature focusing on spiders (Araneae), which is the most diverse animal group using prey attraction and show that the evolution of prey-attraction strategies must be driven by a trade-off between foraging and predator avoidance. This is because increasing detectability by potential prey often also results in increased detectability by predators higher in the food chain. Thus increasing prey attraction must come at a cost of increased risk of predation. Given this trade-off, we should expect lures and other prey-attraction traits to remain suboptimal despite a potential to reach an optimal level of attractiveness. We argue that the presence of this trade-off and the multivariate nature of prey-attraction traits are two important mechanisms that might maintain the diversity of prey-attraction strategies within and between species. Overall, we aim to stimulate research on this topic and progress in our general understanding of the diversity of predator and prey interactions.

The importance of distinguishing individual differences in 'social impact' versus 'social responsiveness' when quantifying indirect genetic effects on the evolution of social plasticity.

Social evolution and the dynamics of social interactions have previously been studied under the frameworks of quantitative genetics and behavioural ecology. In quantitative genetics, indirect genetic effects of social partners on the socially plastic phenotypes of focal individuals typically lack crucial detail already included in treatments of social plasticity in behavioural ecology. Specifically, whilst focal individuals (e.g. receivers) may show variation in their 'responsiveness' to the social environment, individual social partners (e.g. signallers) may have a differential 'impact' on focal phenotypes. Here we propose an integrative framework, that highlights the distinction between responsiveness versus impact in indirect genetic effects for a range of behavioural traits. We describe impact and responsiveness using a reaction norm approach and provide statistical models for the assessment of these effects of focal and social partner identity in different types of social interactions. By providing such a framework, we hope to stimulate future quantitative research investigating the causes and consequences of social interactions on phenotypic evolution.

Carry on caring: infected females maintain their parental care despite high mortality.

Parental care is a key component of an organism's reproductive strategy that is thought to trade-off with allocation toward immunity. Yet, it is unclear how caring parents respond to pathogens: do infected parents reduce care as a sickness behavior or simply from being ill or do they prioritize their offspring by maintaining high levels of care? To address this issue, we investigated the consequences of infection by the pathogen Serratia marcescens on mortality, time spent providing care, reproductive output, and expression of immune genes of female parents in the burying beetle Nicrophorus vespilloides. We compared untreated control females with infected females that were inoculated with live bacteria, immune-challenged females that were inoculated with heat-killed bacteria, and injured females that were injected with buffer. We found that infected and immune-challenged females changed their immune gene expression and that infected females suffered increased mortality. Nevertheless, infected and immune-challenged females maintained their normal level of care and reproductive output. There was thus no evidence that infection led to either a decrease or an increase in parental care or reproductive output. Our results show that parental care, which is generally highly flexible, can remain remarkably robust and consistent despite the elevated mortality caused by infection by pathogens. Overall, these findings suggest that infected females maintain a high level of parental care, a strategy that may ensure that offspring receive the necessary amount of care but that might be detrimental to the parents' own survival or that may even facilitate disease transmission to offspring.

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.

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.

No evidence of sibling cooperation in the absence of parental care in Nicrophorus vespilloides.

Interactions among siblings fall on a continuum with competition and cooperation at opposite ends of the spectrum. Prior work on the burying beetle Nicrophorus vespilloides suggests that parental care shifts the balance between competition and cooperation by masking a density-dependent shift from cooperation to competition. However, these results should be interpreted with caution because they were based on correlational evidence for an association between larval density at dispersal and mean larval mass at dispersal. Here, we test for a causal effect of the initial density of larvae in a brood on the larvae's subsequent performance in the absence of care. We find no effect of the initial larval density on mean larval mass. Thus, our results provide no evidence for sibling cooperation in the absence of care in this species. However, using larval density at dispersal as a predictor of mean larval mass at dispersal, there was a significant correlation between larval density and mean larval mass. Our study highlights the importance of using experimental designs that exclude confounding effects due to shared environmental conditions that otherwise could be misinterpreted as evidence for sibling cooperation.

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.

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.

The Saturniidae of Barro Colorado Island, Panama: A model taxon for studying the long-term effects of climate change?

We have little knowledge of the response of invertebrate assemblages to climate change in tropical ecosystems, and few studies have compiled long-term data on invertebrates from tropical rainforests. We provide an updated list of the 72 species of Saturniidae moths collected on Barro Colorado Island (BCI), Panama, during the period 1958-2016. This list will serve as baseline data for assessing long-term changes of saturniids on BCI in the future, as 81% of the species can be identified by their unique DNA Barcode Index Number, including four cryptic species not yet formally described. A local species pool of 60 + species breeding on BCI appears plausible, but more cryptic species may be discovered in the future. We use monitoring data obtained by light trapping to analyze recent population trends on BCI for saturniid species that were relatively common during 2009-2016, a period representing >30 saturniid generations. The abundances of 11 species, of 14 tested, could be fitted to significant time-series models. While the direction of change in abundance was uncertain for most species, two species showed a significant increase over time, and forecast models also suggested continuing increases for most species during 2017-2018, as compared to the 2009 base year. Peaks in saturniid abundance were most conspicuous during El Niño and La Niña years. In addition to a species-specific approach, we propose a reproducible functional classification based on five functional traits to analyze the responses of species sharing similar functional attributes in a fluctuating climate. Our results suggest that the abundances of larger body-size species with good dispersal abilities may increase concomitantly with rising air temperature in the future, because short-lived adults may allocate less time to increasing body temperature for flight, leaving more time available for searching for mating partners or suitable oviposition sites.

The population determines whether and how life-history traits vary between reproductive events in an insect with maternal care.

The last reproductive event of a female is often associated with major changes in terms of both maternal and offspring life-history traits. However, the nature of these changes and the importance of population-specific environmental constraints in shaping their expression are difficult to predict and, as a consequence, poorly understood. Here, we investigated whether and how life-history traits vary between reproductive events and whether this variation is population-dependent in the European earwig Forficula auricularia. In this insect species, females produce up to two clutches during their lifetime and express extensive forms of maternal care. We conducted a common garden experiment, in which we measured 11 life-history traits of the first and second clutches of 132 females originating from three populations. Our results showed that clutch size was higher and the level of care expressed towards juveniles lower in second as compared to the first clutches in all three populations. In contrast, we found a population-specific effect on whether and how the reproductive event shaped juvenile quality and a trade-off between egg developmental time and female weight at hatching. Overall, these findings emphasise that the last reproductive event of a female entails both positive and negative effects on various life-history traits of the female herself and her clutch of juveniles. Moreover, our study stresses the importance of population idiosyncrasies on the expression and nature of such cohort-specific effects.