0000000000646220
AUTHOR
Joël Meunier
Parent–offspring conflict and the genetic trade-offs shaping parental investment
The genetic conflict between parents and their offspring is a cornerstone of kin selection theory and the gene-centred view of evolution, but whether it actually occurs in natural systems remains an open question. Conflict operates only if parenting is driven by genetic trade-offs between offspring performance and the parent's ability to raise additional offspring, and its expression critically depends on the shape of these trade-offs. Here we investigate the occurrence and nature of genetic conflict in an insect with maternal care, the earwig Forficula auricularia. Specifically, we test for a direct response to experimental selection on female future reproduction and correlated responses i…
Growing up with feces: benefits of allo-coprophagy in families of the European earwig
International audience
Mother and offspring fitness in an insect with maternal care: phenotypic trade-offs between egg number, egg mass and egg care
Background Oviparous females have three main options to increase their reproductive success: investing into egg number, egg mass and/or egg care. Although allocating resources to either of these three components is known to shape offspring number and size, potential trade-offs among them may have key impacts on maternal and offspring fitness. Here, we tested the occurrence of phenotypic trade-offs between egg number, egg mass and maternal expenditure on egg care in the European earwig, Forficula auricularia, an insect with pre- and post-hatching forms of maternal care. In particular, we used a series of laboratory observations and experiments to investigate whether these three components no…
Multiple paternity and mating group size in the European earwig,Forficula auricularia
The patterns of multiple paternity among the progeny of females are key properties of genetic mating systems. Female multiple mating should evolve due to direct or indirect benefits, but it may also partly be driven by the encounter rate with different potential mates. 2. In this study this hypothesis was experimentally tested in the European earwig (Forficula auricularia L.) by establishing experimental mating groups that differed in the number of males and females (i.e. density). The number of sires and mean sibling relatedness in each clutch were estimated using microsatellite-based paternity analysis. 3. As predicted, the mean number of sires per clutch was significantly increased, and …
Negative association between parental care and sibling cooperation in earwigs: a new perspective on the early evolution of family life?
International audience; The evolution of family life requires net fitness benefits for offspring, which are commonly assumed to mainly derive from parental care. However, an additional source of benefits for offspring is often overlooked: cooperative interactions among juvenile siblings. In this study, we examined how sibling cooperation and parental care could jointly contribute to the early evolution of family life. Specifically, we tested whether the level of food transferred among siblings (sibling cooperation) in the European earwig F orficula auricularia (1) depends on the level of maternal food provisioning (parental care) and (2) is translated into offspring survival, as well as fem…
When earwig mothers do not care to share: Parent–offspring competition and the evolution of family life
Kin competition often reduces – and sometimes entirely negates – the benefits of cooperation among family members. Surprisingly, the impact of kin competition on the fitness effects of family life only received close scrutiny in studies on sibling rivalry, whereas the possibility of parent–offspring competition has attracted much less attention. As a consequence, it remains unclear whether and how parent–offspring competition could have affected the early evolution of parental care and family life. Here, we examined the occurrence and consequences of parent–offspring competition over food access in the European earwig Forficula auricularia, an insect with facultative family life reminiscent…
Age, sex, mating status, but not social isolation interact to shape basal immunity in a group-living insect
International audience; Immunity is a crucial but costly trait. Individuals should therefore adjust their investment into immunity to their condition and infection risks, which are often determined by their age, sex, mating status and social environment. However, whether and how these four key factors can interact to shape basal immunity remains poorly understood. Here, we tested the simultaneous effects of these factors on hemocyte concentration and phenoloxidase activity in adults of the European earwig. We found that hemocyte concentration increased with age, and that this increase was stronger in males. We also found an age-dependent increase in phenoloxidase activity in males and virgi…
Maternal care provides antifungal protection to eggs in the European earwig
Many insects raise their offspring on organic substrates or in the soil where microorganisms are abundant. Microbes may pose a serious threat to offspring development and survival by either decomposing food resources or directly infecting the offspring. Selection to cope with these effects may favor social defenses, for example, through forms of parental care that can limit or eliminate these threats to offspring fitness. In this study, we experimentally tested if maternal egg attendance in the European earwig Forficula auricularia has a function as a social defense against mold infection of eggs by manipulating exposure of eggs to mold spores and the presence of the mother in a fully facto…
Sibling cooperation in earwig families provides insights into the early evolution of social life.
The evolutionary transition from solitary to social life is driven by direct and indirect fitness benefits of social interactions. Understanding the conditions promoting the early evolution of social life therefore requires identification of these benefits in nonderived social systems, such as animal families where offspring are mobile and able to disperse and will survive independently. Family life is well known to provide benefits to offspring through parental care, but research on sibling interactions generally focused on fitness costs to offspring due to competitive behaviors. Here we show experimentally that sibling interactions also reflect cooperative behaviors in the form of food sh…
Influences of Relatedness, Food Deprivation, and Sex on Adult Behaviors in the Group-living Insect Forficula auricularia
The evolution of group living is generally associated with the emergence of social behaviors that ensure fitness benefits to group members. However, the expression of these behaviors may depend on group composition, which can vary over time with respect to sex, starvation status, and relatedness. Here, we investigated (1) whether adults of the group-living European earwig, Forficula auricularia, show cooperative behaviors toward conspecifics and (2) whether sex, food availability, and relatedness shape the nature and frequency of these behaviors. We conducted a full-factorial experiment using 108 unisexual pairs of adults, in which we manipulated these three factors and video-recorded the e…
Feces production as a form of social immunity in an insect with facultative maternal care
Background Social animals have the unique capability of mounting social defenses against pathogens. Over the last decades, social immunity has been extensively studied in species with obligatory and permanent forms of social life. However, its occurrence in less derived social systems and thus its role in the early evolution of group-living remains unclear. Here, we investigated whether lining nests with feces is a form of social immunity against microbial growth in the European earwig Forficula auricularia, an insect with temporary family life and facultative maternal care. Results Using a total of 415 inhibition zone assays, we showed that earwig feces inhibit the growth of two GRAM+ bact…
Inbreeding depression in an insect with maternal care: influences of family interactions, life stage and offspring sex.
Although inbreeding is commonly known to depress individual fitness, the severity of inbreeding depression varies considerably across species. Among the factors contributing to this variation, family interactions, life stage and sex of offspring have been proposed, but their joint influence on inbreeding depression remains poorly understood. Here, we demonstrate that these three factors jointly shape inbreeding depression in the European earwig, Forficula auricularia. Using a series of cross-breeding, split-clutch and brood size manipulation experiments conducted over two generations, we first showed that sib mating (leading to inbred offspring) did not influence the reproductive success of…
Offspring reverse transcriptome responses to maternal deprivation when reared with pathogens in an insect with facultative family life
Offspring of species with facultative family life are able to live with and without parents (i.e. to adjust to extreme changes in their social environment). While these adjustments are well understood on a phenotypic level, their genetic underpinnings remain surprisingly understudied. Investigating gene expression changes in response to parental absence may elucidate the genetic constraints driving evolutionary transitions between solitary and family life. Here, we manipulated maternal presence to observe gene expression changes in the fat body of juvenile European earwigs, an insect with facultative family life. Because parents typically protect offspring against pathogens, expression chan…
Maternal condition determines offspring behavior toward family members in the European earwig
International audience; Parental care confers benefits to juveniles but is usually associated with substantial costs for parents. These costs often depend on parental condition, which is thus considered as a key determinant of the level of parental care expressed during family life. However, how parental condition affects the behaviors that juveniles express toward their siblings and parents remains poorly explored. Here, we investigated these questions in the European earwig Forficula auricularia, an insect in which mothers provide extensive forms of care to their juveniles. We measured maternal body condition at egg hatching, subsequently manipulated maternal nutritional state, and finall…
Paternal signature in kin recognition cues of a social insect: concealed in juveniles, revealed in adults
Kin recognition is a key mechanism to direct social behaviours towards related individuals or avoid inbreeding depression. In insects, recognition is generally mediated by cuticular hydrocarbon (CHC) compounds, which are partly inherited from parents. However, in social insects, potential nepotistic conflicts between group members from different patrilines are predicted to select against the expression of patriline-specific signatures in CHC profiles. Whereas this key prediction in the evolution of insect signalling received empirical support in eusocial insects, it remains unclear whether it can be generalized beyond eusociality to less-derived forms of social life. Here, we addressed this…
Condition-Dependent Trade-Off Between Weapon Size and Immunity in Males of the European Earwig
Abstract Investigating the expression of trade-offs between key life-history functions is central to our understanding of how these functions evolved and are maintained. However, detecting trade-offs can be challenging due to variation in resource availability, which masks trade-offs at the population level. Here, we investigated in the European earwig Forficula auricularia whether (1) weapon size trades off with three key immune parameters – hemocyte concentration, phenoloxidase and prophenoloxidase activity - and whether (2) expression and strength of these trade-offs depend on male body condition (body size) and/or change after an immune challenge. Our results partially confirmed conditi…
Surrounding pathogens shape maternal egg care but not egg production in the European earwig
Earwig mothers increase egg care when pathogens are present in the nest, but do not adapt the quantity and quality of their eggs accordingly. Our results confirm that parents can both detect the presence of microbial pathogens in their nesting area and develop pre-hatching behavioral strategies to reduce the associated risk of pathogen infection. These findings overall emphasize the central importance of pathogens in the evolution of parental care in animals.Twitter: @JMeunierEarwig
Survival after pathogen exposure in group-living insects: don't forget the stress of social isolation!
A major cost of group-living is its inherent risk of pathogen infection. To limit this risk, many group-living animals have developed the capability to prophylactically boost their immune system in the presence of group members and/or to mount collective defences against pathogens. These two phenomena, called density-dependent prophylaxis and social immunity, respectively, are often used to explain why, in group-living species, individuals survive better in groups than in isolation. However, this survival difference may also reflect an alternative and often overlooked process: a cost of social isolation on individuals' capability to fight against infections. Here, we disentangled the effect…
Kin and multilevel selection in social evolution: a never-ending controversy?
Kin selection and multilevel selection are two major frameworks in evolutionary biology that aim at explaining the evolution of social behaviors. However, the relationship between these two theories has been plagued by controversy for almost half a century and debates about their relevance and usefulness in explaining social evolution seem to rekindle at regular intervals. Here, we first provide a concise introduction into the kin selection and multilevel selection theories and shed light onto the roots of the controversy surrounding them. We then review two major aspects of the current debate: the presumed formal equivalency of the two theories and the question whether group selection can …
Short-term benefits, but transgenerational costs of maternal loss in an insect with facultative maternal care
A lack of parental care is generally assumed to entail substantial fitness costs for offspring that ultimately select for the maintenance of family life across generations. However, it is unknown whether these costs arise when parental care is facultative, thus questioning their fundamental importance in the early evolution of family life. Here, we investigated the short-term, long-term and transgenerational effects of maternal loss in the European earwig Forficula auricularia , an insect with facultative post-hatching maternal care. We showed that maternal loss did not influence the developmental time and survival rate of juveniles, but surprisingly yielded adults of larger body and force…
PO-CALC: A novel tool to correct common inconsistencies in the measurement of phenoloxidase activity
Abstract A broad range of physiological and evolutionarily studies requires standard and robust methods to assess the strength and activity of an individual’s immune defense. In insects, this goal is generally reached by spectrophotometrically measuring (pro-) phenoloxidase activity, an enzymatic and non-specific process activated after wounding and parasite infections. However, the literature surprisingly lacks a standard method to calculate these values from spectrophotometer data and thus to be able to compare results across studies. In this study, we demonstrated that nine methods commonly used to extract phenoloxidase activities (1) provide inconsistent results when tested on the same …
Social immunity and the evolution of group living in insects
The evolution of group living requires that individuals limit the inherent risks of parasite infection. To this end, group living insects have developed a unique capability of mounting collective anti-parasite defences, such as allogrooming and corpse removal from the nest. Over the last 20 years, this phenomenon (called social immunity) was mostly studied in eusocial insects, with results emphasizing its importance in derived social systems. However, the role of social immunity in the early evolution of group living remains unclear. Here, I investigate this topic by first presenting the definitions of social immunity and discussing their applications across social systems. I then provide a…
Friend or foe? The apparent benefits of gregarine (Apicomplexa: Sporozoa) infection in the European earwig
International audience; Studying the costs and benefits of host-parasite interactions is of central importance to shed light on the evolutionary drivers of host life history traits. Although gregarines (Apicomplexa: Sporozoa) are one of the most frequent parasites in the gut of invertebrates, the diversity of its potential impacts on a host remains poorly explored. In this study, we addressed this gap in knowledge by investigating the prevalence of natural infections by the gregarine Gregarina ovata and testing how these infections shape a large set of morphological, behavioural and physiological traits in the European earwig Forficula auricularia. Our results first show that G. ovata was p…
Social immunity: why we should study its nature, evolution and functions across all social systems.
Mounting defences against pathogens is a necessity for all animals. Although these defences have long been known to rely on individual processes such as the immune system, recent studies have emphasized the importance of social defences for group-living hosts. These defences, called social immunity, have been mostly studied in eusocial insects such as bees, termites and ants, and include, for instance, mutual cleaning and waste management. Over the last few years, however, a growing number of works called for a broader exploration of social immunity in non-eusocial species. In this review, we summarize the rationales of this call and examine why it may provide major insights into our curren…
The evolution of parental care in insects: the roles of ecology, life history and the social environment
Parental care increases the fitness of offspring at a cost to the parents in terms of residual reproductive success. This trade-off may be affected by ecology, life history and the social environment, which raises the question as to how these factors contribute to the evolution of parental care. Here, previous hypotheses concerning the evolution of parental care in insects are summarized and discussed and the underlying empirical evidence is reviewed. Ecological factors such as harsh environments, ephemeral food sources or predation pressure are broadly accepted as evolutionary drivers of parental care. The most consistent evidence supports a role for natural enemies such as predators, micr…
Extended winters entail long-term costs for insect offspring reared in an overwinter burrow
International audience; Winter imposes an ecological challenge to animals living in colder climates, especially if these adverse conditions coincide with reproduction and offspring rearing. To overcome this challenge, some insects burrow in the soil to protect adults, larvae, or eggs from negative effects of winter. However, whether this protection is effective against any long-term consequences of changes in winter duration is unclear. Here, we investigated the long-term effects of winter length variation on eggs of the European earwig Forficula auricularia. In this insect, females construct and maintain a burrow between late autumn and spring, in which they provide extensive forms of care…
Data from: Growing up with feces: benefits of allo-coprophagy in families of the European earwig
An important issue in the evolution of group living is the risk of pathogen and predator exposure entailed by the inherent accumulation of feces within a nesting site. While many group living species limit this risk by cleaning the nest, others do not, raising questions about the benefits of maintaining feces in the nest and their importance in social evolution. Here, we investigated whether one of these benefits could be mediated by coprophagy in families of the European earwig, Forficula auricularia. In this insect species, mothers and mobile juveniles (nymphs) line their nests with feces and consume them. In a first experiment, we tested whether access to feces produced by either nymphs …
Data from: Paternal signature in kin recognition cues of a social insect: concealed in juveniles, revealed in adults
Kin recognition is a key mechanism to direct social behaviours towards related individuals or avoid inbreeding depression. In insects, recognition is generally mediated by cuticular hydrocarbon (CHC) compounds, which are partly inherited from parents. However, in social insects, potential nepotistic conflicts between group members from different patrilines are predicted to select against the expression of patriline-specific signatures in CHC profiles. Whereas this key prediction in the evolution of insect signalling received empirical support in eusocial insects, it remains unclear whether it can be generalized beyond eusociality to less-derived forms of social life. Here, we addressed this…
Data from: When earwig mothers do not care to share: parent-offspring competition and the evolution of family life
1. Kin competition often reduces – and sometimes entirely negates – the benefits of cooperation among relatives, and hence is often regarded as central process in social evolution. Surprisingly, however, our understanding of the role of kin competition in the evolution of family life remains fragmentary, despite the close scrutiny it received in studies on sibling rivarly. This is because much less attention has been given to local competition between parents and their offspring, and its potential impact on the early evolution of parental care and family life. 2. Here, we examined mother-offspring competition over food access in the European earwig Forficula auricularia, an insect with facu…
Data from: Survival after pathogen exposure in group-living insects: don’t forget the stress of social isolation!
A major cost of group-living is its inherent risk of pathogen infection. To limit this risk, many group-living animals have developed the capability to prophylactically boost their immune system in the presence of group members and/or to mount collective defenses against pathogens. These two phenomena, called density dependent prophylaxis and social immunity, respectively, are often used to explain why, in group-living species, individuals survive better in groups than in isolation. However, this survival difference may also reflect an alternative and often overlooked process: a cost of social isolation on individuals’ capability to fight against infections. Here, we disentangled the effect…
Data from: Short-term benefits, but transgenerational costs of maternal loss in an insect with facultative maternal care
A lack of parental care is generally assumed to entail substantial fitness costs for offspring that ultimately select for the maintenance of family life across generations. However, it is unknown whether these costs arise when parental care is facultative, thus questioning their fundamental importance in the early evolution of family life. Here, we investigated the short-term, long-term and transgenerational effects of maternal loss in the European earwig Forficula auricularia, an insect with facultative post-hatching maternal care. We showed that maternal loss did not influence the developmental time and survival rate of juveniles, but surprisingly yielded adults of larger body and forceps…
Data from: Surrounding pathogens shape maternal egg care but not egg production in the European earwig
Pathogens are ubiquitous in nature and typically entail major fitness costs in their hosts. These costs can be particularly important when individuals exhibit poor immune defenses, as it is often the case during early developmental stages. Hence, selection should favor parental strategies limiting the risks of pathogen exposure and infection in their offspring. In this study, we investigated 1) whether females of the European earwig Forficula auricularia avoid areas contaminated with spores of the entomopathogenic fungus Metarhizium brunneum prior to and at egg laying, as well as 2) whether spore presence entails an increase in females’ investment into both pre-hatching forms of care and cl…
Data from: Sibling cooperation in earwig families provides insights into the early evolution of social life
The evolutionary transition from solitary to social life is driven by direct and indirect fitness benefits of social interactions. Understanding the conditions promoting the early evolution of social life therefore requires identification of these benefits in nonderived social systems, such as animal families where offspring are mobile and able to disperse and will survive independently. Family life is well known to provide benefits to offspring through parental care, but research on sibling interactions generally focused on fitness costs to offspring due to competitive behaviors. Here we show experimentally that sibling interactions also reflect cooperative behaviors in the form of food sh…
Figure S1 from Offspring reverse transcriptome responses to maternal deprivation when reared with pathogens in an insect with facultative family life
Genes affected by the presence of the pathogen, independently of maternal presence. Y-axis represents normalized expression across samples per gene (Z-Score).
Data from: Negative association between parental care and sibling cooperation in earwigs: a new perspective on the early evolution of family life?
The evolution of family life requires net fitness benefits for offspring, which are commonly assumed to mainly derive from parental care. However, an additional source of benefits for offspring is often overlooked: cooperative interactions among juvenile siblings. In this study, we examined how sibling cooperation and parental care could jointly contribute to the early evolution of family life. Specifically, we tested whether the level of food transferred among siblings (sibling cooperation) in the European earwig Forficula auricularia (1) depends on the level of maternal food provisioning (parental care), and (2) is translated into offspring survival, as well as female investment into futu…
Data from: Mother and offspring fitness in an insect with maternal care: phenotypic trade-offs between egg number, egg mass and egg care
Background: Oviparous females have three main options to increase their reproductive success: investing into egg number, egg mass and/or egg care. Although allocating resources to either of these three components is known to shape offspring number and size, potential trade-offs among them may have key impacts on maternal and offspring fitness. Here, we tested the occurrence of phenotypic trade-offs between egg number, egg mass and maternal expenditure on egg care in the European earwig, Forficula auricularia, an insect with pre- and post-hatching forms of maternal care. In particular, we used a series of laboratory observations and experiments to investigate whether these three components n…
Tables S1 & S2 from Offspring reverse transcriptome responses to maternal deprivation when reared with pathogens in an insect with facultative family life
Table S1. Comparisons of different transcriptome assemblies. The table on the sheet "Transrate output" shows data obtained using Transrate v.1.03 (Smith-unna et al., 2016). We compared assemblies created using Trinity and CLC Assembly Cell, as well as a merged "hybrid" obtained using CAP3 (Huang and Madan, 1999). The assembly comparison was used to determine the best assembly for continued analyses. Table S2. Full list of all DEGs revealed by the LRTs testing for main and interaction effects, as well as the associated annotations and read counts per sample. Note that no DEGs depended on maternal presence alone. Table headers are default DEseq2 headers, while the Blast annotation was added b…