Short-term benefits, but transgenerational costs of maternal loss in an insect with facultative maternal care

Abstract

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 size, two traits associated with fitness benefits. In a cross-breeding/ cross-fostering experiment, we then demonstrated that maternal loss impaired the expression of maternal care in adult offspring. Interestingly, the resulting transgenerational costs were not only mediated by the early-life experience of tending mothers, but also by inherited, parent-of-origin-specific effects expressed in juveniles. Orphaned females abandoned their juveniles for longer and fed them less than maternally-tended females, while foster mothers defended juveniles of orphaned females less well than juveniles of maternally-tended females. Overall, these findings reveal the key importance of transgenerational effects in the early evolution of family life.

When earwig mothers do not care to share: Parent–offspring competition and the evolution of family life

“…Specifically, mother–offspring competition does not seem to have handicapped low‐quality offspring to an extent that favoured the survival and development of higher‐quality offspring, as the average size of maternally tended offspring should have been larger than that of non‐tended juveniles in this scenario (Mock & Parker, ; Simmons, ). Nevertheless, our results showed that adults were overall smaller when they had been raised with their mother, a negative effect of maternal presence that has already been found under favourable conditions (featuring unrestricted food access) and that might result from maternal behaviours that are maladaptive under laboratory conditions (such as the burying of food, presumably to prevent microbial growth; see Thesing et al., ). Our results also revealed that males were overall smaller but had longer forceps than females, confirming the sexual dimorphism of these morphological traits (Radesäter & Halldórsdóttir, ; Thesing et al., ).…”

“…Nevertheless, our results showed that adults were overall smaller when they had been raised with their mother, a negative effect of maternal presence that has already been found under favourable conditions (featuring unrestricted food access) and that might result from maternal behaviours that are maladaptive under laboratory conditions (such as the burying of food, presumably to prevent microbial growth; see Thesing et al., ). Our results also revealed that males were overall smaller but had longer forceps than females, confirming the sexual dimorphism of these morphological traits (Radesäter & Halldórsdóttir, ; Thesing et al., ). Finally, we showed that body size generally decreased with increasing weight gains of mothers during first brood family life.…”

“…However, post‐hatching maternal presence and care are not obligatory for offspring survival (Kölliker, ; Kölliker & Vancassel, ), as nymphs can forage independently soon after hatching (relying on the same food resources than their mother; Lamb, ) and may even obtain food from their siblings (Falk, Wong, Kölliker, & Meunier, ; Kramer, Thesing, & Meunier, ). Consequently, the cost‐benefit ratio of maternal presence in F. auricularia generally depends on the environmental conditions experienced by mothers and nymphs during family life (Kölliker, ; Meunier & Kölliker, ; Thesing, Kramer, Koch, & Meunier, ).…”

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

“…This is important, as it reveals that these effects are not determined by the environmental conditions experienced during family life, but instead depend on the conditions experienced during female development and/or on (the conditions that have shaped) the evolutionary history of the population. In line with the first hypothesis, the quality of the environment experienced by F. auricularia juveniles during their development is known to affect the lifehistory traits of the resulting adults, for instance in terms of investment into second clutch production and maternal care (Wong and Kölliker 2014;Thesing et al 2015). Conversely, harsh winter conditions have been suggested to select for a delayed production of first clutch eggs , which may benefit females by shortening the developmental time of their first clutch eggs and thus allowing the mothers to exhibit a higher condition (i.e.…”

“…Here, we addressed these questions by comparing a total of 11 life-history traits measured in the first and second clutches of 132 F. auricularia females sampled in three distant populations in Europe. These traits encompassed measures of clutch quantity and quality, maternal condition during post-hatching family interactions, as well as the expression of brood defence and food provisioning, two important forms of post-hatching maternal care (Meunier and Kölliker 2012;Thesing et al 2015).…”