Transgenerational effects of maternal sexual interactions in seed beetles

Abstract

Mating often bears large costs to females, especially in species with high levels of sexual conflict over mating rates. Given the direct costs to females associated with multiple mating, which include reductions in lifespan and lifetime reproductive success, past research focused on identifying potential indirect benefits (through increases in offspring fitness) that females may accrue. Far less attention has, however, been devoted to understanding how costs of sexual interactions to females may extend across generations. Hence, little is known about the transgenerational implications of variation in mating rates, or the net consequences of maternal sexual activities across generations. Using the seed beetle, Callosobruchus maculatus, a model system for the study of sexual conflict, we investigate the effects of mating with multiple males versus a single male, and tease apart effects due to sexual harassment and those due to mating per se, over three generations. A multigenerational analysis indicated that females that were exposed to ongoing sexual harassment and who also were permitted to mate with multiple males showed no difference in net fitness compared to females that mated just once without ongoing harassment. Intriguingly, however, females that were continually harassed, but permitted to mate just once, suffered a severe decline in net fitness compared to females that were singly (not harassed) or multiply mated (harassed, but potentially gaining benefits via mating with multiple males). Overall, the enhanced fitness in multiply mated compared to harassed females may indicate that multiple mating confers transgenerational benefits. These benefits may counteract, but do not exceed (i.e., we found no difference between singly and multiply mated females), the large transgenerational costs of harassment. Our study highlights the importance of examining transgenerational effects from an inclusive (looking at both indirect benefits but also costs) perspective, and the need to investigate transgenerational effects across several generations if we are to fully understand the consequences of sexual interactions, sexual conflict evolution, and the interplay of sexual conflict and multi-generational costs and benefits.

Temperature as a modulator of sexual selection

“…direct or female‐moderated paternal effects arising from variation in the non‐sperm fraction of the ejaculate (Garcia‐Gonzalez & Simmons, 2007; Gasparini et al ., 2018)]. However, any inter‐generational or trans‐generational effect has the capacity to significantly alter the economics of sexual interactions (Dowling, Williams, & Garcia‐Gonzalez, 2014; Zajitschek et al ., 2018), leading to unknown but presumably significant effects on sexual selection. We anticipate that investigations focusing on how temperature‐driven maternal and paternal effects impact sexual selection will yield important insights.…”

An experimental test for body size‐dependent effects of male harassment and an elevated copulation rate on female lifetime fecundity and offspring performance

“…In general, experimental studies show that females continuously housed with males have lower fitness than females that only have intermittent access to males (Edvardsson, ; Lew, Morrow, & Rice, ; Rönn et al , ). In most of these studies, however, researchers cannot determine the relative effects of the actual rate of copulation from those of male sexual harassment: the increased presence of males leads to both greater male harassment and a higher mating rate (but see Fox, Head, & Jennions, ; den Hollander & Gwynne, ; Partridge & Fowler, ; Zajitschek, Dowling, Head, Rodriguez‐Exposito, & Garcia‐Gonzalez, ). The distinction between these two processes matters.…”

“…For example, females might allocate fewer resources to eggs or decrease parental care to ameliorate costs of repeated copulation or greater male harassment. To date, the effects of increased male presence on offspring fitness have rarely been quantified (Brommer, Fricke, Edward, & Chapman, 2012;Le Galliard, Cote, & Fitze, 2008;Priest, Galloway, & Roach, 2008;Zajitschek et al, 2018) and studies have found conflicting results, even within a species. For example, Dowling, Williams, and Garcia-Gonzalez (2014) showed that female Drosophila melanogaster experiencing more sexual interactions produced offspring with lower survival and higher rates of senescence, whereas Priest et al (2008) found that females that mated more often produced daughters with greater lifetime reproductive success.…”

Disentangling the costs of male harassment and the benefits of polyandry for females

“…In those studies that come closest, the level of male harassment is varied while controlling for the cost of mating (i.e. female only mated once), but the individual effects of polyandry and male harassment are conflated in treatments where increased harassment and increased number of mates is associated with an increased mating rate (den Hollander and Gwynne 2009;Zajitschek et al 2018). More studies that use our design to simultaneously examine the effects of male harassment and polyandry, while controlling for the actual mating rate are needed to quantify how costly male sexual harassment really is for females.…”

“…To our knowledge, only one study has simultaneously examined the costs/benefits of male sexual harassment and polyandry (i.e. number of males inseminating) while controlling for the mating rate (Zajitschek et al 2018).…”