Male inbreeding status affects female fitness in a seed‐feeding beetle

Abstract

Inbreeding generally reduces male mating activity such that inbred males are less successful in male–male competition. Inbred males can also have smaller accessory glands, transfer less sperm and produce sperm that are less motile, less viable or have a greater frequency of abnormalities, all of which can reduce the fertilization success and fitness of inbred males relative to outbred males. However, few studies have examined how male inbreeding status affects the fitness of females with whom they mate. In this study, we examine the effect of male inbreeding status (inbreeding coefficient f = 0.25 vs. f = 0) on the fecundity, adult longevity and the fate of eggs produced by outbred females in the seed‐feeding beetle, Callosobruchus maculatus. Females mated to inbred males were less likely to lay eggs. Of those that laid eggs, females mated to inbred males laid 6–12% fewer eggs. Females mated to inbred males lived on average 5.4% longer than did females mated to outbred males, but this effect disappeared when lifetime fecundity was used as a covariate in the analysis. There was no effect of male inbreeding status on the proportion of a female’s eggs that developed or hatched, and no evidence that inbred males produced smaller nuptial gifts. However, ejaculates of inbred males contained 17–33% fewer sperm, on average, than did ejaculates of outbred males. Our study demonstrates that mating with inbred males has significant direct consequences for the fitness of female C. maculatus, likely mediated by effects of inbreeding status on the number of sperm in male ejaculates. Direct effects of male inbreeding status on female fitness should be more widely considered in theoretical models and empirical studies of mate choice.

Effect of Inbreeding on Host Discrimination and Other Fitness Components in a Seed Beetle

“…Eggs produced by inbred females may also be inferior at the stage of egg formation and provisioning. A previous study of C. maculatus found that inbred males produce fewer sperm (Fox et al 2012), so it is possible that inbred females experience similar problems during oogenesis, which could reduce both egg number and quality. Given our broad deÞnition of egg hatch, more detailed studies can reveal whether eggs laid by inbred females exhibit reduced embryogenesis, greater larval mortality before seed entry, or both (Fox et al 2007).…”

“…Periods of inbreeding may be common in these stored-product pests, because populations in stores of grain legumes are often founded by small numbers of individuals that emerge from Þeld-infested or transported seeds Credland 1995, Semeao et al 2012). Beetle populations in both the Þeld and laboratory exhibit substantial inbreeding depression for such traits as larval survival and development time, adult body size and lifespan, and male and female reproduction (Tran and Credland 1995;Fox et al , 2007Fox et al , 2012. Inbreeding depression for some beetle traits (e.g., survival) increases with the stressfulness of the environment (Fox andReed 2010, Fox et al 2011).…”

Influence of Inbreeding on Female Mate Choice in Two Species of Drosophila

“…Female mice ( Mus musculus musculus ) prefer the scent of outbred males to inbred males when both were infected with salmonella (Ilmonen et al 2009) and female mealworm beetles ( Tenebrio molitor ) prefer the scent of outbred males to inbred males (Pölkki et al 2012), but Aparicio et al (2001) found that males of spotless starling ( Sturnus unicolor ) with an intermediate level of heterozygosity were more successful in mating and reproduction than either of the extremes. These preferences may arise from reduced fitness in females who mate with inbred males instead of outbred ones as demonstrated in seed-feeding beetles (Fox et al 2012). …”

Female mating preferences for outbred versus inbred males are conditional upon the female's own inbreeding status

“…Firstly, the costs of inbreeding these preferences for outbred males are unlikely to be driven by indirect (genetic) benefits, 60 because homozygosity is not heritable (Reinhold, 2002;Lehmann et al, 2007; but see Neff and 61 Pitcher, 2008; Nietlisbach et al, 2015). A more likely explanation is that inbreeding reduces 62 overall male quality and condition such that females gain fewer direct benefits from mating with 63 an inbred male (Fox et al, 2012). Direct benefits that may be affected by inbreeding include 64 sperm number and quality, nuptial gift size, and parental care ability (Fox et al, 2012 …”

“…A more likely explanation is that inbreeding reduces 62 overall male quality and condition such that females gain fewer direct benefits from mating with 63 an inbred male (Fox et al, 2012). Direct benefits that may be affected by inbreeding include 64 sperm number and quality, nuptial gift size, and parental care ability (Fox et al, 2012 …”