Experimental evidence for sexual selection against inbred males

Abstract

The detrimental effects of matings between relatives are well known. However, few studies determine the extent to which inbreeding depression in males is due to natural or sexual selection. Importantly, measuring fitness or key fitness components, rather than phenotypic traits allows more accurate estimation of inbreeding depression. We investigate how differences in inbreeding and juvenile diet (i.e. early stressful environment) influence a key component of male fitness, namely their reproductive success. We experimentally created inbred and outbred male mosquitofish (Gambusia holbrooki) by mating full-sibs (f = 0·25). We show that this led to a 23% reduction in genome-wide heterozygosity based on SNPs. Males were raised on different diets early in life to create high-stress and low-stress rearing environments. We then allowed adult males to compete freely for females to test if inbreeding, early diet and their interaction affect a male's share of paternity. Early diet had no effect on paternity, but outbred males sired almost twice as many offspring as inbred males (n = 628 offspring from 122 potential sires). Using artificial insemination methods we determined that this was unlikely to be due to early embryo mortality of eggs fertilised by inbred males: there was no evidence that male inbreeding status affects the realised fecundity of females (n = 288). Given there was no difference in male mortality in our competitive mating experiment, the lower reproductive success of inbred males can most parsimoniously be attributed to inbreeding negatively affecting sexually selected traits that affect male mating success and/or sperm competitiveness. We discuss which sexually selected traits might be involved.

Indirect fitness benefits through extra‐pair mating are large for an inbred minority, but cannot explain widespread infidelity among red‐winged fairy‐wrens

“…Inbreeding depression has often been found to reduce fertility, for example through reduced male attractiveness (Pilakouta and Smiseth ; Vega‐Trejo et al. ) or reduced parental care behaviors, such as female incubation attentiveness (Pooley et al. ).…”

“…In addition to inbreeding depression early in life, inbred adults were less likely to successfully raise a brood to fledging, and this was not caused by inbred adults having less opportunity due to lower chances of obtaining a dominant position. Inbreeding depression has often been found to reduce fertility, for example through reduced male attractiveness (Pilakouta and Smiseth 2017;Vega-Trejo et al 2017) or reduced parental care behaviors, such as female incubation attentiveness (Pooley et al 2014). Future work will have to show what the underlying mechanisms of the lower reproductive success of inbred individuals are.…”

Stabilizing selection on sperm number revealed by artificial selection and experimental evolution

“…) to avoid effects of ageing on reproduction and mortality (e.g., Vega‐Trejo et al. ). Females were individually isolated when visibly pregnant, and tanks were controlled three times per day until parturition.…”

“…In each generation, selected males were individually housed with two unrelated virgin females from the same replicate and selection line in a 3.5 L tank. Males (and females) were allowed to reproduce at an age of about five months, when all fish are sexually mature (Magurran 2005) but before reproductive and/or somatic senescence occurs (e.g., Miller and Brooks 2005;Gasparini et al 2010) to avoid effects of ageing on reproduction and mortality (e.g., Vega-Trejo et al 2017). Females were individually isolated when visibly pregnant, and tanks were controlled three times per day until parturition.…”

The effects of male age, sperm age and mating history on ejaculate senescence

“…Males persistently attempt to copulate (up to one attempt/ minute; Wilson, 2005). Females are polyandrous (Evans, 2011) and typically produce broods sired by multiple males (Booksmythe, Head, Keogh, & Jennions, 2016;Head, Kahn, Henshaw, Keogh, & Jennions, 2017;Vega-Trejo, Head, Keogh, & Jennions, 2017;Zane, Jones, & Avise., 1999). Sperm competition is therefore likely to be intense.…”