How sexual selection can drive the evolution of costly sperm ornamentation

Abstract

Post-copulatory sexual selection (PSS), fuelled by female promiscuity, is credited with the rapid evolution of sperm quality traits across diverse taxa. Yet, our understanding of the adaptive significance of sperm ornaments and the cryptic female preferences driving their evolution is extremely limited. Here we review the evolutionary allometry of exaggerated sexual traits (for example, antlers, horns, tail feathers, mandibles and dewlaps), show that the giant sperm of some Drosophila species are possibly the most extreme ornaments in all of nature and demonstrate how their existence challenges theories explaining the intensity of sexual selection, mating-system evolution and the fundamental nature of sex differences. We also combine quantitative genetic analyses of interacting sex-specific traits in D. melanogaster with comparative analyses of the condition dependence of male and female reproductive potential across species with varying ornament size to reveal complex dynamics that may underlie sperm-length evolution. Our results suggest that producing few gigantic sperm evolved by (1) Fisherian runaway selection mediated by genetic correlations between sperm length, the female preference for long sperm and female mating frequency, and (2) longer sperm increasing the indirect benefits to females. Our results also suggest that the developmental integration of sperm quality and quantity renders post-copulatory sexual selection on ejaculates unlikely to treat male-male competition and female choice as discrete processes.

Altitude underlies variation in the mating system, somatic condition, and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis)

“…These results are consistent with previous reports of condition-dependent testis size in diverse taxa (Simmons and Kotiaho 2002;Schulte-Hostedde and Millar 2004;Schulte-Hostedde et al 2005;Burness et al 2008). Sperm production can be energetically costly (Dewsbury 1982;Olsson et al 1997;Thomsen et al 2006), and so males of superior somatic condition may have relatively more energy available to invest in it, thereby increasing competitive fertilization success and ultimately gaining evolutionary benefits (Preston et al 2003;Lüpold et al 2016). Sperm number (and hence testis size) is particularly important and strongly selected for in external fertilizers, in which environmental stressors can greatly reduce sperm survival and thus fertilization success (Morisawa et al 1983;Billard et al 1986).…”

“…Sperm production is energetically costly (Dewsbury 1982;Olsson et al 1997;Thomsen et al 2006), and so highcondition males may have greater energy reserves to invest in sperm production, thereby gaining evolutionary benefits (Preston et al 2003;Lüpold et al 2016). We thus tested whether variation in testis size reflected differential somatic condition among populations.…”

What do isogamous organisms teach us about sex and the two sexes?

“…Another factor that makes a reversal to isogamy difficult is that anisogamous species have achieved tight linkage or sex-limitation of expression of sizedetermining loci, which can block the evolutionary path from anisogamy back to isogamy [67]. Despite these stabilizing factors, there are known cases where 'giant sperm' have evolved secondarily [87][88][89], approaching isogamy in terms of size; such special cases are, however, quite different from an actual evolutionary reversal to morphological similarity, because a clear sperm-egg dichotomy in morphological traits is maintained.…”

Quantity versus quality: the sperm war

“…However, the evolution of germ size has not been fully exploited. The most recent study by Lüpold et al 1. reveals that the evolution of longer sperm is driven by the female seminal receptacle and mating frequency in Drosophila , which, in turn, increases the benefits to females.…”

“…In their most recent paper, Lüpold et al 1. extended their previous work and further evaluated the genetic and phenotypic correlations, as well as heritabilities in sperm length, SR length, remating day, ejection time, and the proportion of resident spermatozoa that are thoroughly displaced within diallel crosses.…”