Genitalia are conspicuously variable, even in closely related taxa that are otherwise morphologically very similar. Explaining genital diversity is a longstanding problem that is attracting renewed interest from evolutionary biologists. New studies provide ever more compelling evidence that sexual selection is important in driving genital divergence. Importantly, several studies now link variation in genital morphology directly to male fertilization success, and modern comparative techniques have confirmed predicted associations between genital complexity and mating patterns across species. There is also evidence that male and female genitalia can coevolve antagonistically. Determining mechanisms of genital evolution is an important challenge if we are to resolve current debate concerning the relative significance of mate choice benefits and sexual conflict in sexual selection.

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Sexual selection and genital evolution

The female reproductive tract is where competition between the sperm of different males takes place, aided and abetted by the female herself Intense postcopulatory sexual selection fosters inter-sexual conflict and drives rapid evolutionary change to generate a startling diversity of morphological, behavioural and physiological adaptations We identify three main issues that should be resolved to advance our understanding of postcopulatory sexual selection We need to determine the genetic basis of different male fertility traits and female traits that mediate sperm selection; identify the genes or genomic regions that control these traits; and establish the coevolutionary trajectory of sexes

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Postcopulatory sexual selection.

The outcome of sperm competition is mediated largely by the relative numbers of sperm from competing males. However, substantial variation in features of sperm morphology and behaviour, such as length, longevity and motility, exists and researchers have suggested that this variation functions in postcopulatory sexual selection. Recent studies have determined the effect of these sperm-quality traits on fertilization success and a synthesis of this literature reveals that they are important in both sperm competition and cryptic female choice. To understand how postcopulatory sexual selection influences sperm traits, future research should determine sex-specific interactions that influence paternity, identify genetic correlations between ejaculate characters, quantify the relative costs of producing different sperm traits, and test assumptions of models of sperm quality evolution. Such research will shed light on what evolutionary pressures are responsible for the diversity in sperm morphometry and behaviour.

Sperm in competition: not playing by the numbers.

Rapid evolution of reproductive traits has been attributed to sexual selection arising from interaction between the sexes. However, little is known about the nature of selection driving the evolution of interacting sex-specific phenotypes. Using populations of Drosophila melanogaster selected for divergent sperm length or female sperm-storage organ length, we experimentally show that male fertilization success is determined by an interaction between sperm and female morphology. In addition, sperm length evolution occurred as a correlated response to selection on the female reproductive tract. Giant sperm tails are the cellular equivalent of the peacock's tail, having evolved because females evolved reproductive tracts that selectively bias paternity in favor of males with longer sperm.

https://science.sciencemag.org/content/sci/298/5596/1230.full.pdf

Sperm-female coevolution in Drosophila

Publisher Summary
This chapter reviews the current knowledge of variation in sperm morphology over several levels of biological organization: variation within males (both within and across ejaculates), among males, among populations, and among species, along with prevailing hypotheses addressing the adaptive significance of such variation. With regard to developmental mechanisms, three aspects of the physiology of sperm production serve to limit within-ejaculate variation in sperm phenotypes. First, the location of the testes and numerous aspects of testicular physiology of some taxa are clearly adaptations to maintain a homeostatic developmental environment for sperm. Second, developing spermatids may share cytoplasm. Third, sperm phenotypes are predominantly determined by testicular gene expression and hence the diploid genome of the male. Variation across ejaculates but within males can involve several traits including sperm numbers, overall semen quality and individual sperm quality. A special case of intramale variation in sperm form is found in species with sperm heteromorphism, in which different sperm forms are regularly produced by individuals. Differences among males in sperm morphology may derive from both genetic and environmental influences. Theories of condition-dependence basically posit that fitness-related traits are to a large extent dependent on an organism's underlying condition. Conclusions drawn from studies of sperm diversification between natural populations are reinforced by experimental evolution studies of sperm morphology in laboratory populations, as these studies address the evolvability of sperm traits and the nature of selection underlying sperm diversification. Furthermore, a discussion of evolutionary causes and consequences of sperm diversification, along with suggestions of fruitful areas for future exploration is presented.

Sperm morphological diversity

Females of all species belonging to the family Drosophilidae have two kinds of sperm-storage organs: paired spherical spermathecae and a single elongate tubular seminal receptacle. We examined 113 species belonging to the genus Drosophila and closely allied genera and describe variation in female sperm-storage organ use and morphology. The macroevolutionary pattern of organ dysfunction and morphological divergence suggests that ancestrally both kinds of organs stored sperm. Loss of use of the spermathecae has evolved at least 13 times; evolutionary regain of spermathecal function has rarely if ever occurred. Loss of use of the seminal receptacle has likely occurred only once; in this case, all descendant species possess unusually elaborate spermathecae. Data further indicate that the seminal receptacle is the primary sperm-storage organ in Drosophila. This organ exhibits a pattern of strong correlated evolution with the length of sperm. The evolution of multiple kinds of female sperm-storage organs and the rapidly divergent and correlated evolution of sperm and female reproductive tract morphology are discussed.

Therese Marrow

Papers

Evolution of multiple kinds of female sperm-storage organs in drosophila.