Female reproductive tract form drives the evolution of complex sperm morphology

Abstract

The coevolution of female mate preferences and exaggerated male traits is a fundamental prediction of many sexual selection models, but has largely defied testing due to the challenges of quantifying the sensory and cognitive bases of female preferences. We overcome this difficulty by focusing on postcopulatory sexual selection, where readily quantifiable female reproductive tract structures are capable of biasing paternity in favor of preferred sperm morphologies and thus represent a proximate mechanism of female mate choice when ejaculates from multiple males overlap within the tract. Here, we use phylogenetically controlled generalized least squares and logistic regression to test whether the evolution of female reproductive tract design might have driven the evolution of complex, multivariate sperm form in a family of aquatic beetles. The results indicate that female reproductive tracts have undergone extensive diversification in diving beetles, with remodeling of size and shape of several organs and structures being significantly associated with changes in sperm size, head shape, gains/losses of conjugation and conjugate size. Further, results of Bayesian analyses suggest that the loss of sperm conjugation is driven by elongation of the female reproductive tract. Behavioral and ultrastructural examination of sperm conjugates stored in the female tract indicates that conjugates anchor in optimal positions for fertilization. The results underscore the importance of postcopulatory sexual selection as an agent of diversification.ornaments | sperm competition | heteromorphism | genitalia | spermatheca D arwin attributed the evolution of many elaborate male traits to selection exerted by female mate discrimination (1). Female choosiness remains a foundation of sexual selection theory, with most models predicting a pattern of coevolution between female preference and exaggerated male traits (2). The role of cognition, however, renders preferences notoriously difficult to quantify, with constraints on the timing of reproduction, risks associated with mate evaluation, and environmental influences on female perception of mate quality further complicating matters (3). Consequently, few studies have attempted to test macroevolutionary patterns of codiversification of female preference and male traits, and those that do have very limited taxon sampling (4, 5).As with male traits important for mate choice, some sperm attributes exhibit high levels of morphological variation within species (6, 7) and dramatic divergence among species (7). This variation has been widely attributed to postcopulatory sexual selection (8-11), occurring whenever females mate with multiple males within a breeding cycle (12). Experimental and comparative evidence indicates that female reproductive tract architecture can influence competitive male fertilization success and generate selection on sperm form (2, 13-16), thus representing the proximate basis of female sperm choice (17). Reproductive tract dimensions are easily quantifiable and, becau...

An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

“…Female reproductive tract innervation and secretory biology are also known to interact with the ejaculate in ways critical for sperm storage and fertilization (e.g., Adams and Wolfner 2007;Avila and Wolfner 2009;Schnakenberg et al 2011) and hence may also play a role in postcopulatory sexual selection. Our limited knowledge suggests that female reproductive tracts undergo rapid evolutionary diversification, with important implications for the intensity of sexual selection generated on males in general and on the form and function of numerous ejaculate traits in particular (Swanson et al 2001;Miller and Pitnick 2002;Higginson et al 2012aHigginson et al , 2012b. Important advances in postcopulatory sexual selection theory are likely to come from research into the selective causes of female reproductive tract divergence and addressing whether the same models for the evolution of premating female preferences (Andersson 1994) are sufficient to explain divergence in female tract traits functioning as the proximate basis of sperm choice (e.g., Curtsinger 1991; Keller and Reeve 1995;Simmons and Kotiaho 2007).…”

“…Female sperm-storage organs enhance sperm survival and temporally separate insemination from fertilization, expanding the temporal, morphological, and biochemical arenas of postcopulatory sexual selection in general, and are predicted to extend the opportunity for female sperm choice in particular (Birkhead et al 1993;Eberhard 1996;Pitnick et al 2009). Sperm-storage organ morphology can be highly diverse (e.g., birds: Birkhead and Møller 1992; pulmonate snails : Baur 1998;spiders: Uhl 2002;insects: Theodor 1976;Puniamoorthy et al 2010;Higginson et al 2012b), rapidly divergent (e.g., Pitnick et al 1999Pitnick et al , 2003 and have been found to exhibit correlated evolution with sperm morphology in diverse taxa (reviewed by Pitnick et al 2009;Higginson et al 2012b), which in turn may promote reproductive isolation between species (Howard et al 2009;Manier et al 2013a). Relatively little is known, however, about female sperm-storage organ function (Schnakenberg et al 2012), particularly with regard to sperm choice.…”

Evolution of sperm structure and energetics in passerine birds

“…However, species included in this study represent a broad range of sperm competition levels as inferred from both extra-pair (EP) paternity levels (EP young, 9-37%; EP broods, 23-72%; electronic supplementary material, table S3) and relative testis size ( percentage body mass: range 0.7-4.7%; electronic supplementary material, table S3). Alternatively, sperm traits may evolve as an adaptation to the female reproductive tract environment [66,67], especially in species with sperm storage. In pheasants, Immler et al [68] showed that sperm velocity was negatively related to the duration of sperm storage (see also [4]), but independent of the risk of sperm competition.…”

Complex sperm evolution

“…Using phylogenetically controlled comparative analyses, Higginson et al show that this sperm structural evolution is significantly associated with the morphological complexity of the female reproductive tract (6). Although primarily functioning as a site for sperm storage and fertilization, the tract has undergone extensive diversification across closely related species (Fig.…”

“…1), making the conjugate much longer than an individual sperm. In addition, some species produce two sperm types, which then link up in the female tract to swim as celldimorphic tandems (6).…”