Mating behavior and the evolution of sperm design

Abstract

Sperm are the most diverse of all animal cell types, and much of the diversity in sperm design is thought to reflect adaptations to the highly variable conditions under which sperm function and compete to achieve fertilization. Recent work has shown that these conditions often evolve rapidly as a consequence of multiple mating, suggesting a role for sexual selection and sexual conflict in the evolution of sperm design. However, very little of the striking diversity in sperm design is understood functionally, particularly in internally fertilizing organisms. We use phylogenetic comparative analyses covering 16 species of the hermaphroditic flatworm genus Macrostomum to show that a complex sperm design is associated with reciprocal mating and that this complexity is lost secondarily when hypodermic insemination-sperm injection through the epidermis-evolves. Specifically, the complex sperm design, which includes stiff lateral bristles, is likely a male persistence trait associated with sexual conflicts over the fate of received ejaculates and linked to female resistance traits, namely an intriguing postcopulatory sucking behavior and a thickened epithelium of the sperm-receiving organ. Our results suggest that the interactions between sperm donor, sperm, and sperm recipient can change drastically when hypodermic insemination evolves, involving convergent evolution of a needle-like copulatory organ, a simpler sperm design, and a simpler female genital morphology. Our study documents that a shift in the mating behavior may alter fundamentally the conditions under which sperm compete and thereby lead to a drastic change in sperm design.Platyhelminthes | sexually antagonistic coevolution | simultaneous hermaphrodite | sperm morphology | traumatic insemination P arker's (1-3) far-reaching extension of Darwin's (4) narrow focus on precopulatory mating interactions highlighted that sexual selection continues to operate after mating partners have agreed to mate and that considering postcopulatory sexual selection therefore is crucial to understand the evolution of many reproductive traits (5, 6). This insight has led to extensive research in evolutionary biology that focused on understanding the biology of sperm (7), the most diverse of all animal cell types (8,9). From this research emerged an apparent consensus that the diversity in sperm design-the strikingly variable ways of constructing a sperm-reflects the highly variable physiological and morphological environments in which sperm have to survive, function, and compete for fertilization (5,(10)(11)(12)(13)(14). Moreover, recent studies have documented clearly that these environments can evolve rapidly, probably because of coevolutionary interactions linked to multiple mating and the resulting sexual selection and sexual conflicts (15-21). However, the bewildering diversity in sperm design is poorly understood at the functional level, particularly in internally fertilizing organisms (9,12,22). A recent review on the evolution of sperm morphological diversity concluded...

Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition

“…Moreover, reciprocal mating may lead to receipt of too much sperm or sperm from unattractive sires, favouring post-copulatory mechanisms to remove or choose among sperm of different sperm donors, promoting sperm digestion and cryptic female choice, and probably leading to antagonistic coevolution [18,49] (see also §5). But whether Bateman's principle usually operates in hermaphrodites is of course an empirical question, not a theoretical one [11,53,58]. There is a long-standing debate about this question [49,57,[59][60][61][62], but the relevant data needed to inform this debate are largely lacking at the moment.…”

“…Indeed, much of what we currently know about sexual selection in hermaphrodites appears to occur at the post-copulatory level [36,[49][50][51][52][53], including the highly variable allocation to sperm production under different competition scenarios that we mentioned in §2 when discussing LSC. In §5, we discuss a range of additional mechanisms of post-copulatory sexual selection, how they may affect LSC and thus the evolution of sex allocation and how their interaction could potentially lead to sexual conflicts (see also [11]).…”

Female reproductive tract form drives the evolution of complex sperm morphology

“…This variation has been widely attributed to postcopulatory sexual selection (8)(9)(10)(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)(14)(15)(16), thus representing the proximate basis of female sperm choice (17). Reproductive tract dimensions are easily quantifiable and, because they are relatively invariant over the reproductive lifespan of a female, represent a consistent female preference unaffected by external environmental conditions.…”

Sexual selection in hermaphrodites, sperm and broadcast spawners, plants and fungi

“…But sperm may also have to combat 'female' countermeasures (cryptic female choice) aimed at preventing fertilization by particular males, or to prevent polyspermy. Interestingly, with the evolution of traumatic insemination, sperm morphology loses its complexity and becomes adapted to rapidly move through the body towards the 'female' reproductive organs [16]. Traumatic insemination most likely evolved to circumvent cryptic female choice, but also allows an individual to inseminate while lowering the risk of being inseminated.…”

“…At the same time, selection acts to increase the 'female's' control over which sperm fertilizes the eggs. Using comparative analyses of the flatworm genus Macrostomum, Schärer et al [16] mapped sperm morphology to mating biology to determine the extent to which the evolution of sperm morphology is driven by sperm competition and cryptic 'female' choice. The rstb.royalsocietypublishing.org Phil.…”