Can cryptic female choice prevent invasive hybridization in external fertilizing fish?

Polyandrous mating systems result in females mating with multiple males. This includes the potential for unintended matings and subsequent sperm competition with hybridizing species, especially in the presence of alternative reproductive tactics (sneaker males). Cryptic female choice allows females to bias paternity towards preferred males under sperm competition and may include conspecific sperm preference when under hybridization threat. The potential becomes particularly important in context of invasive species that can novelly hybridize with natives. We provide the first examination of conspecific sperm preference in a system of three species with potential to hybridize: North American native Atlantic salmon (Salmo salar) and brook char (Salvelinus fontinalis), and invasive brown trout (Salmo trutta) from Europe. Using naturalized populations on the island of Newfoundland, we measured changes in sperm swimming performance, a known predictor of paternity, to determine the degree of upregulation to female cues related to conspecific sperm preference. Compared to water alone, female ovarian fluid in general had a pronounced effect and upregulated sperm motility (mean 53%) and swimming velocity (mean 30%). However, patterns in the degree of upregulation suggest there is no conspecific sperm preference in the North American populations. Furthermore, female cues from both native species tended to boost the sperm of invasive males more than their own. We conclude that cryptic female choice is too weak in this system to prevent invasive hybridization and is likely insufficient to promote or maintain reproductive isolation between the native species.

Sperm of more colorful males are better adapted to ovarian fluids in lake char (Salmonidae)

Fish often spawn eggs with ovarian fluids that have been hypothesized to support sperm of some males over others (cryptic female choice). Alternatively, sperm reactions to ovarian fluids could reveal male strategies linked to their likely roles during spawning. Sperm of males who would usually be close to females during spawning are then expected to be better adapted to the presence of ovarian fluids than to water only, while the reverse would be expected for males that typically spawn at larger distance to the females. We tested these predictions with gametes and ovarian fluids from wild-caught lake char (Salvelinus umbla). We found that sperm of more colorful males showed increased sperm velocity in diluted ovarian fluids while sperm of paler males were fastest in water only. We then let equal numbers of sperm compete for fertilizations in the presence or absence of ovarian fluids and used microsatellite markers to assign in total 1,464 embryos (from 70 experimental trials) to their fathers. Overall, sperm of more colorful males reached higher fertilization success than sperm of pale males. This difference was enhanced by the presence of ovarian fluids and best explained by the increased sperm velocity. Sperm competitiveness was not enhanced with decreasing male inbreeding coefficients or decreasing genetic distance to a given female, although parallel stress tests on embryos revealed that females would profit more from mating with least related males rather than most colored ones. We conclude that sperm of more colorful males are best adapted to ovarian fluids, and that the observed reaction norms reveal male strategies rather than cryptic female choice.

Post-Copulatory Sexual Selection

The field of post-copulatory sexual selection investigates how female and male adaptations have evolved to influence the fertilization of eggs while optimizing fitness during and after copulation, when females mate with multiple males. When females are polyandrous (one female mates with multiple males), they may optimize their mating rate and control the outcome of mating interactions to acquire direct and indirect benefits. Polyandry may also favor the evolution of male traits that offer an advantage in post-copulatory male-male sperm competition. Sperm competition occurs when the sperm, seminal fluid, and/or genitalia of one male directly impacts the outcome of fertilization success of a rival male. When a female mates with multiple males, she may use information from a number of traits to choose who will sire her offspring. This cryptic female choice (CFC) to bias paternity can be based on behavioral, physiological, and morphological criteria (e.g., copulatory courtship, volume and/or composition of seminal fluid, shape of grasping appendages). Because male fitness interests are rarely perfectly aligned with female fitness interests, sexual conflict over mating and fertilization commonly occur during copulatory and post-copulatory interactions. Post-copulatory interactions inherently involve close associations between female and male reproductive characteristics, which in many species potentially include sperm storage and sperm movement inside the female reproductive tract, and highlight the intricate coevolution between the sexes. This coevolution is also common in genital morphology. The great diversity of genitalia among species is attributed to sexual selection. The evolution of genital attributes that allow females to maintain reproductive autonomy over paternity via cryptic female choice or that prevent male manipulation and sexual control via sexually antagonistic coevolution have been well documented. Additionally, cases where genitalia evolve through intrasexual competition are well known. Another important area of study in post-copulatory sexual selection is the examination of trade-offs between investments in pre-copulatory and post-copulatory traits, since organisms have limited energetic resources to allocate to reproduction, and securing both mating and fertilization is essential for reproductive success.

Copulatory behaviour increases sperm viability in female spiders

One remarkable reproductive feature in animals with internal fertilization is a reduction in sperm viability over time in females. Whether this reduction is driven by male–male competition and/or cryptic female choice is unclear. From the perspective of cryptic female choice, we postulated that sperm viability is affected by a particular male copulatory behaviour. In this study, we investigated the following aspects: (1) sperm viability in mated females vs. males; (2) whether sperm viability varies temporally after mating; and (3) whether male copulatory behaviour covaries positively with sperm viability within females. We used the spider Holocnemus pluchei, whose males use several copulatory behaviours to court females. We found that females that stored sperm for 4 or 15 days showed no difference in sperm viability but had lower sperm viability compared with males, and males that performed a longer post-insemination behaviour had higher sperm viability inside the female. It is unclear how sperm viability is reduced and how male post-insemination behaviour affects this. It is possible that extending copulation allows males to induce females to keep sperm alive for longer. This result is predicted by theory whereby males induce females to facilitate sperm to reach and fertilize eggs based on male postcopulatory behaviour.

Detecting Cryptic Female Choice in Decapod Crustaceans

Decapod Crustacea (shrimps, lobsters, and crabs) employ a range of different reproductive mechanisms that affect paternity, but does it include cryptic female choice (CFC)? This chapter focuses on events surrounding the fertilization of an egg by a sperm and the opportunities where cryptic fertilization bias might occur. It presents a new model of decapod fertilization, defined in terms of space and time to fertilization. Females have several ways to store sperm and influence fertilization outcomes, which should be affected by (1) their growth pattern (indeterminate or determinate), (2) the link between molting and mating (soft-shell or hard-shell mating), (3) fertilization latency, and (4) how sperm are protected (no protection or storage is separate from the oviduct, or storage in a seminal receptacle is linked to the oviduct). Paternity data available for 26 decapods show that in 85% of species, females carry broods with multiple paternity and 15% have broods with single paternity. Therefore many (if not most) females mate with several males and so they certainly could make a choice. However, whether this pattern is due to CFC or merely reflects mating history is a matter of debate. At present, there are no unequivocal data that demonstrate CFC: outcomes caused by male mate guarding and sperm competition cannot be distinguished from female choice. The challenge is to understand what females might be choosing and how to detect that choice. Detecting CFC in field data is difficult, if not impossible, because both single and multiple paternities could be favored.

Chemical signals from eggs facilitate cryptic female choice in humans

Mate choice can continue after mating via chemical communication between the female reproductive system and sperm. While there is a growing appreciation that females can bias sperm use and paternity by exerting cryptic female choice for preferred males, we know surprisingly little about the mechanisms underlying these post-mating choices. In particular, whether chemical signals released from eggs (chemoattractants) allow females to exert cryptic female choice to favour sperm from specific males remains an open question, particularly in species (including humans) where adults exercise pre-mating mate choice. Here, we adapt a classic dichotomous mate choice assay to the microscopic scale to assess gamete-mediated mate choice in humans. We examined how sperm respond to follicular fluid, a source of human sperm chemoattractants, from either their partner or a non-partner female when experiencing a simultaneous or non-simultaneous choice between follicular fluids. We report robust evidence under these two distinct experimental conditions that follicular fluid from different females consistently and differentially attracts sperm from specific males. This chemoattractant-moderated choice of sperm offers eggs an avenue to exercise independent mate preference. Indeed, gamete-mediated mate choice did not reinforce pre-mating human mate choice decisions. Our results demonstrate that chemoattractants facilitate gamete-mediated mate choice in humans, which offers females the opportunity to exert cryptic female choice for sperm from specific males.