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.

Disentangling the determinants of reproductive success in a temperate reef fish, Forsterygion lapillum

<p>Identifying sources of individual variation in reproductive success has been a longstanding challenge for evolutionary ecologists. Reproductive success among individuals can be due to several factors such as competition between conspecifics for nest sites and mating partners, mate choice, or by the physical environment. Reproductive success, particularly among males, can be extremely diverse both within and between species and determining which components contribute to success can be particularly challenging. In this thesis, I investigated patterns and drivers of reproductive success in a temperate marine reef fish, Forsterygion lapillum (the common triplefin). Specifically, I examined how male quality, nest quality, and female choice influence male reproductive success. Additionally, I quantified male reproductive success during the winter and summer of the breeding season to examine the temporal dynamics of breeding success in F. lapillum. Selection of mates by females can be driven by the quality and behavioural attributes of the male or by the quality of resources offered. In Chapter 2, using field-based observations, combined with a lab-based study, I evaluated the effects of different male traits and nest characteristics on female choice and male reproductive success. Specifically, I observed egg guarding males in the field during the breeding season and recorded their phenotypic traits, behaviours, and nest characteristics. I then examined their influence on 3 different components of male reproductive success (brood size, individual egg size, and mate attraction). Additionally, I conducted dichotomous choice tests in the laboratory to evaluate female preference for different sized males, holding different sized nests. In the field, I did not detect a significant relationship between male mating success and male total length or nest size. Brood size and individual egg size were highly variable among sampled males, however, further factors such as courtship frequency, and the number of interactions with potential predators did not explain any additional variation. The number of agonistic displays performed by egg guarding males was the only factor to influence egg size, however, it had no direct impact on brood size or mate attraction. On the contrary, results from the laboratory experiment suggested that male total length and nest size were important during female choice. Females were attracted to and spawned more frequently with larger males holding larger nests. Additionally, females showed a particular preference towards males that displayed intense courtship behaviours. These results suggest that variation in reproductive success among individuals is not random in the common triplefin (F. lapillum) and may be due to a range of complex factors. In natural systems, individual variation in mating success is known to be highly dynamic and vary over time. In Chapter 3, I addressed 3 questions related to reproductive success in male common triplefin: 1) Does the operational sex ratio (OSR) and the density of individuals change predictably within the breeding season? 2) Does male reproductive success change within the breeding season? And 3) Does the age and growth rate of successful males change within the breeding season? To address these questions, I sampled a population of F. lapillum during two periods of the breeding season and quantified a set of morphological and physical traits. Furthermore, I reconstructed individual life histories from the otoliths of egg guarding males. My results show that the density of individuals in the population increased during the summer months, but the operational sex ratio (OSR) remained male-biased. Male reproductive success in terms of brood size and average egg size did not fluctuate during the sampling period. However, the size of males and the size of the nest (cobblestone) held by males was significantly larger in summer compared to winter. Interestingly, successful males sampled in the winter had hatched significantly earlier than successful males sampled in the summer, but their average growth rate remained similar. These findings indicate that variation in male traits across the breeding season plays an important role in female mate choice. The mating system and pool of mating individuals in the common triplefin (F. lapillum) is highly dynamic over the year and has the potential to shape the success of individuals. Overall, this study emphasizes the importance of considering multiple cues and temporal dynamics when disentangling the determinants of individual reproductive success. These findings suggest that male-male competition and female mate choice have a significant influence on male reproductive success. The reproductive ecology of F. lapillum is highly complex and my research has provided valuable insight into its dynamic nature. These results may apply to other species with male parental care and provides an important contribution towards understanding sexual selection and the evolution of mating systems with male parental care.</p>

Disentangling the determinants of reproductive success in a temperate reef fish, Forsterygion lapillum

<p>Identifying sources of individual variation in reproductive success has been a longstanding challenge for evolutionary ecologists. Reproductive success among individuals can be due to several factors such as competition between conspecifics for nest sites and mating partners, mate choice, or by the physical environment. Reproductive success, particularly among males, can be extremely diverse both within and between species and determining which components contribute to success can be particularly challenging. In this thesis, I investigated patterns and drivers of reproductive success in a temperate marine reef fish, Forsterygion lapillum (the common triplefin). Specifically, I examined how male quality, nest quality, and female choice influence male reproductive success. Additionally, I quantified male reproductive success during the winter and summer of the breeding season to examine the temporal dynamics of breeding success in F. lapillum. Selection of mates by females can be driven by the quality and behavioural attributes of the male or by the quality of resources offered. In Chapter 2, using field-based observations, combined with a lab-based study, I evaluated the effects of different male traits and nest characteristics on female choice and male reproductive success. Specifically, I observed egg guarding males in the field during the breeding season and recorded their phenotypic traits, behaviours, and nest characteristics. I then examined their influence on 3 different components of male reproductive success (brood size, individual egg size, and mate attraction). Additionally, I conducted dichotomous choice tests in the laboratory to evaluate female preference for different sized males, holding different sized nests. In the field, I did not detect a significant relationship between male mating success and male total length or nest size. Brood size and individual egg size were highly variable among sampled males, however, further factors such as courtship frequency, and the number of interactions with potential predators did not explain any additional variation. The number of agonistic displays performed by egg guarding males was the only factor to influence egg size, however, it had no direct impact on brood size or mate attraction. On the contrary, results from the laboratory experiment suggested that male total length and nest size were important during female choice. Females were attracted to and spawned more frequently with larger males holding larger nests. Additionally, females showed a particular preference towards males that displayed intense courtship behaviours. These results suggest that variation in reproductive success among individuals is not random in the common triplefin (F. lapillum) and may be due to a range of complex factors. In natural systems, individual variation in mating success is known to be highly dynamic and vary over time. In Chapter 3, I addressed 3 questions related to reproductive success in male common triplefin: 1) Does the operational sex ratio (OSR) and the density of individuals change predictably within the breeding season? 2) Does male reproductive success change within the breeding season? And 3) Does the age and growth rate of successful males change within the breeding season? To address these questions, I sampled a population of F. lapillum during two periods of the breeding season and quantified a set of morphological and physical traits. Furthermore, I reconstructed individual life histories from the otoliths of egg guarding males. My results show that the density of individuals in the population increased during the summer months, but the operational sex ratio (OSR) remained male-biased. Male reproductive success in terms of brood size and average egg size did not fluctuate during the sampling period. However, the size of males and the size of the nest (cobblestone) held by males was significantly larger in summer compared to winter. Interestingly, successful males sampled in the winter had hatched significantly earlier than successful males sampled in the summer, but their average growth rate remained similar. These findings indicate that variation in male traits across the breeding season plays an important role in female mate choice. The mating system and pool of mating individuals in the common triplefin (F. lapillum) is highly dynamic over the year and has the potential to shape the success of individuals. Overall, this study emphasizes the importance of considering multiple cues and temporal dynamics when disentangling the determinants of individual reproductive success. These findings suggest that male-male competition and female mate choice have a significant influence on male reproductive success. The reproductive ecology of F. lapillum is highly complex and my research has provided valuable insight into its dynamic nature. These results may apply to other species with male parental care and provides an important contribution towards understanding sexual selection and the evolution of mating systems with male parental care.</p>

Male coloration affects female gestation period and timing of fertilization in the guppy (Poecilia reticulata)

The trade-up hypothesis is a female behavioral strategy related to mating with multiple males. In this hypothesis, females can produce high-quality offspring while avoiding the risk of losing reproductive opportunities by non-selective mating with males at first mating and then re-mating with more attractive males. As an internal mechanism to realize this behavioral strategy, we predicted that females would immediately fertilize their eggs when they mated with attractive males, whereas females would delay fertilization when they mated with unattractive males to trade-up sires of offspring. The guppy (Poecilia reticulata) is an ovoviviparous fish with internal fertilization, and females show a clear mate preference based on the area of orange coloration on the bodies of males. In addition, it is known that females show a re-mating strategy consistent with the trade-up hypothesis. We tested whether the attractiveness of mated males affected the gestation period and the timing of fertilization. Females were paired with either colorful males or drab males, and the gestation periods (the number of days from mating to parturition) were compared. In addition, we dissected the abdomens of the females at intervals of several days after mating and observed whether the eggs were fertilized. The gestation period in females that were paired with attractive colorful males was significantly shorter than that in females that were paired with drab males. We found that females that mated with colorful males also had their eggs fertilized earlier than those that mated with drab males. Our findings show that differences in the timing of fertilization according to attractiveness of the mate increase the opportunity for cryptic female choice and trading up.

Female choice can explain the fertilization pattern in oaks

We extend a two-step lottery model of Craft et al. to test the hypothesis that oak trees pursue a form of within-flower female choice to increase the diversity of fathers. Oak trees produce six ovules per flower while maturing just one acorn. When assuming a random ovule selection - which is a natural assumption in the absence of other hypotheses - observed fertilization patterns in oaks cannot be explained: long-distance fertilization is unusually common, even as nearby oak trees may be absent as pollen donors. Our model demonstrates how producing multiple ovules per flower permits selection for rare, distant fathers. The number of ovules per flower that maximizes paternal diversity increases with the number of trees. We introduce a cost function for ovule production for which six ovules per flower balance these costs with the benefits of diversifying fathers. Using data from two published field studies, 7 of 8 investigated maternal oaks had actual paternal diversity indices (average diversity index of 15.42) that fit the female choice hypothesis (estimated diversity of 14.66) significantly better than assuming a random selection from the six available ovules (estimated diversity of 7.649). A third field study permitted us to compare paternity by distance classes for two maternal trees. Both fit the female choice model better than random ovule selection.

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.

Domains of Female Choice in Human Evolution

The present article advances the view that women’s mate preferences can be grouped into at least two overarching domains: competitiveness and fatherhood. Theoretical and empirical considerations suggest that female mate preferences evolve in contexts of male competitiveness and often amplify the effects of male-male competition. Evidence for the importance of male-male competition and female choice for competitiveness in humans is reviewed. Evidence is likewise offered for the importance of human fatherhood as an additional domain of female choice outside of male competitiveness. Implications of more inclusive mate preferences for the evolution of cognitive architecture are discussed.