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. Impact Summary Female mediated post-ejaculatory sexual selection, known as cryptic female choice, has only recently been researched in earnest, but has been documented across many taxa. This process allows females to bias paternity to favor a given male and can act as a filter to prevent fertilizations from unwanted males under sperm competition, including those of different species. In internal fertilizers like mammals, birds and insects, mechanisms of cryptic female choice can be very robust as the female can greatly modify the environment that sperm experience. In external fertilizers, females cannot control which males release sperm in close proximity to her eggs as she spawns with a chosen mate, but she can release reproductive fluids that act as a mechanism of cryptic female choice. In fishes, cryptic female choice is often mediated by ovarian fluid that is released with the eggs. This ovarian fluid alters sperm behavior, favoring certain males in situations of sperm competition. The mechanism is reportedly strong in native populations of European Atlantic salmon and brown trout, biasing paternity towards the female’s own species when eggs are under threat of hybridization under sperm competition. We examined cryptic female choice in three species of hybridizing salmonids on the North American island of Newfoundland, native Atlantic salmon and brook char, and invasive brown trout from Europe. Although the same species, salmon populations from both continents are quite distinct and our results suggest cryptic female choice is too weak in North American Atlantic salmon and brook char to prevent hybridization by invasive brown trout. We hope that this research inspires more work on cryptic female choice to better understand patterns across different species and locally adapted populations within species.