Sperm Attraction by Female Reproductive Fluid in a Fish With an Unconventional Fertilisation Strategy

ABSTRACT

Active sperm guidance towards the eggs is necessary for gametes to meet within the fertilisation window and is usually achieved through the action of female reproductive fluids (FRF hereafter) on sperm flagellar movement. However, it remains unknown whether FRF retains this function in species with unusual fertilisation strategies, that is, that deviate from gametes being released in the open water or sperm being transferred directly into the female reproductive tract. Here we tested the sperm attractant role of FRF in the bitterling, a small cyprinid fish that parasitises freshwater mussels. Bitterling deposit sperm and eggs inside the mussel gills and gamete interactions are facilitated by the water current generated by mussel respiration. Because flow‐driven physical processes could facilitate sperm‐egg encounters, we argue that selection on active sperm guidance by FRF may be relaxed. Alternatively, sperm attraction could be maintained by pleiotropic effects of genes involved in other reproductive functions of FRF. Using a recently developed sperm selection chamber and the European bitterling Rhodeus amarus , we find that more sperm accumulate in the FRF channel compared to the water control. Moreover, European bitterling sperm showed no preference for conspecific FRF over that of a distantly related Asian bitterling FRF. Our results suggest that bitterling FRF resembles that of species with conventional fertilisation modes, implying that it could mediate sperm selection and cryptic female choice. We discuss alternative evolutionary scenarios underlying the persistence of sperm attractant properties of bitterling FRF despite the shift to a physically mediated fertilisation environment.