Parasitic fish embryos do a “front-flip” on the yolk to resist expulsion from the host

Abstract

Embryonic development is often considered shielded from the effects of natural selection, being selected primarily for reliable development. However, embryos sometimes represent virulent parasites, triggering a coevolutionary “arms race” with their host. We have examined embryonic adaptations to a parasitic lifestyle in the bitterling fish. Bitterlings are brood parasites that lay their eggs in the gill chamber of host mussels. Bitterling eggs and embryos have adaptations to resist being flushed out by the mussel. These include a pair of projections from the yolk sac that act as an anchor. Furthermore, bitterling eggs all adopt a head-down position in the mussel gills which further increases their chances of survival. To examine these adaptations in detail, we have studied development in the rosy bitterling ( Rhodeus ocellatus ) using molecular markers, X-ray tomography, and time-lapse imaging. We describe a suite of developmental adaptations to brood parasitism in this species. We show that the mechanism underlying these adaptions is a modified pattern of blastokinesis—a process unique, among fish, to bitterlings. Tissue movements during blastokinesis cause the embryo to do an extraordinary “front-flip” on the yolk. We suggest that this movement determines the spatial orientation of the other developmental adaptations to parasitism, ensuring that they are optimally positioned to help resist the ejection of the embryo from the mussel. Our study supports the notion that natural selection can drive the evolution of a suite of adaptations, both embryonic and extra-embryonic, via modifications in early development.