Genomic Contingence Beneath Ecological Convergence: The Tempo and Mode of Gene Loss in Parasitic Bilaterians

Abstract Parasitism has independently evolved hundreds of times among metazoans. Nonetheless, parasites have explored only a limited range of ecologies, and they display frequent convergence in morphological, behavioral, and life-history traits. Although gene loss in particular parasitic species has been documented, it is not known if gene loss converges along the same lines as these other traits. To test for convergent gene loss, we characterized the housekeeping, regulatory, and DNA-repair complements of 48 bilaterian species, including 20 parasites belonging to six different bilaterian phyla. We found that different parasitic strategies do not display characteristic tempos or modes of gene loss. Further, the accelerated rates of gene loss seen in some parasites were almost always shared with their free-living relatives, indicating that the increased rate of loss preceded the rise of parasitism. Therefore, the convergent ecological strategies and adaptations that have arisen in distantly related parasitic lineages overlay contingent gene losses which largely reflect their phylogenetic history. These results have important implications for how ecologists and evolutionary biologists should model the acquisition of parasitism, especially regarding the long-held assumption that reversion from a parasitic to a free-living state is impossible.