Evolution and ecology of associations between Drosophila and their parasitic nematodes

Abstract

In this dissertation, the evolutionary and ecological determinants of host range of nematode parasites (Tylenchida: Allantonematidae: Howardula, Parasitylenchus) of mushroom-breeding Drosophila (Diptera: Drosophilidae) are examined. These nematodes are horizontally transmitted, obligate parasites, often with severe effects on host fitness. Phylogenetic analysis of Drosophila and Howardula DNA sequences shows little congruence between host and parasite phylogenies, with frequent host colonizations and losses. Drosophila -parasitic Howardula are not monophyletic, with host switches occurring between Drosophila and distantly related mycophagous sphaerocerid flies. Molecular analysis reveals eight new Howardula species. The ability of five nematode species to infect and develop in 24 taxonomically diverse Drosophila species is assessed. All nematode potential host ranges but one are large, even for host specialists. Novel hosts that are distantly related from the native host are less likely to be infected, but among closely related hosts there is variation in susceptibility. Potential host ranges differ greatly between related parasite species. Most novel infections do not cause reductions in host fecundity, with the exception of P. nearcticus. Thus, Drosophila-nematode associations are dynamic, and appear to be driven by a combination of repeated opportunities for host colonization due to shared mushroom breeding sites, and large nematode potential host ranges. Recent colonization of novel host species may explain the striking differences in virulence observed in natural Drosophila-nematode associations. For example, Nearctic species of the Drosophila testacea group are more severely affected by infection than Palearctic species, including complete female sterility. Cross-infection experiments reveal that virulence is evolutionarily labile in testacea-Howardula associations, and that high levels of virulence manifested in some host-parasite combinations are due to a lack of host resistance. Finally, ecological determinants of host range are considered. First, competition between a generalist and a specialist parasite of D. recens is assessed by comparing nematode infection success and reproduction in single and double infections. Second, differences between the actual and potential host ranges of Howardula neocosmis are documented. This parasite appears restricted to D. acutilabella in nature, yet successfully parasitizes the closely related, microsympatric D. cardini. Neither differential virulence nor competitive interactions between hosts explain the host range differences.