Most species of insects are infected by symbiotic microorganisms, which spread either by directly benefiting their hosts or by manipulating host reproduction in ways that benefit the symbiont, but not the host. Bacterial Spiroplasma are among the more widespread of these symbionts. All Spiroplasma discovered to date either manipulate host reproduction or are pathogenic to their insect hosts. In populations of the fruit fly, Drosophila neotestacea, Spiroplasma have been found to confer resistance to nematode parasitism. Parasitized flies in the wild are essentially sterilized by the nematode if they do not carry Spiroplasma, but have nearly normal fertility if they are infected with these symbionts. This is the first finding of a beneficial effect of Spiroplasma on any insect species, and the first demonstration of an adverse effect of Spiroplasma on nematodes. Spiroplasma infection in D. neotestacea appears to have increased rapidly in the last 20 years in the eastern US and may be spreading westward. This project will conduct experiments to test for the effect of nematode parasitism on Spiroplasma infection dynamics within populations of D. neotestacea. Reciprocally, the effect of Spiroplasma on nematode parasitism in these flies will also be tested. Although most individuals of D. neotestacea in eastern North America are infected with Spiroplasma, none of the flies west of the Rockies are infected. This project will sample populations in British Columbia and Canadian Prairie Provinces, that were last sampled in 2002, to assess whether Spiroplasma is spreading westward across North America.
The fertility-restoring effect of Spiroplasma will also be tested on other combinations of Drosophila and nematode species. If general, such effects could be of great applied significance. River Blindness and Elephantiasis are caused by filarial nematodes that are transmitted by blackflies and mosquitoes. If Spiroplasma confers resistance to filarial nematodes, then Spiroplasma could spread within populations of the insect vectors, which might reduce nematode reproduction and thus incidence and severity of filarial diseases. In principle, a relatively simple manipulation of the insect vectors could yield great public health benefits. This project will provide research training for undergraduate and graduate students.
Drosophila neotestacea is a small fly that feeds on mushrooms in nature. These flies are often sterilized by Howardula aoronymphium, which are parasitic nematodes (= roundworms). We discovered that some individuals carry a type of bacteria (Spiroplasma) that is transmitted from infected females through their eggs to essentially all of their offspring. One aim of our research has been to follow determine whether and how rapidly Spiroplasma is spreading across North America in natural populations of D. neotestacea. By comparing collections made across the continent in 2002 and 2011, we find that is spreading very rapidly. For instance, the frequency of flies carrying Spiroplasma increased from about 12% in 2002 to about 35% in 2011. We estimate that the Spiroplasma infection is moving west at about 130 km per year. In experimental laboratory populations of D. neotestacea experiencing nematode parasitism, the frequency of Spiroplasma-infected flies increases rapidly, but it neither increases nor decreases in populations not exposed to these parasites. More interestingly, we have found that in these experimental populations of D. neotestacea, Spiroplasma drove the roundworms extinct, whereas in populations lacking Spiroplasma, the frequency of nematode parasitism increased dramatically. Our data reveal that something very similar is happening in the wild. Specifically, the recent spread of Spiroplasma in natural populations of D. neotestacea has coincided with at least a 50% drop in the frequency of roundworm parasitism. Our field and laboratory studies have shown that maternally transmitted bacteria can be a source of adaptive change within an insect species. The selection advantage associated with Spiroplasma infection are large, in the range of 10% to 15%, and thus capable of bringing about rapid evolutionary change within an insect host species. Furthermore, the Spiroplasma symbionts have a major effect on the dynamics of parasite populations, being potentially capable of driving them extinct. This project supported two graduate students, two post-doctoral associates, and six undergraduates. In addition, the research supported by this grant led to a successful application for funding from the Gates Foundation through their Grand Challenges Explorations program. The aim of the Grand Challenges grant is to explore the possibility of using Spiroplasma or genes from them to render crop plants resistant to plant-parasitic nematodes, which annually cause over $120 billion in damage to agricultural crops around the world.