The Geographic Mosaic of Wolbachia Infection in Melanitis leda Butterfly Populations

Insects are the most species-rich multicellular taxon on the planet, and it is estimated that more than half of all insect species are infected with the endosymbiont Wolbachia. This bacterium can manipulate the reproduction of its host and potentially affect host evolution. Most surveys investigating patterns of Wolbachia infection in nature sample limited numbers of individuals; population-level investigations into geographic differences in infection status that might affect host evolution are few. To investigate geographic variability among populations of a single species, we assayed 133 Melanitis leda butterflies (Lepidoptera: Nymphalidae: Satyrinae) for Wolbachia infection collected throughout its range in the Old World tropics and subtropics from Ghana to Fiji. Potential effects of the parasite on the evolution of its host were assessed by inferring phylogenies of the host with nuclear and mitochondrial markers, and by inferring relationships among the Wolbachia strain (sequence type, ST) that we detected in different populations. Geographic variability was apparent on two levels: prevalence of infection and ST of infection. Every M. leda individual on Java and all landmasses south and east of Wallace’s Line were all infected with at least one of three different sequence types; individuals in Australia and Fiji hosted at least two different STs. Butterflies collected elsewhere were often not infected, but most that were had a fourth ST, except for a single individual in Uganda with a fifth ST. Infection status coincided with patterns of nuclear and mitochondrial variability. With the exception of the Ugandan individual, there was no genetic structure in populations collected throughout Africa, Madagascar, South Asia, mainland Asia, the Philippines, Borneo, and Sumatra; this homogeneity implies frequent gene flow between these areas or may be the result of recent M. leda colonization events. Specimens from Australia, New Guinea, and the archipelagos of Southeast Asia and Oceania had nuclear and mitochondrial structure. The topology of nuclear and mitochondrial trees conflicted with regard to the placement of the clades containing specimens from the South Pacific and Ghana. Although this result is consistent with Wolbachia- imposed selection through linkage disequilibria, other factors may play a role in this discord, including the lower effective population size & higher mutation rate of mitochondrial DNA, as well as genetic differences expected between different geographical regions. These results are consistent with the notion that marine barriers limit the dispersal of the host, which seems to permit different strains of Wolbachia to enter insular populations through horizontal transmission at different times and places before subsequent vertical transmission. Some of these STs seem to exert selection on the host, but many do not