Widespread Lateral Transmission in Fergusonina Galling Flies (Diptera: Fergusoninidae) and Their Obligate Nematode...

Cospeciation between symbionts or other tightly associated organisms is believed to occur primarily in the case of strict vertical transmission of the interaction from parents to offspring. In a unique and obligate mutualism, Fergusonina flies and Fergusobia nematodes together form galls on plants in the Myrtaceae, primarily in Australia. The intimate biology of this interaction strongly suggests the presence of strict vertical transmission of nematodes from female flies to daughters. We obtained both fly and nematode mitochondrial sequences from extractions from 136 female flies from 118 galls of Fergusonina daviesae, Fergusonina omlandi, and Fergusonina taylori, all of which feed on overlapping hosts and are broadly sympatric to syntopic. In each of these three focal species, there were many cases of multiple fly haplotypes associated with a single nematode haplotype and vice versa. In the haplotype networks and phylogenies within each species pair, the only case of related fly haplotypes being exclusively associated with related nematode haplotypes was for F. taylori where there was a largely concordant split between fly and nematode haplotypes from Tasmania and mainland Australia. Despite strong evidence of widespread lateral transfer of nematodes within fly species, there was no direct evidence of heterospecific transfer of nematodes. Consistent with this, phylogenetic analyses of 29 Fergusonina and Fergusobia pairs found highly concordant fly and nematode phylogenies indicative of an evolutionary history dominated by cospeciation. In Fergusonina and Fergusobia, what appears to be widespread breakdown of strict vertical transmission within several species does not preclude substantial cospeciation in these groups.