Ecological Divergence, Host Race Formation, and Speciation: Host Plant Adaptation as a Driver of Insect Diversification

The role of ecology in speciation is a central issue in evolutionary biology. Here, five fundamental questions concerning ecological speciation-with-gene-flow are investigated in the Rhagoletis pomonella species complex, a model for sympatric ecological speciation: (1) What constitutes a sympatrically-formed species? (2) Is the initiation of ecological speciation in sympatry a common or exceptional phenomenon? (3) What traits are important to host shifts and reproductive isolation for phytophagous insects? (4) What is the source of genetic variation fueling adaptive divergence? (5) What role does genome structure play in speciation-with-gene-flow and how is this reflected in patterns of genomic differentiation as speciation proceeds?

I addressed these questions by investigating two components of the R. pomonella species complex: 1) populations of R. pomonella infesting an array of hawthorn species in the southeastern U.S. and (2) the flowering dogwood fly, the sister species to R. pomonella. I found that southern populations of R. pomonella are differentiated both phenotypically and genetically and represent partially-isolated host races. Furthermore, these populations may have acted as a reservoir for standing genetic variation, enabling the rapid evolution of the apple race of R. pomonella. Comparisons of the flowering dogwood fly to the hawthorn and apple races of R. pomonella revealed that species-level differentiation was accompanied by the formation of range-wide genetic clustering based on allele frequency differences. I observed a striking correlation in the topology of differentiation between the host race and species, consistent with a genome-wide reduction in effective migration.

These findings support the following conclusions regarding the five questions: (1) Sympatrically-formed species can represent host races writ-large; (2) The initiation of ecological speciation may proceed readily in Rhagoletis; (3) Both olfactory and diapause traits are important to ecological adaptation and reproductive isolation in Rhagoletis, but there are limits to their role in diversification; (4) Standing genetic variation, in the form of heterogeneous resource use in allopatric populations and latitudinal clines, has been a major factor in the radiation of the R. pomonella species complex; and (5) The transition from host race to species appears to involve the uplift of genomic 'continents of speciation' driven global reductions in effective migration.