Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella

Abstract

In On the Origin of Species, Darwin proposed that natural selection had a fundamental role in speciation¹. But this view receded during the Modern Synthesis when allopatric (geographic) models of speciation were integrated with genetic studies of hybrid sterility and inviability^2,3. The sympatric hypothesis posits that ecological specialization after a host shift can result in speciation in the absence of complete geographic isolation^4,5. The apple maggot, Rhagoletis pomonella, is a model for sympatric speciation in progress^4,5. Hawthorn (Crataegus spp.) is the native host for R. pomonella in N. America⁵. But in the mid-1800s, a new population formed on introduced, domesticated apple (Malus pumila)^4,5. Recent studies^6,7,8,9,10 have conferred ‘host race’ status on apple flies as a potentially incipient species, partially isolated from haw flies owing to host-related adaptation. However, the source of selection that differentiates apple and haw flies is unresolved. Here we document a gene–environment interaction (fitness trade-off) that is related to host phenology and that genetically differentiates the races.