Divergent selection on oviposition traits generates reproductive isolation between Neodiprion lecontei and Neodiprion pinetum

Ecological speciation, the evolution of reproductive isolation via divergent natural selection, is thought to be prevalent in plant-feeding insects. However the nature of divergent selection and the mechanisms linking adaptive divergence to reproductive isolation is unknown in most cases. To address these questions, we focus on a well-studied and experimentally tractable group of pine-feeding specialists with an established association between host shifts and speciation. We hypothesize that variation in needle width and resin content among pine species generates divergent selection on oviposition traits in Neodiprion and that this ecologically based selection reduces hybrid fitness. To test this hypothesis, we examined a pair of sister species differing in host use. N. pinetum feeds exclusively on a thin-needled host, while N. lecontei feeds on thicker, more resinous hosts. Using morphometric analyses and oviposition assays, we first demonstrate that these species differ in several oviposition traits, including ovipositor shape and size, egg pattern, and host preference. To determine whether these differences generate host related postzygotic isolation, we generated hybrids and backcrosses and measured host preference, oviposition traits, and hatching success. We found that backcrosses and hybrids had reduced fitness, the rank order of fitness was as predicted under extrinsic postzygotic isolation, and that the reduction of fitness in hybrids seems to be directly attributable to oviposition behavior. Together, these data are consistent with the hypothesis that N. lecontei and N. pinetum have undergone ecological speciation, and suggest that divergent selection on oviposition traits may be a major driver of divergence in this genus.