Comparative analysis of host-shift speciation in the redheaded pine sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)

A fundamental challenge in evolutionary biology is to understand how and why new species arise. While decades of empirical and theoretical work show that a myriad of mechanisms can lead to the evolution of reproductive isolation, it remains to be seen which, if any, of these mechanisms has contributed most to the generation of biodiversity. Comprising over 25% of all species, plant-feeding insects are among the most diverse organisms on the planet, and shifts to herbivory are consistently associated with increased diversification rates. One explanation for this association is that adaptation to divergent host plants plays a central role in the generation of new insect species. This hypothesis is supported by a growing list of examples of host-shift speciation in insects; however, whether this speciation mode predominates in insects remains to be seen because few taxa have been examined within the appropriate comparative framework. The primary objective of the proposed research is therefore to assess the prevalence of host-shift speciation in herbivorous insects. To this end, Neodiprion, a well studied genus of host-specialized insects that is both ecologically variable and experimentally tractable, will be employed as a model for herbivore speciation. Consistent with the host-shift speciation hypothesis, previous work has shown that changes in host use coincide with speciation events in Neodiprion; however, an alternative explanation for these findings is that host shifts tend to occur only after speciation (via some other mechanism) is complete. Distinguishing between these alternatives will require examining populations at the earliest stages of divergence, before post-speciation changes can accrue. Therefore, the proposed research will focus on Neodiprion lecontei, a widespread pest species that occurs on multiple pine species throughout its range in eastern North America. If host-shifts frequently drive herbivore speciation, incipient speciation is expected between N. lecontei populations on different hosts. To test this prediction, genomic data from natural populations of this species will be combined with experimental studies of host use and reproductive isolation. When placed within an explicit comparative framework that investigates the relationship between ecological divergence, reproductive isolation, and time, these data will make it possible to (1) assess the importance of host shifts to Neodiprion speciation and (2) identify general patterns in the evolution of ecological divergence and reproductive isolation. The principal intellectual merit of the proposed research is that it directly tests the longstanding hypothesis that host-shifts are a central driver of herbivorous insect speciation. In addition, the proposed research will reveal the time course of herbivore speciation; for example, with these data one can identify the host use traits and reproductive barriers that tend to evolve first. Together, these data will provide rare insight into the extent to which speciation is predictable (i.e., there are discernable patterns in the evolution of ecological divergence and reproductive isolation) or idiosyncratic. Results will be disseminated broadly to both the scientific community and the public via publications, seminars, and deposition of data and specimens in appropriate repositories (e.g., Genbank; natural history collections). In addition, the proposed research has three main broader impacts. First, the proposed research has the potential to identify host races and cryptic species within Neodiprion lecontei, a destructive pest of pine plantations throughout the eastern U.S.; any such findings will be shared online and with regional, state, and national forest health specialists. Second, the proposed research will provide training opportunities at the undergraduate, graduate, and postdoctoral levels. In recruiting students/postdocs to work on this project, every effort will be made to ensure the participation of underrepresented groups. Third, because speciation via host shifts is an intuitive process and N. lecontei are a part of the local fauna, this system provides an excellent teaching tool for demonstrating how changes at the population level can lead to the origin of new species. Specifically, a Neodiprion-based teaching module (i.e., lesson plan, presentation materials, hands-on activities, and assignments) will be developed, then assessed in classroom settings in eastern Kentucky (including rural schools). Finding effective ways to teach evolution is especially important in evolution/creationism “battleground” states like Kentucky, which is home to the Creation Museum and future home of the Noah’s Ark theme park.