Anatomy of an adaptive radiation: Blepharoneura fruit flies

Authors: WINKLER, ISSAC - Cornell College - Iowa; Scheffer, Sonja; Lewis, Matthew; OTTENS, KRISTINA - University Of Iowa; RASMUSSEN, ANDREW - Cornell College - Iowa; GOMES-COSTA, GRESSICA - University Of Bahia; HUERTO SANTILLAN, LUZ - National University Of San Marcos; CONDON, MARTY - Cornell College - Iowa; FORBES, ANDREW - University Of Iowa

Submitted to: BMC Evolutionary Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/2/2018
Publication Date: 3/14/2018
Citation: Winkler, I., Scheffer, S.J., Lewis, M.L., Ottens, K.J., Rasmussen, A.P., Gomes-Costa, G.A., Huerto Santillan, L.M., Condon, M.A., Forbes, A.A. 2018. Anatomy of an adaptive radiation: Blepharoneura fruit flies. BMC Evolutionary Biology. 18:30-33.

Interpretive Summary: Insects that feed on plants are one of the most diverse groups on Earth, numbering well over 100,000 species. Many insects are pests of crops, horticulture, and forestry products, resulting in annual economic damage of billions of dollars within the U.S. and globally. The causes of the high levels of diversity of insects that feed on plants are unknown. We used DNA sequence data to explore diversity and ecology in tephritid fruit flies feeding on plants in the melon family. We found that in closely related species, geography was more closely associated with new species formation than was colonization of new host plant species. The rate of new species formation varied, possibly due to extinction caused by parasitic wasps, insects often used to control agricultural pests. This research will be of interest to entomologists, ecologists, and evolutionary biologists, in addition to scientists concerned with management of fruit fly pests.

Technical Abstract: Insect herbivores have often been linked to the ecological theory of adaptive radiation, which postulates that divergent selection on phenotypes in different habitats or environments results in the evolution of reproductive barriers between populations and subsequent speciation. An expected result of ecological speciation (and adaptive radiation) is reduced niche overlap within communities. Here, we focus on a hyperdiverse genus of Neotropical fruit flies (Blepharoneura) with patterns of diversity not predicted by models of ecological speciation. We constructed a time-calibrated phylogeny of Blepharoneura flies with ancestral character states reconstructed for host species, host tissue and geographic region. Divergence was consistently associated with allopatry, but not with shifts in host use. Shifts in host use were associated with ~20% of recent splits (<3 Ma), but >60% of older splits (>3 Ma). We used the gamma statistic and maximum likelihood model fitting to evaluate change in diversification rate and found no evidence of diversification rate changes in the overall tree; however, diversification rate in one of component lineages slowed significantly. Decreases in diversification rate are generally interpreted as evidence of adaptive radiation; yet, patterns of Blepharoneura diversity are inconsistent with traditional explanations involving decrease in speciation rates associated with competition. Instead, we suggest that the apparent decrease in diversification rate may be due to higher rates of local extinction (perhaps caused by parasitoids) of lineages that come into secondary contact. While ecology may not drive speciation, ecological differences – either in host use or defenses against parasites or both – may protect lineages against extinction and promote the extraordinary levels of diversity in this system.