Rapid and repeatable host plant shifts drive reproductive isolation following a human-mediated introduction

Authors: HOOD, GLENN - Wayne State University; POWELL, THOMAS - Binghamton University; DOELLMAM, MEREDITH - University Of Notre Dame; Sim, Sheina; GLOVER, MARY - University Of Notre Dame; Yee, Wee; GOUGHNOUR, ROBERT - Washington State University Extension Service; MATTSSON, MONTY - Oregon State University; SCHWARZ, DIETMAR - Western Washington University; FEDER, JEFFREY - University Of Notre Dame

Submitted to: Journal of Molecular Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/27/2019
Publication Date: 1/1/2020
Citation: Hood, G.R., Powell, T.H., Doellmam, M.M., Sim, S.B., Glover, M., Yee, W.L., Goughnour, R.B., Mattsson, M., Schwarz, D., Feder, J.L. 2020. Rapid and repeatable host plant shifts drive reproductive isolation following a human-mediated introduction. Journal of Molecular Evolution. 74(1):156-168. https://doi.org/10.1111/evo.13882.
DOI: https://doi.org/10.1111/evo.13882

Interpretive Summary: A recent introduction of the apple maggot, Rhagoletis pomonella, outside its native range in the eastern United States to the western United States created a unique opportunity to potentially witness the beginning of a new ecological speciation event. To test for evidence of the emergence of population structure in this newly invaded geographic area, R. pomonella flies were collected from apples, black hawthorns, and ornamental hawthorns growing in sympatry from three different sympatric localities. A genetic analysis of these flies using microsatellite loci from across the 5 autosomes revealed evidence for hyper-local genetic differentiation and potentially local adaptation. This suggests that rapid evolution to new hosts may be a common source of differentiation which leads to the creation of new species.

Technical Abstract: Ecological speciation via host-shifting is often invoked as a mechanism for insect diversification, but the relative importance of this process is poorly understood. The shift of Rhagoletis pomonella in the 1850s from the native downy hawthorn, Crataegus mollis, to introduced apple, Malus pumila, is a classic example of sympatric host race formation, a hypothesized early stage of ecological speciation. The accidental human-mediated introduction of R. pomonella into the Pacific Northwest (PNW) in the late-1970’s allows us to investigate how novel ecological opportunities may trigger divergent adaptation and host race formation on a rapid timescale. Since the introduction, the fly has spread in the PNW, where in addition to apple, it now infests native black hawthorn, C. douglasii, and introduced ornamental hawthorn, C. monogyna. We use this “natural experiment” to test for genetic differentiation among apple, black and ornamental hawthorn flies co-occurring at three sympatric sites. We report evidence that populations of all three host-associations are genetically differentiated at the local level, indicating that partial reproductive isolation has evolved in this novel habitat. Our results suggest that conditions suitable for initiating host-associated divergence may be common in nature, allowing for the rapid evolution of new host races when ecological opportunity arises.