Host plant and Wolbachia shape the population genetics of sympatric herbivore populations

Authors: FU, ZHEN - Washington State University; MEIER, AMANDA - University Of Georgia; EPSTEIN, BRENDEN - University Of Minnesota; BERGLAND, ALAN - University Of Virginia; CASTILLO CARRILLO, CARMEN - Washington State University; Cooper, William - Rodney; CRUZADO, REGINA - University Of Idaho; Horton, David; JENSEN, ANDREW - Washington State Potato Foundation; KELLEY, JOANNA - Washington State University; RASHED, ARASH - University Of Idaho; REITZ, STUART - Oregon State University; RONDON, SILVIA - Oregon State University; THINAKARAN, JENITA - University Of Idaho; WENNINGER, ERIK - University Of Idaho; WOHLEB, CARRIE - Washington State University; CROWDER, DAVID - Washington State University; SNYDER, WILLIAM - Washington State University

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/13/2020
Publication Date: 8/1/2020
Citation: Fu, Z., Meier, A.R., Epstein, B., Bergland, A.O., Castillo Carrillo, C.I., Cooper, W.R., Cruzado, R.K., Horton, D.R., Jensen, A.S., Kelley, J.L., Rashed, A., Reitz, S.R., Rondon, S.I., Thinakaran, J., Wenninger, E.J., Wohleb, C.H., Crowder, D.W., Snyder, W.E. 2020. Host plant and Wolbachia shape the population genetics of sympatric herbivore populations . Evolutionary Applications. 13:2740-2753.
DOI: https://doi.org/10.1111/eva.13079

Interpretive Summary: Potato psyllid, a key pest of potato and vector of the zebra chip pathogen, occurs in the Pacific Northwest as distinct genetic populations that differ in the presence of a bacterial endosymbiont called Wolbachia. Wolbachia causes reproductive incompatibilities between certain potato psyllid populations, but direct evidence for Wolbachia’s role in maintaining reproductive isolation between psyllid populations was not known. An international team of researchers that included researchers at the USDA-ARS in Wapato, WA investigated the links between potato psyllid populations, presence of Wolbachia, and host plant use. They confirmed that psyllids with Wolbachia were genetically distinct from those without Wolbachia, and showed that psyllids with Wolbachia occur primarily on a common non-crop shrub called Lycium and on potato, while those without Wolbachia occur on a different weed called bittersweet nightshade and do not move to potato. Results of this study provide an improved understanding of potato psyllid biology in the Pacific Northwest and suggests that development of landscape management plans for potato psyllid should focus on populations moving from Lycium.

Technical Abstract: Changing climate and land-use practices have the potential to bring previously isolated populations of pest insects into new sympatry. This heightens the need to better understand how differing patterns of host–plant association, and unique endosymbionts, serve to promote genetic isolation or integration. We addressed these factors in populations of potato psyllid, Bactericera cockerelli (Šulc), a generalist herbivore that vectors a bacterial pathogen (Candidatus Liberibacter solanacearum, causal pathogen of zebra chip disease) of potato (Solanum tuberosum L.). Genome-wide SNP data revealed two major genetic clusters—psyllids collected from potato crops were genetically similar to psyllids found on a common weed, Lycium spp., but dissimilar from those found on another common non-crop host, Solanum dulcamara L. Most psyllids found on Lycium spp. and potato represented a single mitochondrial cytochrome oxidase I (COI) haplotype that has been suggested to not be native to the region, and whose arrival may have been concurrent with zebra chip disease first emerging. The putatively introduced COI haplotype usually co-occurred with endosymbiotic Wolbachia, while the putatively resident COI haplotype generally did not. Genetic intermediates between the two genetic populations of insects were rare, consistent with recent sympatry or reproductive isolation, although admixture patterns of apparent hybrids were consistent with introgression of genes from introduced into resident populations. Our results suggest that both host–plant associations and endosymbionts are shaping the population genetic structure of sympatric psyllid populations associated with different non-crop hosts. It is of future interest to explicitly examine vectorial capacity of the two populations and their potential hybrids, as population structure and hybridization might alter regional vector capacity and disease outbreaks