Isolation by distance, source-sink population dynamics and dispersal facilitation by trade routes: impact on population genetic structure of a stored grain pest

Authors: CORDEIRO, ERICK M. - Kansas State University; Campbell, James - Jim; PHILLIPS, THOMAS - Kansas State University; AKHUNOV, EDUARD - Kansas State University

Submitted to: G3, Genes/Genomes/Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/11/2019
Publication Date: 5/1/2019
Citation: Cordeiro, E.G., Campbell, J.F., Phillips, T., Akhunov, E. 2019. Isolation by distance, source-sink population dynamics and dispersal facilitation by trade routes: impact on population genetic structure of a stored grain pest. G3, Genes/Genomes/Genetics. 9(5):1457-1468. https://doi.org/10.1534/g3.118.200892.
DOI: https://doi.org/10.1534/g3.118.200892

Interpretive Summary: Large scale patterns of insect dispersal and the corresponding effects on movement of genes leads to development of population structure that has important implications for pest management. Previous studies have tended to find little evidence of population structure for stored product insects and it has been hypothesized that this is due to the movement of insects in grain as it is transported and mixed, but could also be due to limitations to the analytical approaches used. Applying a new molecular population genetic technique that can generate a large number of molecular markers, lesser grain borer populations collected from 11 locations across the United States were shown to have increased genetic isolation with increased geographical distance, which is consistent with predictions based on population genetics. However, other factors also appear to be important in generating population structure. There was a significant effect of ecological region where the insects were collected, but no significant effect of whether location was in a primarily rice or wheat growing region. Variables associated with amount of wheat produced and stored and the shipment of wheat by railroad also appeared to explain some of the variation among beetle collection locations. Whether the region of the U.S. where the beetles were collected is a net source for wheat production and shipment or a net sink, or receiver, of wheat impacted population differentiation and diversity. This information can help in improving pest management programs, such as understanding sources of infestation and how insecticide resistance may develop and spread.

Technical Abstract: Population structure of agricultural insect pests is likely impacted not only by geographic distance and ecoregions, but also by patterns of crop production and distribution of the harvested commodity into and out of a region, such that different geographic regions are potential sources and sinks. We used 209 adult beetles of the stored grain pest Rhyzopertha dominica collected at 11 different sites across the United States that were sequenced using double digest RADseq to generate 5379 SNP markers to assess the genetic diversity and genetic structure of presumed demic populations. Genetic data indicated that nucleotide diversity values were similar among populations, but tended to be lower in small wheat-production areas and greater in large wheat-production areas. Ecoregions, such as the Mississippi Valley or Central Valley of California, were more important in explaining structure of R. dominica populations (FSC=0.023, p<0.001) than crop type (i.e., rice or wheat regions) (FCT=0.003; p> 0.05; AMOVA hierarchical analysis), suggesting insect movement between rice and wheat growing regions. Although isolation by distance (IBD) was significant according to the Mantel test (r=0.68; p=0.003), a substantial degree of admixture between populations was found. A model selection approach elected the volume of grain received, wheat acreage, and average geographical distance to other locations as the most important variables to explain the degree of population differentiation and diversity found in R. dominica populations in the United States. We conclude that R. dominica populations experienced isolation by distance, but the degree of genetic similarity and the admixture by gene flow is also affected by commercial grain movement by railroads and the acreage of wheat being grown and stored in the surrounding area. A source-sink dynamic has been suggested as a suitable model to explain grain movement in the U.S., and it seems to have a significant impact on the genetics of insect populations associated with grain commodities as well.