Did maize domestication and early spread mediate the population genetics of corn leafhopper?

ABSTRACT

Investigating how crop domestication and early farming mediated crop attributes, distributions, and interactions with antagonists may shed light on today's agricultural pest problems. Crop domestication generally involved artificial selection for traits desirable to early farmers, for example, increased productivity or yield, and enhanced qualities, though invariably it altered the interactions between crops and insects, and expanded the geographical ranges of crops. Thus, some studies suggest that with crop domestication and spread, insect populations on wild crop ancestors gave rise to pestiferous insect populations on crops. Here, we addressed whether the emergence of corn leafhopper (Dalbulus maidis) as an agricultural pest may be associated with domestication and early spread of maize (Zea mays mays). We used AFLP markers and mitochondrial COI sequences to assess population genetic structuring and haplotype relationships among corn leafhopper samples from maize and its wild relative Zea diploperennis from multiple locations in Mexico and Argentina. We uncovered seven corn leafhopper haplotypes contained within two haplogroups, one haplogroup containing haplotypes associated with maize and the other containing haplotypes associated with Z. diploperennis in a mountainous habitat. Within the first haplogroup, one haplotype was predominant across Mexican locations, and another across Argentinean locations; both were considered pestiferous. We suggested that the divergence times of the maize-associated haplogroup and of the "pestiferous" haplotypes are correlated with the chronology of maize spread following its domestication. Overall, our results support a hypothesis positing that maize domestication favored corn leafhopper genotypes preadapted for exploiting maize so that they became pestiferous, and that with the geographical expansion of maize farming, corn leafhopper colonized Z. diploperennis, a host exclusive to secluded habitats that serves as a refuge for archaic corn leafhopper genotypic diversity. Broadly, our results help explain the extents to which crop domestication and early spread may have mediated the emergence of today's agricultural pests.