Genetic mapping of male pheromone response in the European corn borer identifies candidate genes regulating neurogenesis

Abstract

The sexual pheromone communication system of moths is a model system for studies of the evolution of reproductive isolation. Females emit a blend of volatile components that males detect at a distance. Species differences in female pheromone composition and male response directly reinforce reproductive isolation in nature, because even slight variations in the species-specific pheromone blend are usually rejected by the male. The mechanisms by which a new pheromone signal-response system could evolve are enigmatic, because any deviation from the optimally attractive blend should be selected against. Here we investigate the genetic mechanisms enabling a switch in male response. We used a quantitative trait locus-mapping approach to identify the genetic basis of male response in the two pheromone races of the European corn borer, Ostrinia nubilalis. Male response to a 99:1 vs. a 3:97 ratio of the E and Z isomers of the female pheromone is governed by a single, sex-linked locus. We found that the chromosomal region most tightly linked to this locus contains genes involved in neurogenesis but, in accordance with an earlier study, does not contain the odorant receptors expressed in the male antenna that detect the pheromone. This finding implies that differences in the development of neuronal pathways conveying information from the antenna, not differences in pheromone detection by the odorant receptors, are primarily responsible for the behavioral response differences among the males in this system. Comparison with other moth species reveals a previously unexplored mechanism by which male pheromone response can change in evolution.Ostrinia nubilalis | Z chromosome | pheromone response | sexual communication | QTL analysis

A combination of sexual and ecological divergence contributes to rearrangement spread during initial stages of speciation

“…Although recombination suppression is directly observed in our single between‐strain pedigree, Koutroumpa et al . () found a major QTL for male pheromone response segregating among collinear sex chromosomes. Furthermore, at Landisville where bivoltine populations occur and sampled males came from E or Z pheromone‐specific traps (Linn et al .…”

“…; Koutroumpa et al . ). Blastn searches of GBS sequences against amplicons identified shared markers.…”

Introgression between divergent corn borer species in a region of sympatry: Implications on the evolution and adaptation of pest arthropods

“…Such an imbalance in mating success and selection for advantageous introgressed alleles within hybrid zones may impact the observed displacement of O. nubilalis from the region, but additional investigation is warranted. The genetics of male Ostrinia pheromone response is yet to be fully resolved, but is known to involve genes on the Z chromosome that may influence neural development (Dopman, Bogdanowicz, & Harrison, ; Koutroumpa et al., ). The role of this potentially “hardwired” male response in relation to the functionally divergent Z chromosome‐linked OR4 (Leary et al., ) and courtship behaviour remains unknown, and it is intriguing to hypothesize about the impact of hybridization of F 1 and backcross males in regard to mate preferences as determined by species origin and epistatic interaction of genes on the Z chromosome.…”

“…Prior studies have demonstrated that a small proportion of males of both O. nubilalis and O. furnacalis responded to interspecific female pheromone blends at long distances within nonchoice wind tunnel experiments (Linn, Musto, & Roelofs, ; Linn, O'Connor, & Roelofs, ; Martin, Moore, Musto, & Linn, ). The basis of this interspecies sex pheromone response of these “rare” males was found to reside within the lack of antagonistic neuron signalling (Domingue, Musto, Linn, Roelofs, & Baker, ), but the exact structural or functional changes that give rise to these neurological responses downstream of OR4 are yet to be resolved (Groot, Dekker, & Heckel, ; Koutroumpa, Groot, Dekker, & Heckel, ). Regardless, the asymmetric tracking hypothesis proposes that males respond to a greater diversity of pheromones compared the corresponding range of pheromones produced by cognate females within the same species (Phelan, ) and in doing so provide a reproductive advantage.…”

Influence of host plant, geography and pheromone strain on genomic differentiation in sympatric populations of Ostrinia nubilalis

“…Estimates of hybridization and positive assortative mating based on this autosomal marker vary among natural populations (Coates, Johnson, et al, 2013). Resp is located within a region of the Z-chromosome that encodes a suite of genes putatively involved in neuronal development and function (Koutroumpa, Groot, Dekker, & Heckel, 2016). In addition to Resp, a major QTL for voltinism differences between strains is located on the Z-chromosome (Dopman et al, 2004).…”