The Inheritance of the Pheromone Sensory System in Two Helicoverpa Species: Dominance of H. armigera and Possible Introgression from H. assulta

Abstract

Hybridization of sympatric closely related species may sometimes lead to introgression and speciation. The sister species Helicoverpa armigera and Helicoverpa assulta both use (Z)-11-hexadecenal and (Z)-9-hexadecenal as sex pheromone components but in reversed ratios. Female H. armigera and male H. assulta could hybridize and produce fertile male hybrids, which can then backcross with females of the two parent species to get backcross lines in the laboratory. In this study, we compared the olfactory responses to pheromone compounds in the periphery and in the antennal lobes (ALs) of males of the two species, as well as of their hybrids and backcrosses. Single-sensillum recordings were carried out to explore characteristics of male-specific sensilla on the antennae, and in vivo calcium imaging combined with digital 3D-reconstruction was used to describe what happens in the macroglomerular complex (MGC) of the AL. The results show that the population ratio of the two male-specific types of olfactory sensory neurons responding to two sex pheromone components are controlled by a major gene, and that the allele of H. armigera is dominant. Consistently, the study of the representative areas activated by sex pheromone components in the ALs further support the dominance of H. armigera. However, the topological structure of the MGC in the hybrid was similar but not identical to that in H. armigera. All subtypes of male-specific sensilla identified in the two species were found in the male hybrids and backcrosses. Moreover, two new subtypes with broader response spectra (the expanded A subtype and the expanded C subtype) emerged in the hybrids. Based on the inheritance pattern of the pheromone sensory system, we predict that when hybridization of female H. armigera and male H. assulta occurs in the field, male hybrids would readily backcross with female H. armigera, and introgression might occur from H. assulta into H. armigera through repeated backcrossing.

Review of pheromone receptors in heliothine species: expression, function, and evolution

“…The pheromone‐sensitive sensilla have been characterized by single sensillum recording in male antennae of H. virescens (Almaas & Mustaparta, 1991; Berg et al, 1995), H. subflexa (Baker et al, 2004), H. zea (Grant et al, 1989; Cossé et al, 1998), H. armigera (Wu et al, 2013, 2015, Chang et al, 2016; Xu et al, 2016), and H. assulta (Berg & Mustaparta, 1995; Berg et al, 2005; Wu et al, 2013, 2015; Chang et al, 2016; Xu et al, 2016). Based on the tuning specificity, the pheromone‐sensitive sensilla are classified into three functional types, A, B, and C: type A specifically responds to Z11‐16:Ald, type B responds to Z9‐14:Ald, and type C to Z9‐16:Ald, Z9‐14:Ald, and some other structurally related compounds (Berg & Mustaparta, 1995; Cossé et al, 1998; Baker et al, 2004; Wu et al, 2015; Xu et al, 2016, 2017). B‐ and C‐type sensilla are further classified into subtypes according to their response spectra in H. armigera and H. assulta (Xu et al, 2016).…”

“…F1 male analysis proved that the mutation with one copy of some PRs would suffice to react to the pheromone components, and could broaden the tuning of its ORN (Gould et al, 2010). From the hybridization analysis from H. armigera and H. assulta , it is demonstrated that the population ratio of the two male‐specific types of olfactory sensory neurons responding to two sex pheromone components is controlled by a major gene, and that the allele of H. armigera is dominant (Xu et al, 2017). Moreover, two new subtypes with broader response spectra emerged in the hybrids, implying introgression related to PR genes might occur from H. assulta into H. armigera through repeated backcrossing (Xu et al, 2017).…”

“…From the hybridization analysis from H. armigera and H. assulta , it is demonstrated that the population ratio of the two male‐specific types of olfactory sensory neurons responding to two sex pheromone components is controlled by a major gene, and that the allele of H. armigera is dominant (Xu et al, 2017). Moreover, two new subtypes with broader response spectra emerged in the hybrids, implying introgression related to PR genes might occur from H. assulta into H. armigera through repeated backcrossing (Xu et al, 2017). The evolutionary mechanism of PRs diversification needs to be analyzed further, especially from the hybrids.…”

Comparison of male antennal morphology and sensilla physiology for sex pheromone olfactory sensing between sibling moth species: Ectropis grisescens and Ectropis obliqua (Geometridae)

“…A study of closely related species of Helicoverpa moths indicated that the position of the MGC corresponding to the H. assulta antagonist differed between H. armigera and H. assulta (Wu et al, ). This difference in position of the MGC might have hereditary importance for species differentiation (Xu et al, ). Therefore, the functional difference of Z3,epo6,Z9–19:H between species might originate in the primary olfactory center (the AL), and further research should investigate this question.…”

Anatomical Comparison of Antennal Lobes in Two Sibling Ectropis Moths: Emphasis on the Macroglomerular Complex

“…Sibling moth species generally have the same number of MGC glomeruli. Nevertheless, the position of the MGC glomeruli is slightly different in Helicoverpa species (Xu et al, 2016a , b ), while the same number and position of MGC glomeruli are present in Heliothine species (Vickers and Christensen, 2003 ). The study of two Helicoverpa sibling species, Helicoverpa armigera and H. assulta , showed that different combinations of certain glomeruli positions and volumes in the MGC could reflect the ratio of the major and minor sex pheromone compartments, which play a vital role in sex pheromone discrimination (Wu et al, 2013 ).…”