Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes

Abstract

Long distance sexual communication in moths has fascinated biologists because of the complex, precise female pheromone signals and the extreme sensitivity of males to specific pheromone molecules. Progress has been made in identifying some genes involved in female pheromone production and in male response. However, we have lacked information on the genetic changes involved in evolutionary diversification of these mate-finding mechanisms that is critical to understanding speciation in moths and other taxa. We used a combined quantitative trait locus (QTL) and candidate gene approach to determine the genetic architecture of sexual isolation in males of two congeneric moths, Heliothis subflexa and Heliothis virescens. We report behavioral and neurophysiological evidence that differential male responses to three female-produced chemicals (Z9-14:Ald, Z9-16:Ald, Z11-16:OAc) that maintain sexual isolation of these species are all controlled by a single QTL containing at least four odorant receptor genes. It is not surprising that pheromone receptor differences could control H. subflexa and H. virescens responses to Z9-16:Ald and Z9-14:Ald, respectively. However, central rather than peripheral level control over the positive and negative responses of H. subflexa and H. virescens to Z11-16:OAc had been expected. Tight linkage of these receptor genes indicates that mutations altering male response to complex blends could be maintained in linkage disequilibrium and could affect the speciation process.Other candidate genes such as those coding for pheromone binding proteins did not map to this QTL, but there was some genetic evidence of a QTL for response to Z11-16:OH associated with a sensory neuron membrane protein gene.mating | speciation | AFLP | odorant receptor | Heliothis E volutionary diversification of sexual communication traits remains paradoxical (1, 2) because signal production and signal reception are under independent genetic control, and a mutation causing an alteration in one component of the system is predicted to reduce efficiency of communication and to cause a loss of fitness. The resulting stabilizing selection is expected to promote evolutionary stasis, not diversification (3-5). Systems in which changes in signals and responses are governed by the same genetic alterations (i.e., pleiotropy) should be less evolutionarily constrained in many cases (6), and studies of mating communication have revealed a few systems that appear to have this property (7-9). However, no pleiotropy has been found between signal production and response in moths (e.g., 5, 10). Because female and male moths with divergent signals and responses appear to be selected against (11, 12), we have no simple explanation for the great diversity of moths (∼180,000 species) and moth pheromones (5,13,14).Beyond capturing the attention of evolutionary biologists, the diversity of long distance, pheromone-based sexual communication traits in moths has become a focus of some molecular biologists, biochemists, neurophysiologists, and communi...

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

“…In strong support of this idea, Gould et al (14) showed that a cluster of OR genes expressed in the antenna is very tightly linked to an autosomal gene controlling the interspecific difference in male behavioral response among Heliothis virescens and Heliothis subflexa. Moreover, single-cell recordings showed that species-specific spike-amplitude responses to individual pheromone components were also linked to the OR cluster (14). In O. nubilalis, five of the seven pheromone ORs are located within a large cluster on the Z chromosome (34).…”

“…The distance between the different loci is measured in centimorgans, and the LOD scores obtained for the ORs and the second peak are shown in boldface type. responses and most of the neurophysiological responses to pheromone components cosegregated with the autosomal OR cluster (14). The candidate genes in the Resp QTL region (Table 1) suggest that other factors affect the structure, function, or connectivity of the OSNs or other neurons in the antennal lobe or elsewhere in the brain.…”

“…There is empirical evidence for such selection against deviance in moths (4, 10, 11). A coordinated change of both signal and response would seem necessary to overcome this problem but is hard to imagine because genes affecting female pheromone production and male response are different and reside on separate chromosomes (12)(13)(14)(15)(16)(17). Moreover, despite significant advances in the biochemistry of pheromone synthesis and the physiology of pheromone detection, the identity and mode of action of most genes that shape these traits are unknown.…”

On the scent of pleiotropy

“…Indeed, case studies indicating an absence of genetic coupling abound. For instance, in several species of moth, including the almond moth (6), adzuki borer moth (7), corn borer moth (8), and heliothine moths (9,10), it is quite clear that the female pheromone signal and male response are under separate genetic control. Similarly, male and female mating behaviors in Drosophila arizonensis and Drosophilia mojavenis have distinct genetic bases (11), as do pheromone production and response in the pine engraver beetle (12).…”

Expression of a desaturase gene,desat1, in neural and nonneural tissues separately affects perception and emission of sex pheromones inDrosophila

“…However, the basic genetic architecture of prezygotic sexual isolation remains largely unexplored in most natural populations (4,5), and there is very little empirical evidence for tight genetic linkage between the emission and reception of a sensory signal (6)(7)(8)(9). Theoritical prediction and experimental studies assume that the "emission/reception coupling" depends on the inheritance of separate genes found on the same or on different chromosomes and linked with a high probability (linkage desequilibrium (10)(11)(12)(13)(14), whereas the "single-gene" hypothesis seems very unlikely (4), as the tissues involved in the emission and perception of sensory signals are usually different (15).…”