Males perceive honest information from female released sex pheromone in a moth

There is accumulating evidence that male insects advertise their quality to conspecific females through pheromones. However, most studies of female released sex pheromone assume information transfer regarding merely the species of the female and her mating status. We show that more and precise information is conveyed through the female sex pheromone, positioning it as an honest sexual trait. We demonstrate that females in bad physical conditions (small, starved or old) lay significantly fewer eggs than females in good conditions (large, fed or young). The ratio of the sex pheromone blend in gland extracts of female pink bollworm moths accurately describes the female phenotypic condition whereas the pheromone amount in the glands fails to provide an honest signal of quality. Moreover, males use the female released pheromone blend to choose their mates and approach females that signal higher reproductive potential. In addition, surrogating the female effect, using synthetic pheromone blend that represents that of higher quality females (0.6:0.4 ZZ:ZE) more males were attracted to this blend than to the blend representing the population mean (0.5:0.5 ZZ:ZE). Both, female advertisement for males and the male choosiness, suggest that pheromones have evolved as sexual traits under directional, sexual selection.

Early-exposure to new sex pheromone blend alters mate preference in female butterflies and in their offspring

Insects use species-specific sex pheromone blends to attract members of the opposite sex which express the corresponding molecular receptors. Given this lock and key mechanism used for species identification and mate choice, it is currently not well understood how pheromone blends or receptor systems evolve. One possibility is that insects develop preferences for new sex pheromone blends via the process of learning, and that these learned preferences may be passed on to the next generation. We tested these hypotheses by exposing newly emerged Bicyclus anynana female butterflies to either wild type or to modified male sex pheromone blends. A few days later, we scored female mating outcome in a choice trial involving both male types. We also assessed the mating outcome of naïve offspring of females that underwent distinct odor learning trials to test for a potential inheritance of learned odor preferences. Naïve (parental) females mated preferentially with Wt-blend males, but females pre-exposed to new blends either shifted their preference to new-blend males, or mated equally with males of either blend type; the response depending on the new blend they were introduced to. Naïve daughters of females who were exposed to new-blend males behaved similarly to their experienced mothers. We demonstrate that females are able to learn preferences for novel pheromone blends in response to a short social experience, and pass that learned preference down to the next generation. This suggests that learning can be a key factor in the evolution of sex pheromone blend recognition and in chemosensory speciation.Significance statementWhile the diversity of sex pheromone communication systems across insects is well documented, the mechanisms that lead to such diversity are not well understood. Sex pheromones constitute a species-specific system of sexual communication that reinforces interspecific reproductive isolation. When odor blends evolve, the efficacy of male-female communication becomes compromised, unless preference for novel blends also evolves. We explore odor learning as a possible mechanism leading to changes in sex pheromone preferences. We show that preferences for new blends can develop following a short learning experience, and that these novel preferences can be transmitted to the next generation. To our knowledge, this is the first investigation of sex pheromone blend preference learning impacting mate choice and being inherited in an insect.

Within-population variability in a moth sex pheromone blend: genetic basis and behavioural consequences

Evolutionary diversification of sexual communication systems in moths is perplexing because signal and response are under stabilizing selection in many species, and this is expected to constrain evolutionary change. In the moth Heliothis virescens , we consistently found high phenotypic variability in the female sex pheromone blend within each of four geographically distant populations. Here, we assess the heritability, genetic basis and behavioural consequences of this variation. Artificial selection with field-collected moths dramatically increased the relative amount of the saturated compound 16:Ald and decreased its unsaturated counterpart Z11–16:Ald, the major sex pheromone component (high line). In a cross between the high- and low-selected lines, one quantitative trait locus (QTL) explained 11–21% of the phenotypic variance in the 16:Ald/Z11–16:Ald ratio. Because changes in activity of desaturase enzymes could affect this ratio, we measured their expression levels in pheromone glands and mapped desaturase genes onto our linkage map. A delta-11-desaturase had lower expression in females producing less Z11–16:Ald; however, this gene mapped to a different chromosome than the QTL. A model in which the QTL is a trans-acting repressor of delta-11 desaturase expression explains many features of the data. Selection favouring heterozygotes which produce more unsaturated components could maintain a polymorphism at this locus.