Experimental evidence for interspecific directional selection on moth pheromone communication

Abstract

The chemical composition of the sexual communication signals of female moths is thought to be under strong stabilizing selection, because females that produce atypical pheromone blends suffer lower success in finding mates. This intraspecific selection pressure cannot explain the high diversity of moth pheromone blends found in nature. We conducted experiments to determine whether communication interference from males of closely related species could exert strong enough directional selection to cause evolution of these signals. Attraction and mating success of Heliothis subflexa (Hs) females with a normal quantitative trait locus for production of acetate pheromone components (norm-OAc) were compared with Hs females with an introgressed quantitative trait locus from Heliothis virescens (Hv) that dramatically decreased the amount of acetate esters in their pheromone glands (low-OAc). In field experiments with natural Hv and Hs populations, 10 times more Hv males were captured in traps baited with live low-OAc Hs females than in traps with norm-OAc Hs females. This pattern was confirmed in mate-choice assays in cages. Hybrids resulting from Hv-Hs matings have effectively zero fitness in the field. Combining our results with the extensive data set gathered in the past 40 years on the reproductive biology of Hv, we can quantitatively estimate that the directional selection exerted by Hv males on Hs females to produce relatively high amounts (>5%) of acetates can range from 0.135 to 0.231. Such intense interspecific selection may counteract intraspecific stabilizing selection that impedes evolutionary changes in pheromone blends and could lead to diversification of sexual signals.

Fig. 1.

Frequency distributions of acetate esters in backcross females with and without the low-OAc QTL. All females genotyped in the field experiments (n = 212) and cage experiments (n = 256) were combined in this analysis.

Fig. 2.

Mean number of Hs and Hv males attracted in the field experiments to the parental species females (fem) (A and B) and to the backcross females (C and D). Hs males were captured more in traps baited with Hs females (A) or with backcross females with the norm-OAc QTL (C), whereas Hv males were attracted more to traps baited with Hv females (B) or with backcross females with the low-OAc QTL (D). The upper numbers in the bar graphs represent the number of males attracted. The lower numbers represent the number of females tested. Error bars represent SEM.

Fig. 3.

Regression and frequencies (insets) of the number of males caught in traps baited with Hs-like females with the norm-OAc QTL or the low-OAc QTL against the acetate content in the pheromone glands of these females. (A) For Hs males, a significant positive relationship is seen between the relative amount of the three acetates and the number of males lured to live females. (B) A significant negative relationship is evident between the acetate content of glands and the number of Hv males caught per female per night. These regressions show that backcross females that produced intermediate amounts of the acetate esters attracted Hs and Hv males approximately equally [females with 1% acetate esters caught 0.7 ± 0.02 (SEM) Hs males and 0.4 ± 0.01 Hv males per female per night], whereas females producing more acetate esters selectively attracted Hs males (females with 10% acetates caught 1.8 ± 0.1 Hs males per female per night and no Hv males).

Fig. 4.

Fraction of matings in the cage experiments with the parental species females (A and B) and the backcross females without and with the low-OAc QTL (C and D). In separate cages, Hs males (A and C) or Hv males (B and D) were offered a concurrent choice of Hs and Hv females (A and B) or backcross females without and with the low-OAc QTL (C and D). Mating was confirmed by presence of a spermatophore in the female’s bursa. Error bars represent SEM.