Moths Behaving like Butterflies. Evolutionary Loss of Long Range Attractant Pheromones in Castniid Moths: A Paysandisia archon Model

Abstract

BackgroundIn the course of evolution butterflies and moths developed two different reproductive behaviors. Whereas butterflies rely on visual stimuli for mate location, moths use the ‘female calling plus male seduction’ system, in which females release long-range sex pheromones to attract conspecific males. There are few exceptions from this pattern but in all cases known female moths possess sex pheromone glands which apparently have been lost in female butterflies. In the day-flying moth family Castniidae (“butterfly-moths”), which includes some important crop pests, no pheromones have been found so far.Methodology/Principal FindingsUsing a multidisciplinary approach we described the steps involved in the courtship of P. archon, showing that visual cues are the only ones used for mate location; showed that the morphology and fine structure of the antennae of this moth are strikingly similar to those of butterflies, with male sensilla apparently not suited to detect female-released long range pheromones; showed that its females lack pheromone-producing glands, and identified three compounds as putative male sex pheromone (MSP) components of P. archon, released from the proximal halves of male forewings and hindwings.Conclusions/SignificanceThis study provides evidence for the first time in Lepidoptera that females of a moth do not produce any pheromone to attract males, and that mate location is achieved only visually by patrolling males, which may release a pheromone at short distance, putatively a mixture of Z,E-farnesal, E,E-farnesal, and (E,Z)-2,13-octadecadienol. The outlined behavior, long thought to be unique to butterflies, is likely to be widespread in Castniidae implying a novel, unparalleled butterfly-like reproductive behavior in moths. This will also have practical implications in applied entomology since it signifies that the monitoring/control of castniid pests should not be based on the use of female-produced pheromones, as it is usually done in many moths.

Paysandisia archon: Behavior, Ecology, and Communication

“…A different type of mate-localization behavior was observed by Sarto i Monteys et al (2012), in which the perching or patrolling male first locates and approaches the female. In some butterflies, one individual can perform both types of behavior or can alternate between the two, depending on ecological factors (Scott 1974;Dennis and Shreeve 1988).…”

“…In some butterflies, one individual can perform both types of behavior or can alternate between the two, depending on ecological factors (Scott 1974;Dennis and Shreeve 1988). However, no data were reported by Sarto i Monteys et al (2012) on the "perching index"-the proportion of copulations initiated by a sitting male relative to a flying male (Scott 1974).…”

“…Sarto i Monteys et al (2012) reported that the P. archon male wing appears to distribute a scent over the female antenna during the pair flight. Putative short-range male pheromones have been identified from the proximal halves of male forewings and hindwings.…”

“…Putative short-range male pheromones have been identified from the proximal halves of male forewings and hindwings. These compounds are released in a passive process associated with the flight phase of the courtship, inducing the female to alight (Sarto i Monteys et al 2012).…”

“…The androconia release huge quantities of the pheromone-like compound E2,Z13-16:OH (Frérot et al 2013). This compound was first identified by Sarto i Monteys et al (2012) but from wing extracts, probably because of passive adsorption on the wing cuticle. This compound was previously identified in other Sesioidea, confirming the classification of P. archon and, by extension, the Castniid family in the Sesioidea, in this systematic group.…”