Sensory trap as the mechanism of sexual selection in a damselfly genitalic trait (Insecta: Calopterygidae)

During copulation, males of some calopterygid damselfly species displace the sperm stored in the spermatheca: the male genital appendages enter into the spermathecal ducts and physically remove sperm. In Calopteryx haemorrhoidalis, the genital appendages are too wide to penetrate the spermathecae, but males use a different mechanism in which the aedeagus stimulates the vaginal sensilla that control spermathecal sperm release. Since these sensilla are used during egg fertilization and oviposition, it was hypothesized that this function evolved before the male stimulatory ability. I investigated this using Hetaerina cruentata, a species whose position in the Calopterygidae phylogeny is more basal than Calopteryx. Given this position and having determined that males of this species are not able to displace sperm of their conspecific females during copulation, it was expected that H. cruentata females would eject sperm when stimulated with the aedeagi of C. haemorrhoidalis but not when stimulated with the aedeagi of their conspecifics. This prediction was confirmed. In order to investigate the widespread nature of this result, some other Calopteryx species-Calopteryx xanthostoma and Calopteryx virgo-were investigated. The results were similar to those of H. cruentata: conspecific males were unable to stimulate their females, but females ejected sperm when stimulated with C. haemorrhoidalis aedeagi. Morphometric analysis suggests that the mechanistic explanation for the stimulatory ability of C. haemorrhoidalis genitalia is that the aedeagal region that makes contact with the vaginal sensilla is wider in C. haemorrhoidalis than in the other species. These results suggest that the sensory "bias" shown and shared by H. cruentata, Calopteryx splendens, C. virgo, and C. haemorrhoidalis females represents an ancestral condition and that the male stimulatory ability is absent in the evolutionary history of the clade. These pieces of evidence as well as another one presented elsewhere, which indicates that C. haemorrhoidalis males vary in their stimulatory ability, constitute the three criteria for a case of sexual selection via exploitation of a female sensory bias. These results also provide support to the sensory trap hypothesis that indicates that the female bias-in this case, egg fertilization and oviposition-evolved in a context different from sexual selection. Considering that the male genital appendages responsible for physically removing spermathecal sperm in other calopterygids are present in C. haemorrhoidalis, I suggest that males were once able to displace spermathecal spermphysically. Such ability may have been later impeded by a reduction in size of the spermathecal ducts. Possibly, one of the latest events in this sequence is the male's stimulatory ability. This hypothetical series of events suggests a coevolutionary scenario in which the central actor is the sperm stored in the spermathecae.