The Evolution of a Female Genital Trait Widely Distributed in the Lepidoptera: Comparative Evidence for an Effect of Sexual Coevolution

Abstract

BackgroundSexual coevolution is considered responsible for the evolution of many male genital traits, but its effect on female genital morphology is poorly understood. In many lepidopterans, females become temporarily unreceptive after mating and the length of this refractory period is inversely related to the amount of spermatophore remaining in their genital tracts. Sperm competition can select for males that delay female remating by transferring spermatophores with thick spermatophore envelopes that take more time to be broken. These envelopes could select for signa, sclerotized sharp structures located within the female genital tract, that are used for breaking spermatophores. Thus, this hypothesis predicts that thick spermatophore envelopes and signa evolve in polyandrous species, and that these adaptations are lost when monandry evolves subsequently. Here we test the expected associations between female mating pattern and presence/absence of signa, and review the scant information available on the thickness of spermatophore envelopes.Methodology/Principal FindingsWe made a literature review and found information on female mating pattern (monandry/polyandry), presence/absence of signa and phylogenetic position for 37 taxa. We built a phylogenetic supertree for these taxa, mapped both traits on it, and tested for the predicted association by using Pagel's test for correlated evolution. We found that, as predicted by our hypothesis, monandry evolved eight times and in five of them signa were lost; preliminary evidence suggests that at least in two of the three exceptions males imposed monandry on females by means of specially thick spermatophore envelopes. Previously published data on six genera of Papilionidae is in agreement with the predicted associations between mating pattern and the characteristics of spermatophore envelopes and signa.Conclusions/SignificanceOur results support the hypothesis that signa are a product of sexually antagonistic coevolution with spermatophore envelopes.

Sexual Selection Within the Female Genitalia in Lepidoptera

“…Sánchez et al (2011) tested this prediction by means of a comparative study of 37 taxa, finding statistical support for the prediction. They found that: (1) polyandry and presence of signa are plesiomorphic for the taxa analyzed; (2) as expected from the SAC hypothesis, 93 % of polyandrous species had signa, in comparison with only 33.3 % in monandrous species; (3) the phylogenetically controlled analysis also found support for the predicted association between female mating pattern and presence of signa; (4) monandry evolved eight times and in five of them, its evolution was associated with the loss of signa; and (5) signa were lost seven times, five of them in taxa that evolved monadry.…”

“…Signa are present in numerous species belonging to most families of Lepidoptera. Their shape, size, texture, position, and number vary widely (e.g., Sánchez et al 2011;Lincango et al 2013), and Figs. 12.1b and 12.2b-f only provide a glimpse of this variation.…”

“…12.1b and 12.2b-f only provide a glimpse of this variation. Such variation suggests that signa evolved rapidly and divergently (Sánchez et al 2011). The phylogenetic reconstruction of the Lepidoptera has received much attention (Regier et al 2013), and the available information on the ground plan of the order, including primitive subgroups and relation with sister orders, is excellent (Kristensen 1999).…”

“…However, Simmons (2014) claims that the absence of rapid and divergent evolution in female genital morphology probably is not real, but results of the inadequate study of female genitalia by taxonomists (see also Ah-King et al 2014). Although Eberhard (1985) discarded this explanation by mentioning that in several groups in which female genitalia have been considered by taxonomists, they tend to be uniform, there is an increasing number of studies showing that male genital morphology and female genital morphology have coevolved in several groups of animals producing complex and diverse structures that play a broad gamut of functions (reviews in Sánchez et al 2011;Simmons 2014).…”

“…However, there is a large amount of taxonomic papers and books that clearly show that the female genitalia of many (probably most) Lepidoptera are complex organs (Figs. 12.1b and 12.2), composed of several structures that exhibit great diversity of shapes, sizes, positions, and, possibly, functions, suggesting that they have evolved in a relatively rapid and divergent way (Sánchez et al 2011;Lincango et al 2013). As explained in the following section, although there are hundreds of detailed descriptions of the genitalia of female Lepidoptera, knowledge about the functions of its different structures is rather poor.…”