Sexual coevolution of spermatophore envelopes and female genital traits in butterflies: Evidence of male coercion?

Víctor Sánchez,Carlos Cordero

doi:10.7717/peerj.247

Víctor Sánchez, Carlos Cordero

Open Access

https://doi.org/10.7717/peerj.247

Copy DOI

Abstract

Signa are sclerotized structures located on the inner wall of the corpus bursa of female Lepidoptera whose main function is tearing open spermatophores. The sexually antagonistic coevolution (SAC) hypothesis proposes that the thickness of spermatophore envelopes has driven the evolution of the females signa; this idea is based in the fact that in many lepidopterans female sexual receptivity is at least partially controlled by the volume of ejaculate remaining in the corpus bursa. According to the SAC hypothesis, males evolved thick spermatophore envelopes to delay the post-mating recovery of female sexual receptivity thus reducing sperm competition; in response, females evolved signa for breaking spermatophore envelopes faster, gaining access to the resources contained in them and reducing their intermating intervals; the evolution of signa, in turn, favored the evolution of even thicker spermatophore envelopes, and so on. We tested two predictions of the SAC hypothesis with comparative data on the thickness of spermatophore envelopes of eleven species of Heliconiinae butterflies. The first prediction is that the spermatophore envelopes of polyandrous species with signa will be thicker than those of monandrous species without signa. In agreement with this prediction, we found that the spermatophore envelopes of a polyandrous Heliconius species with signa are thicker than those of two monandrous Heliconius species without signa. The second prediction is that in some species with signa males could enforce monandry in females by evolving “very thick” spermatophore envelopes, in these species we predict that their spermatophore envelopes will be thicker than those of their closer polyandrous relatives with signa. In agreement with this prediction, we found that in two out of three comparisons, spermatophore envelopes of monandrous species with signa have thicker spermatophore envelopes than their closer polyandrous relatives with signa. Thus, our results support the idea that selective pressures arising from sexually antagonistic interactions have been important in the evolution of spermatophore envelopes, female signa and female mating patterns.

Highlights

During sexual interactions males and females exert selection pressures on the opposite sex that can produce reciprocal adaptations in a process known as sexual coevolution (Parker, 1979; Eberhard, 1985, 1996; Holland & Rice, 1998)
We used published data about female mating pattern estimated from spermatophore counts in field collected females (Heliconius spp. (Ehrlich & Ehrlich, 1978; Walters et al, 2012); Eueides spp., Dryadula phaetusa, Dryas iulia, Philaethria diatonica and Dione juno: (Ehrlich & Ehrlich, 1978); Agraulis vanillae (Drummond, 1984); Dione moneta: data from females collected by VS in the Pedregal de San Angel ecological preserve, located in the main campus of the Universidad Nacional Autónoma de México in southern Mexico City, these females were different from those used for measuring thickness of spermatophore envelopes)
The spermatophore envelopes of the polyandrous species with signa (H. ismenius) were thicker than those of the monandrous species lacking signa (H. hortense and H. charithonia) (Kruskal-Wallis ANOVA, H2,12 = 8.33, p = 0.016; Fig. 2B). This result is in agreement with the sexually antagonistic coevolution (SAC) hypothesis that proposes that polyandry selects for males that produce thicker spermatophore envelopes to delay female remating, and that, in response, females evolved signa that allowed them to increase the rate of spermatophore digestion, increasing their remating rate (Cordero, 2005; Sánchez, Hernández-Baños & Cordero, 2011)

Summary

Introduction

During sexual interactions males and females exert selection pressures on the opposite sex that can produce reciprocal adaptations in a process known as sexual coevolution (Parker, 1979; Eberhard, 1985, 1996; Holland & Rice, 1998). In species in which females increase their fitness by mating with multiple mates, males could evolve genital structures for damaging female genitalia if this damage decreases female mating rates; these structures, in turn, could select for protective genital structures in females. In the Drosophila melanogaster species subgroup evidence indicates that females have coevolved genital structures that protect them from damage by male genital structures (Yassin & Orgogozo, 2013). Evidence suggests that the extremely complex vaginal morphology of waterfowl species coevolved with the long and complex male phallus as a cryptic choice mechanism (Brennan et al, 2007 )

Methods

Results

Conclusion