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

Sexual 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.We 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.Our results support the hypothesis that signa are a product of sexually antagonistic coevolution with spermatophore envelopes

Phylogenetic mapping of mating pattern and presence of signa in a sample of Lepidoptera.

<p>Consensus supertree for 37 taxa (plus outgroup) of Lepidoptera in which female mating pattern (monandry/polyandry) and presence/absence of the female genital trait known as signa are mapped. References of source phylogenies are in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022642#pone-0022642-t001" target="_blank">Table 1</a>.</p

A sampler of the morphological diversity of signa in female Lepidoptera.

<p>Each signum is indicated by an “S”. (A) <i>Callophrys xami</i> (Lycaenidae): signa are a pair of thin thorns. (B) <i>Erbessa priverna</i>: (Notodontidae): signum is a plate covered by small thorns. (C) <i>Pyrisitia nise</i> (Pieridae): signum is a strong structure covered by thick spines of different lengths. (D) <i>Ephialtias draconis</i> (Notodontidae): signum is a long, narrow, concave structure with thin spines along the margins of its internal surface. In (A), (C) and (D) the signa are observed through the wall of the corpus bursae, whereas in (B) the corpus bursae was opened and two spermatophores removed. In (B) several deciduous cornuti shed from the male endophallus are attached to the corpus bursae wall, and in (C) there are spermatophore remains within the corpus bursae. db: ductus bursae. Photographs are at different scales.</p

Sources of data on signa (presence or absence), female mating pattern (polyandry or monandry) and phylogeny, used in the comparative phylogenetic analysis summarized in Figure 3.

<p>Information on signa was obtained for all taxa listed in the “Species” column, whereas data on mating pattern was obtained only for taxa marked with an asterisk. The characters used for phylogenetic reconstruction in the source phylogenies are as following: <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022642#pone.0022642-Arnqvist2" target="_blank">[57]</a>: morphological and ecological; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022642#pone.0022642-Clench2" target="_blank">[51]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022642#pone.0022642-Penz2" target="_blank">[58]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022642#pone.0022642-Cordero3" target="_blank">[59]</a>: morphological; <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022642#pone.0022642-Gage1" target="_blank">[60]</a>: molecular (28S ribosomal RNA and mitochondrial ND1); <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022642#pone.0022642-Ackery1" target="_blank">[61]</a>: molecular (mitochondrial COI-COII region and nuclear gene <i>wingless</i>); <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022642#pone.0022642-Speidel1" target="_blank">[62]</a>: molecular (nuclear gene <i>wingless</i>). Species names were actualized according to information in <a href="http://www.nic.funet.fi/pub/sci/bio/life/intro.html" target="_blank">www.nic.funet.fi/pub/sci/bio/life/intro.html</a> (consulted 5/26/2011); a table with the names used in the original references can be obtained from the corresponding author.</p