Coevolution between Male and Female Genitalia in the Drosophila melanogaster Species Subgroup

Abstract

In contrast to male genitalia that typically exhibit patterns of rapid and divergent evolution among internally fertilizing animals, female genitalia have been less well studied and are generally thought to evolve slowly among closely-related species. As a result, few cases of male-female genital coevolution have been documented. In Drosophila, female copulatory structures have been claimed to be mostly invariant compared to male structures. Here, we re-examined male and female genitalia in the nine species of the D. melanogaster subgroup. We describe several new species-specific female genital structures that appear to coevolve with male genital structures, and provide evidence that the coevolving structures contact each other during copulation. Several female structures might be defensive shields against apparently harmful male structures, such as cercal teeth, phallic hooks and spines. Evidence for male-female morphological coevolution in Drosophila has previously been shown at the post-copulatory level (e.g., sperm length and sperm storage organ size), and our results provide support for male-female coevolution at the copulatory level.

Co-option of an Ancestral Hox-Regulated Network Underlies a Recently Evolved Morphological Novelty

“…The posterior lobe is a hook-shaped outgrowth unique to the external genitalia of D. melanogaster and its closest relatives in the melanogaster clade (Figure 1) (Jagadeeshan and Singh, 2006; Kopp and True, 2002). A cuticular projection similar to the posterior lobe is also present in the yakuba clade (Yassin and Orgogozo, 2013), suggesting a recent origin of this structure in the melanogaster subgroup (Figure S1). Among members of the melanogaster clade, the posterior lobe is highly divergent in shape and size, and represents the only reliable character to distinguish species identity (Coyne, 1993).…”

Mechanisms and Evidence of Genital Coevolution: The Roles of Natural Selection, Mate Choice, and Sexual Conflict

“…A genetic covariance exists between male damage and female susceptibility to damage exists in this species as evidenced by a full sib/half sib design (Gay et al 2011). A recent comparative study in the Drosophila melanogaster species complex, revealed previously unknown internal and external female adaptations some of which appear to counteract or prevent the damage cause by male genital structures, therefore likely evolving by SAC, whereas others seeming to facilitate copulation, therefore evolving by female choice (Yassin and Orgogozo 2013).…”

“…For example, female genitalia in Drosophila were deemed to be fairly invariant across species (Eberhard and Ramirez 2004;Jagadeeshan and Singh 2006), but a recent study showed that in nine species of Drosophila, several aspects of female genital morphology covary with male genital traits ( Fig. 2) (Yassin and Orgogozo 2013). A geometric morphometric analysis of genital shape among two sister species of water snakes (Nerodia sp.)…”

“…For this reason alone, coevolution between genital morphologies of males and females is expected. Morphological and genetic components of male and female genitalia have been shown to covary in many taxa (Sota and Kubota 1998;Ilango and Lane 2000;Arnqvist and Rowe 2002;Brennan et al 2007;Rönn et al 2007;Kuntner et al 2009;Tatarnic and Cassis 2010;Cayetano et al 2011;Evans et al 2011Evans et al , 2013Simmons and García-González 2011;Yassin and Orgogozo 2013; and see examples in Table 1). The likely mechanism is that suggested by the authors, and it includes sexually antagonistic coevolution (SAC), natural selection, sexual selection, female choice, or none specified.…”

Copulatory Wounding and Traumatic Insemination

“…Females in the melanogaster group show a pattern of sclerotized structures that are hypothesized to function as a resistance adaptation (Kamimura and Mitsumoto 2011;Yassin and Orgogozo 2013). Correspondingly, interspecific matings between the sister species Drosophila santomea and Drosophila yakuba resulted in more damaging CW than in intraspecific matings (Kamimura 2012).…”