170 Years of “Lock-and-Key”: Genital Morphology and Reproductive Isolation

Abstract

The divergent genital morphology observed among closely related animal species has long been posited as a mechanism of reproductive isolation. Despite the intuitive appeal that rapidly evolving genitalia might cause speciation, evidence for its importance—or even its potential—in reproductive isolation is mixed. Most tests of genital structural isolation between species often fail to find convincing evidence that differences in morphology prevent copulation or insemination between species. However, recent work suggests that differences in genital morphology might contribute to reproductive isolation in less obvious ways through interactions with sensory mechanisms that result in lowered reproductive fitness in heterospecific matings. In this paper, I present a brief history of the “lock-and-key” hypothesis, summarize the evidence for the involvement of genital morphology in different mechanisms of reproductive isolation, discuss progress in identifying the molecular and genetic bases of species differences in genital morphology, and discuss prospects for future work on the role of genitalia in speciation. L'armure copulatrice est un organe ou mieux un instrument ingénieusement compliqué, destiné à s'adapter aux parties sexuelles externes de la femelle pour l'accomplissement de l'acte copulatif; elle est la garantie de la conservation des types, la sauvegarde de la légitimité de l'espèce. [The copulation armor is an organ or better an instrument ingeniously complicated, destined to adapt to sexual parts external to the female for the completion of copulation; it is the guarantee of the preservation of the standards, the safeguard of the legitimacy of the species.] L. Dufour, 1844

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

“…First, crossings between species with different genital sizes are almost always impossible or lethal to females, especially when males are much larger (Masly 2012). Second, when size dimorphism is marked, selection can operate to match genital size.…”

“…They conclude that although there is no evidence that lock and key explains most instances of genital elaboration in insects, the hypothesis has not really been falsified. A more recent review centers on examining hybridization between species, in which genital morphology seems to play a role in reproductive isolation via mechanical incompatibility (Masly 2012). Lock and key is supported by recent studies of millipede genitalia (e.g., Tanabe and Sota 2008;Simmons 2012, 2013).…”

Correlated evolutionary changes in Drosophila female genitalia reduce the possible infection risk caused by male copulatory wounding

“…santomea is endemic to the small African volcanic island of São Tomé, while D. yakuba is widely distributed in central Africa (Lachaise et al 2000;Markow and O'Grady 2006). These two species form a hybrid zone in São Tomé (Lachaise et al 2000;Llopart et al 2005).…”

Systematic review of the firefly genus Scissicauda (Coleoptera, Lampyridae, Amydetinae) from Brazil

“…It was shown that in polyandric systems, female choice can promote male genitalic diversification (Arnqvist 1998), although the modus operandi is still disputed (Hosken and Stockley 2004). Furthermore, structures involved in mating are generally species-specific (which is the case in Scissicauda ) and evolve fast (Eberhard 2004), often as a consequence of sexual selection (Hosken and Stockley 2004), and may promote reproductive isolation either by structural or sensory lock-and-key, thus avoiding hybridization (Masly 2012). Future field observations and detailed histological studies would be useful to test these hypotheses.…”