Demonstrating sexual selection by cryptic female choice on male genitalia: What is enough?

Abstract

Rapid divergence in external genital structures occurs in nearly all animal groups that practice internal insemination; explaining this pattern is a major challenge in evolutionary biology. The hypothesis that species‐specific differences in male genitalia evolved under sexual selection as courtship devices to influence cryptic female choice (CFC) has been slow to be accepted. Doubts may stem from its radical departure from previous ideas, observational difficulties because crucial events occur hidden within the female's body, and alternative hypotheses involving biologically important phenomena such as speciation, sperm competition, and male‐female conflicts of interest. We assess the current status of the CFC hypothesis by reviewing data from two groups in which crucial predictions have been especially well‐tested, Glossina tsetse flies and Roeseliana (formerly Metrioptera) roeselii bushcrickets. Eighteen CFC predictions have been confirmed in Glossina and 19 in Roeseliana. We found data justifying rejection of alternative hypotheses, but none that contradicted CFC predictions. The number and extent of tests confirming predictions of the CFC hypothesis in these species is greater than that for other generally accepted hypotheses regarding the functions of nongenital structures. By this criterion, it is reasonable to conclude that some genital structures in both groups likely involved sexual selection by CFC.

Sexual selection on bushcricket genitalia operates in a mosaic pattern

“…Several competing hypotheses have been formulated. These include the lock-and-key hypothesis, which does not apply in most cases (Eberhard, 1985;Shapiro & Porter, 1989) and has only support in a very limited number of cases (Langerhans, Anderson, & Heinen-Kay, 2016;Simmons, 2014), sperm competition (Parker, 1970;Simmons, 2001), cryptic female choice (CFC) (Arnqvist, 2014;Eberhard, 1996Eberhard, , 2010aEberhard, , 2010bEberhard & Lehmann, 2019;Thornhill, 1983;Vahed, 2015), and sexually antagonistic coevolution (SAC) (Arnqvist & Rowe, 2005;Rice, 1996). The latter three hypotheses are not mutually exclusive, and the differences between them may be even less strict than they appear (Schilthuizen, 2003(Schilthuizen, , 2013.…”

“…To test for the different hypotheses of sexual selection acting on bushcricket titillators, we have developed specific predictions for the six copulatory and four postcopulatory traits ( Table 5). Many of the predictions can be deduced from our list supporting cryptic female choice in insect genitalia of tsetse flies and the bushcricket R. roeselii (Eberhard & Lehmann, 2019). Cryptic female choice and sexually antagonistic coevolution make distinct predictions for the outcomes in mating with genitalia-manipulated males.…”

“…Many—sometimes conflicting—theories have been proposed for the sexual selection forces driving the evolution of internal genitalia (Arnqvist, ; Arnqvist & Rowe, ; Briceño & Eberhard, ; Eberhard, , , , , ; Hosken & Stockley, ; Simmons, ). These range from sperm competition (Parker, ; Simmons, ; Waage, ), sexually antagonistic coevolution (Arnqvist & Rowe, ; Parker, ; Rice, ), to cryptic female choice (Eberhard, ; Eberhard & Lehmann, ; Thornhill, ). There is strong evidence for the evolution of insect genitalia under cryptic female choice at least in the broadly studied tsetse flies and a bushcricket species (Eberhard & Lehmann, ).…”

“…These range from sperm competition (Parker, ; Simmons, ; Waage, ), sexually antagonistic coevolution (Arnqvist & Rowe, ; Parker, ; Rice, ), to cryptic female choice (Eberhard, ; Eberhard & Lehmann, ; Thornhill, ). There is strong evidence for the evolution of insect genitalia under cryptic female choice at least in the broadly studied tsetse flies and a bushcricket species (Eberhard & Lehmann, ). However, we also see prime examples of insect genitalia fulfilling the criteria for sexually antagonistic coevolution, especially water striders and beetles of the genus Callosobruchus (summarized in Simmons, ).…”

“…, sexually antagonistic coevolution (Arnqvist & Rowe, 2002;Parker, 1979;Rice, 1996), to cryptic female choice (Eberhard, 1996;Eberhard & Lehmann, 2019;Thornhill, 1983). There is strong evidence for the evolution of insect genitalia under cryptic female choice at least in the broadly studied tsetse flies and a bushcricket species (Eberhard & Lehmann, 2019).…”