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Species-Specific Genitalic Copulatory Courtship in Sepsid Flies (Diptera, Sepsidae, Microsepsis) and Theories of Genitalic Evolution

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Species-Specific Genitalic Copulatory Courtship in Sepsid Flies (Diptera, Sepsidae, Microsepsis) and Theories of Genitalic Evolution Evolution, 55(1), 2001, pp. 93±102 SPECIES-SPECIFIC GENITALIC COPULATORY COURTSHIP IN SEPSID FLIES (DIPTERA, SEPSIDAE, MICROSEPSIS) AND THEORIES OF GENITALIC EVOLUTION WILLIAM G. EBERHARD Smithsonian Tropical Research Institute and Escuela de BiologõÂa, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica E-mail: [email protected] Abstract. Males of Microsepsis eberhardi and M. armillata use their genitalic surstyli to rhythmically squeeze the female's abdomen with stereotyped movements during copulation. Squeezing movements did not begin until intro- mission had occurred and, contrary to predictions of the con¯ict-of-interest hypothesis for genitalic evolution, did not overcome morphological or behavioral female resistance. Contrary to predictions of the lock-and-key hypothesis, female morphology was uniform in the two species and could not mechanically exclude the genitalia of either species of male. The complex pattern of squeezing movements differed between the two species as predicted by the sexual selection hypothesis for genitalic evolution. Also, evolutionarily derived muscles and pseudoarticulations in the male's genitalic surstyli facilitated one type of movement, whose patterns were especially distinct. The data support the hypothesis that the male surstyli evolved to function as courtship devices. Key words. Copulatory courtship, cryptic female choice, genitalic evolution, sexual selection. Received December 22, 1999. Accepted July 27, 2000. Rapid and divergent evolution of male genitalia is one of naturally selected advantages, not because the female thereby the most widespread patterns of animal evolution (Eberhard obtains superior sons that will more effectively court the 1985). The three hypotheses most often mentioned to explain females in the next generation (and, if the female ancestors this pattern are species isolation by lock and key (e.g., Sha- of the male were especially selective, more selective daugh- piro and Porter 1989), male-female con¯ict over control of ters). For instance, if the female is able to avoid being obliged copulation (Lloyd 1979; Alexander et al. 1997), and sexual to copulate, she may gain by having more opportunity to selection by cryptic female choice (Eberhard 1985, 1996, forage or to oviposit or she may avoid increased risks of 1997; Arnqvist and Danielsson 1990). Observations of the predation. Similar naturally selected payoffs to the female behavior of male genitalia during copulation offer a chance are also presumed to be common in other more general mod- to discriminate among these hypotheses. els of male-female con¯ict such as chase-away selection The lock-and-key hypothesis, which has received little (Holland and Rice 1998). The advantages mentioned as likely convincing support despite a long history of attempts to test to result from female resistance include copulation at more it (summary in Shapiro and Porter 1989; also Arnqvist 1998), ideal times and places, less frequent copulation, higher sur- predicts morphological complementarity between males and vival, decreased predation, decreased energy costs, decreased females: the species-speci®c features of male and female gen- exposure to parasites, and decreased harassment by other italia should mesh or come into contact during copulation, males. Con¯ict ideas assume that these naturally selected and these features of the female should be capable of phys- advantages to the female outweigh any indirect bene®ts she ically excluding the male genitalia of closely related species would derive from the kinds of offspring superiority assumed but not those of her own species. The con¯ict-of-interest under sexual selection models (Alexander et al. 1997). hypothesis also predicts frequent morphological complemen- A second difference is that the con¯ict-of-interest hypoth- tarity in species-speci®c traits (Alexander et al. 1997) and esis predicts that species-speci®c male genitalic structures that the female will often have the morphological ability to will forcefully overcome species-speci®c morphological or exclude at least some males of her own species. The sexual behavioral female resistance: ``The clue to this interpretation selection hypothesis, in contrast, does not make strong pre- will often be evidence of forcing or manipulation by one sex, dictions about morphological ®t and is compatible with a usually the male,'' and ``the possibility must be considered lack of species-speci®c morphological complementarity. that variations in success of insemination result from force Discriminating between the con¯ict-of-interest and the or coercion rather than titillation'' (Alexander et al. 1997, sexual selection hypotheses can be confusing, in part because pp. 9, 20). In addition, such coercive behavior is predicted the names themselves are misleading. The hypothesis of sex- to occur at moments during male-female interactions when ual selection by cryptic female choice also involves a con¯ict the outcome of the male's attempt to copulate and fertilize of interest between male and female: the male's best interests the female's eggs is being determined. Except in cases in are favored by fertilizing all of the eggs of all of the females which the female is placed under physical duress by the male, he encounters; the female's best interests are favored by only relatively direct types of male genitalic manipulation of the allowing a biased subsample of males to fertilize her eggs. female are expected, such as forcing open her genital aperture The con¯ict-of-interest hypothesis, however, is an explicit to allow intromission. In contrast, the sexual selection hy- alternative to cryptic female choice (Alexander et al. 1997). pothesis does not presume that overt female genitalic resis- One important difference between the two hypotheses con- tance occurs and is compatible with male behavior that cannot cerns the payoffs to females. Female resistance under the forcefully overcome female resistance and is apparently only con¯ict-of-interest hypothesis is favored because she obtains stimulatory in nature. Indirect rather than direct manipula- 93 q 2001 The Society for the Study of Evolution. All rights reserved. 94 WILLIAM G. EBERHARD tions of the female are expected to be used by the male to mediately dropped into 80% ethyl alcohol at room temper- obtain favorable responses (e.g., stroke the female to induce ature. A previous study of Archisepsis spp. showed that the her to open her genital aperture and allow intromission). positions of male surstyli are not altered by this treatment Sepsid ¯ies offer an opportunity to make these crucial (Eberhard and Pereira 1996). This lack of effect was con- observations due to a combination of traits. As is common ®rmed directly in both species of this study, because there in insects, the male genitalia of sepsids are usually species- were no noticeable differences in the positions of the surstyli speci®c in form. One portion of the male's genitalia, the or their de¯ections of the female's abdominal sclerites when surstyli, are clasping organs that are especially useful in dis- living and preserved pairs were compared. The positions of tinguishing closely related species whose morphology is oth- the male's intromittent genitalia, which are tightly braced erwise relatively similar (e.g., Duda 1925, 1926; Hennig within the female (Eberhard and Huber 1998), were presumed 1949; Silva 1993; Ozerov 1992, 1993). The surstyli do not to also be unaffected by freezing. Whole mounts to be ex- enter the female, but rather grasp the surface of her abdomen amined with a compound microscope were dissected in 80% (Eberhard and Pereira 1996; Eberhard and Huber 1998; W. ethyl alcohol and transferred to euparol on microscope slides. G. Eberhard, unpubl. ms.). Thus, in contrast to the genitalia All orientations mentioned in descriptions of pairs (e.g., of many other animals, which are hidden inside the female anterior, posterior) refer to the perspective of the female. during copulation, the behavior of a male sepsid's genitalic Sample sizes for different aspects of behavior vary because surstyli can be observed directly. A previous study of sepsid of differences in female mobility that impeded observation, genitalic function, however, did not include behavior and was angles of viewing, and different attention to different details. based instead on pairs frozen during copulation. It showed Means are followed by one standard deviation, and times are that lock-and-key arguments failed to explain the species- given as minutes:seconds. Statistical tests employed Will- speci®c surstylus forms in two species of Archisepsis, because coxon ranks tests unless speci®ed otherwise. Names for gen- there was no female lock that could mechanically exclude italic structures follow McAlpine (1981) and Eberhard and males and because the site on the female abdomen that was Huber (1998). There is no comparative study of male sepsid grasped by the male's surstyli varied instraspeci®cally (Eber- intromittent genitalia that permits determination of homol- hard and Pereira 1996). Although there was also evidence ogies with those of other ¯ies. arguing against male-female con¯ict, the overall conclusion was that surstylus function was probably a combination of RESULTS physical restraint and stimulation. Male Morphology The present study, which describes the movements of the male surstyli just prior to and during copulation in Micro- As in other sepsids, the male genitalia of both Microsepsis sepsis eberhardi Ozerov and M. armillata (Melander and Spu- species consist of intromittent structures (including the ae- ler) suggests that this conclusion should be changed. Both deagus), which are introduced into the female's body during the movements themselves and the contexts in which they copulation, and clasperlike epandria, whose distal portions, occur support the idea that the male surtsyli function to stim- the surstyli, grasp the external surface of her abdomen. The ulate the female, as proposed by the sexual selection by cryp- male's intromittent genitalia differ only slightly from those tic female choice hypothesis, rather than to mesh with a spe- of Archisepsis (Eberhard and Huber 1998).
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