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Experimental Removal of Sexual Selection Reverses Intersexual Antagonistic Coevolution and Removes a Reproductive Load

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Experimental Removal of Sexual Selection Reverses Intersexual Antagonistic Coevolution and Removes a Reproductive Load Proc. Natl. Acad. Sci. USA Vol. 96, pp. 5083–5088, April 1999 Evolution Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load BRETT HOLLAND* AND WILLIAM R. RICE Department of Biological Sciences, University of California, Santa Cruz, CA 95064 Communicated by Sarah Blaffer Hrdy, University of California, Davis, CA, February 8, 1999 (received for review December 14, 1998) ABSTRACT Although sexual selection can provide bene- We replaced the naturally promiscuous mating system of D. fits to both sexes, it also can be costly because of expanded melanogaster with enforced monogamy and random mate opportunities for intersexual conflict. We evaluated the role of assignment in replicate populations. This treatment removes sexual selection in a naturally promiscuous species, Drosophila the opportunity for both intersexual and intrasexual selection. melanogaster. In two replicate populations, sexual selection Therefore, we expected that natural selection would favor was removed through enforced monogamous mating with those individuals who are less harmful to their mate, indicating random mate assignment or retained in promiscuous con- the variety and strength of conflicts that remained in the trols. Monogamous mating constrains the reproductive suc- promiscuous control populations. cess of mates to be identical, thereby converting prior conflicts The treatment and control populations were given the between mates into opportunities for mutualism. Random opportunity to diverge for 32 generations before we began a mate assignment removes the opportunity for females to series of assays. We measured the level of male-induced harm choose beneficial qualities in their mate. The mating treat- to females, as well as changes in specific male traits that were ments were maintained for 47 generations, and evolution was expected a priori to have contributed to a reduction of allowed to proceed naturally within the parameters of the male-induced harm. If males evolve to become benign toward design. In the monogamous populations, males evolved to be females, female defense against such harm becomes obsolete less harmful to their mates, and females evolved to be less and will be selected against if it interferes with other compo- resistant to male-induced harm. The monogamous popula- nents of female fitness. Therefore, we also assayed the level of tions also evolved a greater net reproductive rate than their female resistance to male-induced harm. Finally, we assessed promiscuous controls. These results indicate a potentially the net reproductive rate of the populations under both mating widespread cost of sexual selection caused by conflicts inher- environments. This measure evaluates the extent to which the ent to promiscuity. removal of sexual selection has affected the ability of the populations to propagate themselves. A large body of theoretical and empirical evidence indicates that sexual selection can provide a variety of benefits to MATERIALS AND METHODS females (reviewed in refs. 1 and 2). Laboratory populations of Drosophila melanogaster have proven to be a valuable model Experimental Protocol. The ancestral population of D. system for measuring such benefits, e.g., improved survival melanogaster was established in 1988 from 400 mated females (3–5). However, sexual selection is also demographically collected by L. Harshman (University of Nebraska, Lincoln, costly, reducing male viability through encumbering traits (6, NE) in central California. Subsequently, this population has 7). The costs of sexual selection that apply to females and those been maintained under the following conditions: effective that arise from intersexual conflict have not been studied as population size of .5,000; 25°C; cornmealymolassesykilled- thoroughly as the benefits. Theory and experiments indicate yeast medium; 12-h light:12-h dark diurnal cycle; and 14-day that some sexually selected traits increase male fitness at the generation cycle. Our experimental protocol maintains these expense of females (7–31). D. melanogaster has proven to be a conditions except as noted otherwise below. valuable model here as well: (i) females experiencing experi- To begin the experiment, 220 females and 220 males were mentally reduced courtship (19) or mating rates (18) survive sampled from the ancestral population. The sample was di- longer than controls but reproduce at the same rate; (ii) vided equally into replicates (A and B) and cultured. On the seminal-fluid components increase the competitive ability of ninth day after egg laying, virgin progeny were collected from accompanying sperm (32, 33) but also increase the mortality each replicate culture. Half of the offspring were assigned to rate of inseminated females (27); and (iii) net male fitness a monogamy treatment (114 females, each housed individually increases at the expense of female survival when females are with one randomly assigned male), and the other half were artificially prevented from coevolving with males (30). assigned to a control treatment (three males per female; Conflict between mates hinges on sexual infidelity. Under otherwise identical to the monogamy treatment). The differ- strict, life-long monogamy, any trait that lowers the reproduc- ence in sex ratio between treatments is a natural aspect of tive success of one’s mate lowers one’s own reproductive sexual selection in this species: ‘‘Mating takes place at the success equally. Alternatively, whenever an individual has feeding site, where arriving females are greeted by the court- multiple mates, the lifetime reproductive success of that indi- ship of an average of five wild-type males’’ (34). vidual will differ from the success of its mates. Thus, promis- The assignment to the treatments described above was cuity necessarily introduces the opportunity for sexual conflict performed on day 1 of a 14-day propagation cycle. All flies through the evolution of novel traits that increase the repro- were collected2haftereclosion by using CO2 anesthesia for ductive success of members of one sex at a cost to members of 3–4 min. Then the sexes were combined according to treat- the opposite sex. ment type and housed for 5 days in ‘‘interaction vials’’ (100 mm 3 13 mm) containing 3 ml of medium. The flies matured The publication costs of this article were defrayed in part by page charge and mated in the interaction vials but no progeny were payment. This article must therefore be hereby marked ‘‘advertisement’’ in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. e-mail: holland@ PNAS is available online at www.pnas.org. darwin.ucsc.edu. 5083 5084 Evolution: Holland and Rice Proc. Natl. Acad. Sci. USA 96 (1999) retained. On day 6, all flies were transferred without anesthe- nents, virgin test females were allowed to mate once with sia to fresh ‘‘culture vials’’ (identical to interaction vials but experimental males. The males were then removed, and the seeded with live yeast), where eggs were laid overnight to survival and fecundity of the test females was measured. This propagate the next generation. On day 7, the adults from each assay was identical to the assay described in Net reproductive of the four newly founded populations were discarded, and rate of adult test females, except that 100 min after being their progeny were allowed to develop until the end of the 14 combined with the test females, the experimental males were day cycle. On day 1 of the following cycle, the day of maximum removed by using CO2 anesthesia for 45 s. The 50% mortality adult emergence, progeny eclosing within an 8-h period were point was reached 22 days after mating. Copulation frequency collected and pooled without anesthesia from 100 productive was measured during the exposure period; 20 min after culture vials per population;2haftercollection, virgin males combining the sexes, most of the females were simultaneously and females from each population were anesthetized with CO2 in copula, and the frequencies between treatment were virtu- and randomly parceled into individual interaction vials, as ally identical: monogamy, 0.81 6 0.025; control, 0.83 6 0.042. described above, to begin the next generation. In subsequent After the initial pulse of mating, the copulation frequency generations, the above protocol was reiterated. The number of decreased rapidly to 0 (by 70 min). No copulation occurred productive culture vials used to propagate subsequent gener- during the final 30 min. The above pattern indicates that after ations varied (n 5 100–114), but in every generation an mating once, the females remained refractory for the duration identical number was used from each population. No manip- of male exposure, consistent with previous studies (35) and our ulation of family size or other aspect of artificial selection was unpublished observations of the ancestral population. Per used. Initially, the treatments showed no evidence of produc- capita female fecundity was measured (as described in Net ing different offspring densities: monogamy, 19.4 6 3.6; con- reproductive rate of adult test females) during the first 2 days trol, 17.2 6 2.6; P 5 0.5; Student’s t test, n 5 4, df 5 2; densities after insemination. This assay encompasses the period when were estimated in the third generation by the number of eggs seminal fluid is known to influence this trait and when sperm per vial; 20 vials per population. Compared with the ancestral stores remain unexhausted (36). Per capita fecundity was population, our protocol caused both treatments to have a calculated as the total egg mass produced divided by the sum lower density of adults and larvae. of the number of females surviving over day 1 and day 2 of the Male Effect Assays. Overview. After 34 generations of assay. enforced monogamy, two assays were performed to look for Courtship Rate. Adults used in this assay were sampled from differences in the harm induced by males on their mates. One the pool of virgin adults produced on day 1 in generation 45.
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