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The Evolution of Multiple Mating Costs and Benefits of Polyandry to Females and of Polygyny to Males

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The Evolution of Multiple Mating Costs and Benefits of Polyandry to Females and of Polygyny to Males EXTRA VIEW Fly 6:1, 3–11; January/February/March 2012; G 2012 Landes Bioscience The evolution of multiple mating Costs and benefits of polyandry to females and of polygyny to males Patricia Adair Gowaty Department of Ecology and Evolutionary Biology; Institute of Environment and Sustainability; UCLA; Los Angeles, CA USA; Smithsonian Tropical Research Institute; Washington, DC USA; Polistes Foundation, Inc.; Belmont, MA USA View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by PubMed Central olyandry is a paradox: why do opportunities and constraints mold P females mate multiple times when evolutionary responses. a single ejaculate often provides enough sperm for lifetime egg production? Gowaty et al. addressed explanations for Multiple Mating in Drosophila polyandry in Drosophila pseudoobscura from the perspective of hypotheses based “Multiple mating” is mating with more © 2012 Landeson sex differences in costs of reproduction Bioscience.than one potential mate, which potentially (CoR). Contrary to CoR, Gowaty et al. produces offspring of mixed parentage. showed that (1) a single ejaculate was Multiple mating is called “polyandry” inadequate for lifetime egg production; when females do it and “polygyny” when (2) polyandry provided fitness benefits to males do it. In the vast majority of tested females beyond provision of adequate species, females mated in nature produce Do notsperm and (3)distribute. fitness benefits of poly- offspring sired by more than one male. andry were not offset by costs. Here, I Polyandry is common in wild Droso- discuss predictions of the ad hoc hypo- phila,1-17 but also in crickets,18 burying theses of CoR and three alternative beetles19 and other insects,20 as well as hypotheses to CoR to facilitate a discus- birds21 and mammals.22,23 Compared with sion and further development of a strong birds, in which studies of hundreds of inference approach to experiments on the species in the wild demonstrate the adaptive significance of polyandry for ecological correlates of genetic polyandry, females. Each of the hypotheses makes generalities about Drosophila polyandry Keywords: multiple insemination, cost of testable predictions; simultaneous tests of come mostly from laboratory studies, and reproduction, compensation hypothesis, the predictions will provide a strong most generalities about Drosophila poly- mating theory, switch point theorem, inference approach to understanding the andry come from only two species, sexual conflict adaptive significance of multiple mating. D. melanogaster and D. pseudoobscura, I describe a sex-symmetric experiment though this is changing as more behavioral Submitted: 09/01/11 meant to evaluate variation in fitness and evolutionary ecologists24 ask questions Revised: 10/05/11 among lifelong virgins (V); monogamous about non-model Drosophila and Accepted: 10/05/11 females and males with one copulation Drosophila species in nature. Despite (MOC); monogamous females and males enormous success in understanding the http://dx.doi.org/10.4161/fly.18330 with multiple copulations (MMC); PAND, ecology of polyandry in birds and its costs Correspondence to: Patricia Adair Gowaty; polyandrous females; and PGYN, polygyn- and benefits to wild-living females, much Email: [email protected] ous males. Last, I recommend the study less is known about proximate causation in of many different species, while taking birds than in Drosophila. Almost all we Extra View to: Gowaty PA, Kim YK, Rawlings J, ’ Anderson WW. Polyandry increases offspring care in choice of study species and now know of polyandry s proximate causes viability and mother productivity but does not attention to the assumptions of specific has come from Drosophila. A better decrease mother survival in Drosophila hypotheses. I particularly urge the study understanding of the ultimate causes pseudoobscura. Proc Natl Acad Sci USA 2010; of many more Drosophila species both in of polyandry in a variety of species of 107:13771–6; PMID:20643932; http://dx.doi.org/ laboratory and the wild to understand Drosophila, along with more studies of 10.1073/pnas.1006174107 the “nature of flies in nature,” where Drosophila in the wild, will close the www.landesbioscience.com Fly 3 intertwining linkages of proximate and the laboratory, male Drosophila multiple In this paper, I describe conceptual and ultimate causation in the paradoxes of mating is much easier to observe, espe- theoretical ideas (Table 1) that together polyandry—at least for Drosophila—and cially under experimental mating schemes allow a strong inference33 approach to provide additional direction for studies of with sequential presentations of females current investigations of the costs and polyandry in other taxa. to subject males; and, in the laboratory, benefits to polyandry in species from any In laboratory studies of multiple male multiple mating is common.13 taxa, concentrating on the implications in Drosophila species, females often readily Observations in some species suggest studies of Drosophila. The ideas that I mate with more than one male.15,17,25 that female re-mating rate may be higher consider here have implications for future Investigators often present experimental than male re-mating rate,28 which may investigations of the fitness consequences males to females sequentially rather than be associated with sex differences in for both females and males of multiple simultaneously, and this methodology has development time, in turn affecting the mating, i.e., of genetic polyandry and led to categorization of species as those operational sex ratio at eclosion sites genetic polygyny. I also suggest an experi- with females re-mating at relatively fast where females often commence mating.17 ment for the future (Table 2), from the vs. slow rates.17 There are very few fly Even Bateman’s29 classic laboratory experi- perspective of a balanced approach34 to the species in which most females mate just ment with D. melanogaster suggested on constraints and opportunities for males31,35 once.17,26,27 In contrast, no studies of reflection30,31 and later re-analysis32 that and females of multiple mating. Drosophila from nature have demon- most females re-mated more than once, strated that specific males have sired sometimes as often as most males in the Polyandry Hypotheses offspring with more than one female, experimental trials. Thus, the widespread which might be explained by the metho- general expectation derived mostly from Hypotheses 1–5: Cost of reproduction. dological difficulty of assigning rather than laboratory studies of D. melanogaster Anisogamy36 and parental investment37 rejecting paternity (assigning paternity is a that male Drosophila always re-mate theories are evolutionary explanations for ©problem not2012 unique to Drosophila, butLandesmore often than females re-mate Bioscience. remains fixed sex differences in pre-copulatory and also in studies of other wild animals). In speculation. copulatory mating behavior and physi- Table 1. Comparison of fitness predictions for scenarios from cost of mating, compensation, demographic stochastic mating theory and the switch point theorem Component of Fitness PolyandryDo notNumber of distribute.Egg to adult Number adult Mother Adult offspring hypotheses fertile eggs survival† offspring survival* survival† MOC MMC PM MOC MMC PM MOC MMC PM MOC MMC PM MOC MMC PM 1 1 CoR: Guards against “sperm limitation” MOC , MMC =PM No prediction No prediction No prediction No prediction 1,2 2 CoR: Decreases gamete incompatibilities MOC =MMC , PM No prediction No prediction No prediction No prediction 1 3 CoR: Enhances offspring health MOC =MMC , PM MOC =MMC , PM MOC =MMC , PM No prediction MOC =MMC , PM 1 4 CoR: Enhances direct benefits to females No prediction No prediction No prediction MOC # MMC # PM No prediction 1,2 5 CoR: Male coercion of remating by MOC =MMC =PM MOC =MMC =PM MOC =MMC =PM MO $ MMC $ PM MOC =MMC =PM females 3 6 Compensation MOC =MMC , PM MOC =MMC , PM MOC =MMC , PM MO $ MMC $ PM MOC =MMC , PM 4 7 Demographic stochastic mating theory MOC # MMC , PM No prediction ## No prediction No prediction 5 8 Switch Point Theorem MOC =MMC , PM MOC =MMC , PM MOC =MMC , PM MOC =MMC =PM MOC =MMC , PM Hypotheses for polyandry predict differences in components of fitness and the direction of effect comparing experimental treatments. The experimental treatments are (1) females with access to one randomly assigned male during only one day of their lives, i.e., monogamous females with one copulation MOC; (2) females with continuous access to a single randomly assigned male; i.e., monogamous females with multiple copulations MMC and (3) polyandrous females with access to a different randomly-assigned male (controlling for age and experience of males in MMC) on each day of the experiment; i.e., polyandrous females with multiple copulations, PMC. Read the entries thusly: MOC = MMC = PMC and so forth. *Mother survival is always expected to be lower for mothers with greater contact with conspecifics as required when females mate with more than one male, because of higher risk to pathogens and parasites, unless pathogen risk is offset by greater access to resources or other factors. †Offspring survival/per cohort is almost always expected to be higher under hetorozygosity, particularly at immune coding loci, which in many ecological circumstances will be higher when mothers have broods sired by more than one male. 1Assumes the cost of reproduction CoR organizes sex differences, and for species in which
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