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Experimental Removal of Sexual Selection Reveals Adaptations to Polyandry in Both Sexes

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Experimental Removal of Sexual Selection Reveals Adaptations to Polyandry in Both Sexes Evol Biol (2014) 41:62–70 DOI 10.1007/s11692-013-9246-3 RESEARCH ARTICLE Experimental Removal of Sexual Selection Reveals Adaptations to Polyandry in Both Sexes Marco Demont • Vera M. Grazer • Łukasz Michalczyk • Anna L. Millard • Sonja H. Sbilordo • Brent C. Emerson • Matthew J. G. Gage • Oliver Y. Martin Received: 31 January 2013 / Accepted: 1 July 2013 / Published online: 12 July 2013 Ó Springer Science+Business Media New York 2013 Abstract Polyandrous mating is extremely common, yet polyandrous regime had more offspring in the experiments for many species the evolutionary significance is not fully with multiple males present than monogamous counterparts. resolved. In order to understand the evolution of mating However, in single male experiments, neither females nor systems, it is crucial that we investigate the adaptive conse- males differed between selection regimes. Subsequent mat- quences across many facets of reproduction. We performed ing trials with multiple males suggested that adaptations to experimental evolution with the naturally polygamous flour polyandry in both sexes provide benefits when choice and beetle Tribolium castaneum subjected to either polyandry or competition were allowed to take place. Polyandrous females enforced monogamy, creating contrasting selection regimes delayed the first copulation when given a choice of males and associated with the presence or absence of sexual selection. polyandrous males were quicker to achieve copulation when After 36 generations, we investigated male and female facing competition. In conclusion, we show that the expected adaptations by mating beetles with an unselected tester strain benefits of evolutionary adaptation to polyandry in T. casta- to exclude potential effects of male–female coevolution. neum depended on the availability of multiple mates. This Reproductive success of focal monogamous and polyandrous context-dependent effect, which concerned both sexes, beetles from each sex was assessed in separate single male highlights the importance of realistic competition and choice and multiple male experiments emulating the different experiments. selection backgrounds. Males and females from the Keywords Experimental evolution Á Mating system Á Monogamy Á Multiple mating Á Reproductive success Á Marco Demont and Vera M. Grazer have contributed equally to this Tribolium castaneum study. M. Demont Á V. M. Grazer Á S. H. Sbilordo Á O. Y. Martin (&) Experimental Ecology, Institute of Integrative Biology (IBZ), Introduction ETH Zu¨rich, Universita¨tsstrasse 16, CHN J 11, 8092 Zurich, Switzerland Across the animal kingdom, females commonly mate with e-mail: [email protected] more than one male although this is not strictly necessary Ł. Michalczyk to cover fertilization needs. Polyandrous mating is espe- Department of Entomology, Institute of Zoology, Jagiellonian cially puzzling given that mating is often associated with University, Gronostajowa 9, 30-387 Krako´w, Poland considerable costs, such as mechanical damage caused during copulation (Blanckenhorn et al. 2002) or harmful A. L. Millard Á B. C. Emerson Á M. J. G. Gage School of Biological Sciences, University of East Anglia, substances transferred with the ejaculate (Chapman et al. Norwich NR4 7TJ, UK 1995; Wigby and Chapman 2005). Although polyandry is widespread in nature, the underlying evolutionary causes B. C. Emerson often remain elusive and may differ for various species Island Ecology and Evolution Research Group (IPNA-CSIC), C/Astrofı´sico Francisco Sa´nchez 3, 38206 La Laguna, Tenerife, (Jenni 1974; Zeh and Zeh 1996; Zeh and Zeh 1997; Canary Islands, Spain Arnqvist and Nilsson 2000; Jennions and Petrie 2000; 123 Evol Biol (2014) 41:62–70 63 Arnqvist and Rowe 2005; Simmons 2005). Therefore, Another particularly clear means of achieving contrasting several evolutionary explanations for polyandry have been selection regimes is to apply monogamy versus polyandry. proposed to date. According to these, polyandry is vari- Under monogamy with random mate allocation, sexual ously driven by direct material (e.g. Vahed 1998; Hosken selection and conflict are essentially absent (Rice 2000), so, and Stockley 2003), or indirect genetic benefits (Jennions one can assess the presence of these selection pressures via and Petrie 2000; Simmons 2001; Zeh and Zeh 2001; Neff an intuitive yes–no dichotomy (e.g. Holland and Rice and Pitcher 2005; but see also Kotiaho and Puurtinen 1999; Hosken et al. 2001; Hosken and Ward 2001; Martin 2007), avoiding costs of not remating (Thornhill and and Hosken 2003a; Martin et al. 2004). Alcock 1983), or via non-adaptive routes (e.g. Halliday and Tribolium castaneum is naturally highly promiscuous, Arnold 1987). Furthermore, it has been suggested that and direct costs to females of mating multiply are rather female polyandry might provide a means to combat the low (reviewed in Fedina and Lewis 2008). Hence, this negative consequences of inbreeding (Tregenza and organism is highly suited to investigate potential adapta- Wedell 2002; Firman and Simmons 2008; Michalczyk tions to polyandry. Here we assess reproductive success of et al. 2011a) or mating with males bearing selfish genetic males and females from monogamous versus polyandrous elements (Zeh and Zeh 1996; Price et al. 2008). experimental evolution lines when subjected to single male Nevertheless, there are various obstacles to progress on versus multiple male scenarios to investigate how selection the way to fully understanding evolutionary causes and has shaped male and female traits. We focus on two main consequences of polyandry in many species. At the indi- questions: a) Are polyandrous line beetles generally fitter, vidual level, there is still a lack of knowledge concerning perhaps due to good genes effects of sexual selection, or meaningful natural levels of polyandry and resulting less fit, reflecting costs of sexual conflict? b) Are animals impacts on males and females. In recent studies, this gap from contrasting selection backgrounds better adapted to has partly been addressed via the use of molecular methods equivalent scenarios, i.e. are monogamous beetles fitter enabling quantification of natural mating rates and sperm when assessed as monogamous pairs, whilst polyandrous utilization (e.g. Bretman and Tregenza 2005; Simmons beetles are better when multiple males are present? In et al. 2007; Demont et al. 2011, 2012). At a larger scale, we addition, we assess male and female mating behaviours in also do not fully understand the adaptations in reproductive the presence of choice and competition, as well as lon- traits involved in male–female coevolution associated with gevity as a measure of general vigour. having multiple mates. Although polyandry enables sexual selection to occur (via mate choice and competition) it also provides fertile ground for sexual conflicts over all facets Methods of reproduction to germinate. The interests of the sexes are very frequently in opposition (Parker 1979; Arnqvist and Experimental Evolution Lines Rowe 2005), thus, polyandry can drive adaptations and counter-adaptations to evolve as each sex is selected to Tribolium castaneum is an eminent model system for studies gain an edge in this conflict (Chapman et al. 2003; Martin of pre- and postcopulatory sexual selection, characterized by and Hosken 2003a, b; Wigby and Chapman 2004). high mating and remating rates (reviewed in Fedina and Therefore, sexual selection and sexual conflict may drive Lewis 2008). As the source population for the experimental specific adaptations to the polyandrous mating system in evolution lines described below, we used the T. castaneum females, males or both sexes. wild type strain Georgia 1 (Ga1, initial collection 1980, Experimental evolution is a particularly powerful tool maintained in culture by the Beeman lab at USDA, Man- for the study of male–female co-evolution and responses to hattan, Kansas). Experimental evolution lines (initiated in sexual conflict, and has been put to good use in a number of 2005 at the University of East Anglia) and other experi- species and contexts (reviewed in Arnqvist and Rowe mental animals were kept on organic white flour supple- 2005; Edward et al. 2010). Across previous evolution mented with 10 % brewer’s yeast at 30 °C and ca. 65 % RH. experiments, contrasting sexual selection/conflict intensi- To achieve contrasting sexual selection intensities, we ties have been implemented in a variety of ways, such as established the following two regimes: monogamy (=sexual population size/density (e.g. Martin and Hosken 2003b, selection absent) and polyandry (=sexual selection present). 2004b; Gay et al. 2009; Hosken et al. 2009), or through Both treatments consisted of three replicate lines each, i.e. contrasting sex ratios (e.g. Wigby and Chapman 2004; M A/B/C and P A/B/C. Effective population sizes in each Crudgington et al. 2005). Experimental evolution using line and in both treatments were estimated as Ne = 40. This regimes with different population sex ratios has recently is comparable to the Ne = 36 used in related experimental been used in Tribolium castaneum to expose evidence for evolution lines using the same source population (see sexual conflict in this system (Michalczyk et al. 2011b). Michalczyk et al. 2011b; Hangartner et al., in press), as well 123 64 Evol Biol (2014) 41:62–70 as population sizes in similar experiments (see Snook et al. the interacting effects due to coevolved females. Therefore, 2009 for an overview). Each monogamy line was founded using the males from
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