BRIEF COMMUNICATION doi:10.1111/evo.12926 Why anisogamy drives ancestral sex roles Jussi Lehtonen, 1,2,3 Geoff A. Parker, 4 and Lukas Sch ¨ arer 2 1 Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia 2 Evolutionary Biology, Zoological Institute, University of Basel, Vesalgasse 1, CH-4051 Basel, Switzerland 3 E-mail: jussi.lehtonen@iki.fi 4 Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, United Kingdom Received January 18, 2016 Accepted April 1, 2016 There is a clear tendency in nature for males to compete more strongly for fertilizations than females, yet the ultimate reasons for this are still unclear. Many researchers—dating back to Darwin and Bateman—have argued that the difference is ultimately driven by the fact that males (by definition) produce smaller and more numerous gametes than females. However, this view has recently been challenged, and a formal validation of the link between anisogamy and sex roles has been lacking. Here, we develop mathematical models that validate the intuition of Darwin and Bateman, showing that there is a very simple and general reason why unequal gamete numbers result in unequal investment in sexually competitive traits. This asymmetry does not require multiple mating by either sex, and covers traits such as mate searching, where the male bias has been difficult to explain. Furthermore, our models show males and females are predicted to diverge more strongly when the fertilization probability of each female gamete is high. Sex roles thus ultimately trace back to anisogamy and the resulting consequences for the fertilization process. KEY WORDS: Anisogamy, female, isogamy, male, sex roles, sexual selection. Males and females often clearly differ beyond the definitional dimorphism in gamete size and number, and in particular, males tend to be more competitive over fertilization opportunities (e.g., Parker and Pizzari 2015). While the ultimate reasons behind this asymmetry are still being debated, anisogamy is widely held to be the ultimate driving factor (Bateman 1948; Parker et al. 1972; Trivers 1972; Sch¨ arer et al. 2012; Parker 2014; Parker and Pizzari 2015). This view has recently been challenged by some re- searchers (Gowaty and Hubbell 2005; Gowaty and Hubbell 2009; Ah-King 2013) who argue that sex roles instead arise by chance, or from sex differences in environment-driven “habits of life,” such as encounter rates, mortality schedules and remating rates. Differences in these life habits are assumed to be extrinsic, arising from an individual’s or species’ ecological setting, rather than be- ing an intrinsic consequence of anisogamy (reviewed in Sch¨ arer et al. 2012). Anisogamy itself has evolved independently several times; the selective forces that are thought to generate it have been extensively analyzed, and it seems unlikely that it has evolved by chance (see e.g., Parker et al. 1972; Lessells et al. 2009; Togashi and Cox 2011; Lehtonen and Parker 2014). Although it has been argued that explanations based on chance cannot explain why a given sex is more likely to ex- hibit a characteristic sex role (Sch¨ arer et al. 2012), to our knowl- edge, no mathematical models exist that explicitly explore why an asymmetry at the gamete level (anisogamy) should tend to generate a stereotypical asymmetry in the sex roles at the or- ganism level (“classical” sex roles). Here we confirm the in- tuition of Bateman (1948) by developing mathematical mod- els that—despite assuming no initial asymmetry between the sexes other than anisogamy—show how typical sex roles arise as a simple, general, and almost inevitable consequence of ga- mete dimorphism. In particular, we focus on sexually compet- itive traits, and show that such traits tend to be more strongly selected for in the sex producing the smaller gametes (i.e., the male sex, by definition) as a consequence of gamete dimor- phism. This asymmetry, based on simple principles of resource allocation does not require multiple mating, nor any preexist- ing asymmetry except a difference in gamete sizes. It applies to a wide range of traits, such as mate searching. Models are de- rived first for the simple scenario where all female gametes are 1129 C  2016 The Author(s). Evolution C  2016 The Society for the Study of Evolution. Evolution 70-5: 1129–1135