Animal Ecology Evolutionary Biology Centre Uppsala University An evolutionary perspective on sex in animals Ivain Martinossi-Allibert Introductory Research Essay No. 105 ISSN 1404 – 4919 Uppsala 2017 Introductory Research Essay No. 105 Postgraduate studies in Biology with specialization in Animal Ecology An evolutionary perspective on sex in animals Ivain Martinossi-Allibert Department of Ecology and Genetics / Animal Ecology Evolutionary Biology Centre Uppsala University Norbyvägen 18D SE-752 36 Uppsala Sweden ISSN 1404-4919 1 Introduction…………………………………………………………………….4 I. Biological sexes: Definition and evolution from isogamy………….4 Males and females……………………………………………………………………...4 The evolution of anisogamy and mating types…………………………………….…5 (i) Gamete competition models…………………………………………………………….…5 (ii) Gamete limitation models……………………………………………………………….…7 (iii) Intracellular conflict models…………………………………………………………….....8 (iv) Towards a synthesis using the “Fisher condition”……………………………………....…8 (v) Summary…………………………………………………………………………………...9 II. The study of mating systems from an evolutionary perspective……9 Sexual dimorphism and sexual selection………………………………………………9 What are sex roles?........................................................................................................10 (i) Emergence of the concept…………………………………………………………………10 (ii) Definition and use of the sex-role concept………………………………………………..11 (iii) What is sex-role reversal?....................................................................................................12 The measures of a mating system: Bateman Gradient, PI, PRR, OSR, I………….13 (i) Bateman gradient………………………………………………………………………….13 (ii) Trivers’ parental investment theory……………………………………………………….14 (iii) Operational sex-ratio and potential reproductive rate……………………………………..15 (iv) The opportunity for sexual selection………………………………………………………16 The evolution of parental care, variance in reproductive success and sexual competition traits from anisogamy………………………………………………….17 (i) Parental care………………………………………………………………………………17 (ii) Strength of selection/variance in reproductive success…………………………………...18 (iii) Competition and mate-searching traits……………………………………………………19 Summary………………………………………………………………………………20 References……………………………………………………………………..21 2 Introduction Sexual reproduction is predominant among eukaryotes (Kondrashov, 1988), and scientists have been particularly interested in their study. This interest likely stems from several sources. First, humans reproduce sexually and have a passion for understanding themselves. Second, a lot of species humans interact with are also sexually reproducing (such as those involved in animal breeding, crops, pests, pets etc.). Finally, evolutionary biologists see sexual selection as a powerful driver that generate great amounts of variation and may be involved in speciation processes. Evolutionary biologists have also realized that while sex is so pervasive among multicellular organisms, its occurrence throughout the tree of life represents a challenging enigma because its cost in terms of reproductive output seem to outweigh potential benefits. It is often observed in sexually reproducing species that males and females differ in their morphology and behavior. This raises the question of why there are two sexes and what is the cause of their differences. It also makes one wonder about the evolutionary consequence of such differences. In this essay, I will review the theoretical work describing the origin of the male and female sex, the evolution of anisogamy. I will then focus on the study of sex-specific patterns in mating strategies (i.e. are there consistent differences between the sexes and if so through which mechanisms) by exploring the diversity of mating systems. I. Biological sexes: Definition and evolution from isogamy Males and females Sexual reproduction does not necessarily imply the existence of males and females. Sexual reproduction can be achieved by a single individual (selfing) or by two individuals of any compatible mating types. Male and female describe two very specific mating types in an anisogamous system, i.e. mating types with distinct gametes. The female sex produces larger, fewer, and generally non-motile gametes, whereas the male sex produces smaller, numerous motile gametes (Schärer et al., 2012). This description is mostly applied to multicellular animals and plants, but mating types and anisogamy can also be found in multicellular fungi, as well as in unicellular organisms. In this text, I will focus on multicellular animals and the male and female mating types. It is not known whether it was mating types or anisogamy that evolved first, and multiple theories were developed starting from the 1970s until today (but see Kalmus 1932 for an earlier hypothesis of anisogamy evolution based on group selection). 3 The evolution of anisogamy and mating types In this part, I will present different frameworks that have attempted to describe mechanisms for the evolution of anisogamy and mating types: (i) gamete competition models, (ii) gamete limitation models, and (iii) intracellular conflict models. The radically different point of view between the two first frameworks simply stems from the study of different types of organisms. Gamete competition models relate more to a context of internal fertilization, in which sperm is never limiting because it is deposited directly in the female genital tract. At the opposite, gamete limitation models are based on external fertilizing species, such as marine animals releasing gametes in their environment, a context in which sperm limitation is frequent (i.e. in a given population, not all the eggs produced will be fertilized ) (Lehtonen & Kokko, 2011). Even of at first glance they seem irreconcilable, gamete competition and gamete limitation models may be described in a single framework, see (iv). (i) Gamete competition models The first model describing the evolution of anisogamy in a gene-centric view (as opposed to earlier work based on group selection) was published by Parker et al. in 1972. In this model, the evolution of anisogamy is driven by energetic constraints on gamete production and a trade- off between gamete size and number. Larger gametes have higher chances of survival but with limiting resources producing larger gametes limits the total number of gametes produced, therefore reducing the chances of gamete encounter and fertilization. In this model, reproductive success can be maximized by two opposite strategies, either by increasing gamete size or gamete number. In other words there is disruptive selection on gamete size: some individuals specialize into producing numerous small gametes (increasing the chances of fertilization), whereas others produce fewer large gametes (increasing survival chances of the zygote), resulting in anisogamy. The evolution of mating types would occur in this case after the evolution of anisogamy, as a consequence of it, because two small gametes cannot form a viable zygote (Parker, 1978). However this model does not account for the incompatibility between two larger gametes (Randerson & Hurst, 2001a). Maynard-Smith (Smith, 1982), later followed by Hoekstra (1987) and Bulmer (1994)suggested that the evolution of mating types, probably as a mechanism to avoid selfing, would be a necessary first step making the evolution of anisogamy possible. A more recent elaboration by Bulmer and Parker (2002) on the disruptive selection model this time based on pre-existing mating types, suggested that multicellularity may promote anisogamy. This is because multicellular organism require more energy for zygote survival, thereby imposing a heavier 4 constraint on one mating type to specialize into the production of fewer larger gametes (Bulmer & Parker 2002, Lehtonen and Kokko 2010). This hypothesis finds support in the observation that anisogamy is widespread in sexually reproducing multicellular organisms. An empirical relationship between the degree of complexity and anisogamy across several algal groups also support this view (Bell, 1982; Randerson & Hurst, 2001b). (ii) Gamete limitation models While the gamete limitation hypothesis, first formulated by Parker et al. (1972), relies on a trade-off between number of gametes and chances of survival, another body of theoretical work was built around the calculation of encounter rates between gametes. Schuster and Sigmund (1981) showed that in a Brownian motion model, i.e. random displacement of particles, the encounter rate would be maximized if the two mating types were of different sizes, both the number and the radius of gametes having an impact on the chances of a “hit”, i.e. encounter. Various theories based on encounter rate were then developed, relying on the pre-existence of mating types and differences in motility (anisomotility): Hoekstra et al. (1984a and b) suggested first that anisogamy could evolve in a population with pre-existing mating types of different motility, but this idea was highly criticized because it relied on the assumption that all gametes had the same thrust yet experienced a drag proportional to their size. Contradicting this last assumption, Dusenbery (2000) argued that the amount of energy allocated to movement should be proportional to size; this later model lead to the prediction of anisogamy with the smaller gamete being non-motile, a state that had never been observed empirically. Levitan (1998) suggested that anisogamy could have evolved in a sperm limitation context (i.e. there is not