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Home , Anisogamy, Isogamy, Sexual reproduction

Ecology Evolutionary Centre Uppsala University

An evolutionary perspective on in

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 / Animal Ecology Centre Uppsala University Norbyvägen 18D SE-752 36 Uppsala Sweden

ISSN 1404-4919

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Introduction…………………………………………………………………….4

I. Biological : Definition and from ………….4

Males and ……………………………………………………………………...4

The evolution of and types…………………………………….…5

(i) 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 ………………………………………………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 : 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 , variance in 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

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Introduction

Sexual is predominant among (Kondrashov, 1988), and scientists have been particularly interested in their study. This interest likely stems from several sources. First, reproduce sexually and have a passion for understanding themselves. Second, a lot of 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 processes. Evolutionary biologists have also realized that while sex is so pervasive among multicellular , its occurrence throughout the tree of 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 . 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 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. can be achieved by a single individual () 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 . 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 , 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).

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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 , in which 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 , 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 -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 ), 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 require more energy for zygote survival, thereby imposing a heavier 4 constraint on one 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 (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 enough sperm to encounter and fertilize all the eggs), which is common in external fertilizers such as non-motile marine organisms. In this context, he showed empirically (Levitan, 1993, 1996) that not only do larger gametes favor survival, but also favor chances of fertilization. Anisogamy may very well have been driven by disruptive selection on gamete size for increased chances of fertilization in both sexes. This hypothesis contrasts with the gamete competition framework described above, in which selection for small male gametes is driven by fertilization success, but selection for larger gametes in females is driven by increased survival chances only.

A major drawback of the previously cited theories is the empirical evidence for isogamous species exhibiting anisomotility (Randerson and Hurst 2001a), which indicates that a situation with mating types and anisomotility does not necessary lead to anisogamy as predicted in this framework. 5

(iii) Intracellular conflict models Cosmides and Tooby (1981) were the first to suggest a model for the evolution of anisogamy based on intracellular conflict. Intracellular genomic conflict may occur because different subsets of the genome within a , such as nuclear and cytoplasmic genes, can maximize their somewhat independently. For example, in eukaryotes the nuclear genome and the mitochondrial genome have different patterns of inheritance and therefore experience different selection pressures, setting the stage for intracellular conflict (Cosmides and Tooby 1981).

During gamete fusion in contemporary isogamous species, a conflict between the cytoplasmic genetic materials of the two cells usually results in the destruction of the less abundant one. Consequently, there should be a selection pressure on cytoplasmic genes to increase gamete size, resulting in the apparition of “proto-eggs” (relatively larger gametes). Alternatively, a selection pressure on the nuclear genome to maximize fertilization success could result in the production of smaller but more numerous gametes able to fertilize many “proto-eggs” but at the loss of their cytoplasm. The different selection pressures experienced by cytoplasmic and nuclear genes may have led to anisogamy according to this scenario (Cosmides and Tooby 1981).

(iv) Towards a synthesis using the “Fisher condition” Queller (1997) emphasized that a large number of theoretical models of sex roles and parental care do not take into account what is called the “Fisher condition” (Houston & McNamara, 2006): the straightforward fact that in a group of reproducing individuals, males and females share the same total reproductive success. By applying this condition to the gamete competition models Lehtonen and Kokko (2010) confirmed that organismal complexity does favor anisogamy as suggested by Bulmer & Parker (2002). They also showed that gamete competition models will lead to anisogamy only if the density of reproducing individuals is high (i.e. gamete competition is intense). In turn, they further showed that from the same starting conditions, gamete limitation can lead to anisogamy too: when the encounter rate of gametes is lowered (in a low density population) or when the energy allocated to gamete production is low. In this latter case, maximum number of surviving is achieved by one sex specializing in provisioning (maximizing survival) and the other specializing in the number of gametes (maximizing encounter rates).

(v) Summary It seems that gamete competition and gamete limitation models of the evolution of anisogamy are not irreconcilable and may present two extremes of the same continuum in different types 6 of or environments. Whether it originates from gamete competition or gamete limitation, sexually reproducing multicellular organisms are almost exclusively of anisogamous type, allowing the definition of a male and a female sex. The fact that males and females produce different gametes, and therefore invest differently in reproduction, has the power to shape the way the two sexes experience selection, the way they interact and coevolve. In the next part I will try to give a historical perspective on the study of mating systems, as well as a summary of the current view on the ultimate causes of sex-specific patterns of behavior and morphology, and how it relates to anisogamy.

II. The study of mating systems from an evolutionary perspective

Sexual dimorphism and sexual selection.

In multicellular animals, males and females usually differ by more than just the type of gametes they produce. Their reproductive organs differ, as well as an array of what is called secondary sexual characters, including morphological, life-history and behavioral traits; this differentiation is called sexual dimorphism (Andersson, 1994). Darwin (1871) also observed that this multidimensional sexual dimorphism presented some recurrent patterns. When studying for example, he could see that plumage elaboration in males was linked with courtship behavior. From those observations, Darwin built the concept of (pre-ejaculatory) sexual selection, a type of selection favoring individuals better able to ensure mating. This was an important part of Darwin’s theory, as it had the power to explain a great amount of diversity observed in sexually reproducing species (Andersson 1994).

Darwin described competitive and showy males and choosy females, but also noted the occurrence of showy females and choosy males, later classified as reversed sex-roles (Ah-King & Ahnesjö, 2013). This conception, implemented in the early developments of evolutionary biology, led to the following question: does sexual dimorphism and sex roles tend to follow a general pattern, and if yes, is it a direct consequence of anisogamy?

What are sex roles?

(i) Emergence of the concept In 1966, George Williams (Williams, 1966) introduced the concept of sex syndromes, arrays of morphological and behavioral traits that are specific to a sex and supposedly result directly from anisogamy (described in Barlow 2005): given that males produce numerous cheap gametes,

7 they are selected to compete. The male sex therefore exhibits aggressive behavior, a large body size and elaborate courtship displays. In turn, as females produce few but costly eggs, they are selected for increased choosiness and minimizing costly activities related to sexual competition.

Trivers (Trivers 1972) later described those groups of sex-specific traits as sex roles (as they include numerous behavioral traits) and proposed that they were initially caused by sex differences in parental investment (energy expenditure) into . According to Trivers, reproductive rate is limited by the sex that invests most energy per offspring. This situation automatically triggers competition in the other sex for access to mating, resulting in the observed sexual dimorphism (this will be discussed in more details later).

Even if the Darwinian sex roles presented as a general rule has been repeatedly challenged since the late 1970s (Ralls, 1976; Gowaty, 1981; Hrdy, 1986), the concept of sex roles is still widely used today (see Janicke et al. 2016 for a recent example), but under debate.

(ii) Definition and use of the sex-role concept In a relatively recent paper, Schärer et al. (2012) described sex roles as usually defined by “(i) the degree of within sex reproductive competition, (ii) how discriminant individuals are during pair formation and (iii) the extent to which they exhibit parental care after mating. A “typical” male sex role would be defined by high within sex reproductive competition for access to mating, low discrimination during pair formation, and low parental care after mating, whereas a “typical” female sex role would correspond to low within sex competition, high discrimination during pair formation and high level of parental care after mating (Schärer et al. 2012).

The notion of “typical” or “classical” as opposed to “reversed” sex role implies the existence of a general pattern of sex-specific in competition and parental care, as well as in sex- specific morphologies. Such a pattern is appealing to evolutionary biologists because it bears a tremendous explanatory power; more than just summarizing a vast number of sexually reproducing species into one concept, it also represents a strategic anchoring point in theorizing the evolutionary history of sex. Indeed, a general pattern of sex-roles could be both (i) the result of a common evolutionary history (if anisogamy drives the evolution of sex-roles) and (ii) the source of further common evolutionary change (in conventional sex role species, males experience stronger selection than females). However, I will in the next paragraph present that the sex-role concept can also be misleading. Additionally, in the last section we will review current theoretical evidence for the evolution of sex-roles from anisogamy.

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(iii) What is sex-role reversal? It is easy to picture how the sex role concept can become misleading by looking at multiple examples of “sex-role reversal”. Are sex roles reversed when females are competing? In anemonefish the mating system is described as “sex-role reversed” because the largest dominant individual in a group is a female, but the mating system is a polyandrous one in which males compete (Barlow 2005). In the black coucal, females are aggressive and territorial and can potentially reproduce faster, yet males compete for and guard females. Males also provide care for the egg and young. In harem species, females may compete and be territorial, inside the harem of a male that competes with other males. Some readers may find it surprising that the examples given above would be described as “sex-role reversed”, but they were indeed and references to other similar examples can be found in Barlow (2005) and Ah-King and Ahnesjö (2013).

From the previous paragraph we can see that the sex-role concept is context-dependent. For example, an evolutionary biologist working on passerine birds may imply female courtship when referring to sex-role reversal, whereas another one would mean male biased parental care. Moreover, a scientist working only with species could imply female biased parental care when mentioning sex-role reversal!

Adding to this issue, the sex-role concept may also easily be related to gender stereotypes in society; as facts about have commonly been used to fuel sociological debates at the scholar or popular levels (Haraway, 1989; Ah-King, 2009) all confusion with sexual selection research should preferably be avoided.

In the next section, I will move forward from the mostly semantic sex-role argument, to a description of the metrics that are practically used to describe a mating system: Bateman gradient, parental investment (PI), potential reproductive rate (PRR), operational sex ratio (OSR) and intensity of sexual selection (I).

The measures of a mating system: Bateman Gradient, PI, PRR, OSR, I.

The measures used to quantify mating systems are quite different from one another. They describe different aspects of reproduction, sometimes at the individual level, sometimes at the population level, but they all share the same purpose: to describe the mating system (i.e. male-

9 female interactions related to reproduction) and account for observed difference between the sexes.

(i) Bateman gradient Bateman’s now renowned experiment with Drosophila melanogaster (1948) showed that the reproductive success of males increased more steeply with the number of matings than the reproductive success of females. From this observation, a first measure of a mating system was developed: The Bateman gradient (BG). This measure is the slope of the regression of reproductive success on the number of matings. This gradient can be calculated for each sex in a population; if the BG is positive, it indicates that increasing the number of matings will increase reproductive success, whereas a null or negative gradient shows that multiple matings are not beneficial or even harmful. Bateman also noted that the reproductive success among males was more variable than among females, with notably more males having a null reproductive success, and the highest reproductive success of a male being five times higher than the one of the most successful female (focal individuals were given five mates in this experiment). The variance in reproductive success is another measure that is important to the study of mating systems. Bateman’s explanation for the observed pattern was that males didn’t invest much energy in gamete production, and that therefore mating multiply was not as costly for this sex as it was for females (Jones, 2009). Bateman concluded that this principle should be applicable to all non-monogamous sexual species. The results of this experiment and subsequent generalization have been criticized (Sutherland, 1985; Tang-Martinez & Ryder, 2005; Gowaty et al., 2012), but the BG nevertheless remains a meaningful measure to evaluate male and female mating strategies.

(ii) Trivers’ parental investment theory In 1972, following Fisher’s (1958) ideas on sex ratio and “parental expenditure”, Trivers added a layer of complexity to Bateman’s scenario, stating that parental investment should be taken into account when measuring the costs and benefits of mating (whereas Bateman was only concerned with the energy spent on gamete production). Trivers (1972) defined parental investment as: “any investment by the parent in an individual offspring that increases the offspring’s chances of surviving at the cost of the parent’s ability to invest in other offspring”. We can see that this definition therefore also includes the initial energy investment in gamete production that was considered by Bateman as a main cause of sex-specific selection. Assuming an equal sex ratio, Trivers showed that the sex with the largest parental investment should automatically become limiting for reproduction, as males and females from the same population

10 share their reproductive success. This situation will in turn result in competition within the sex with the lowest level of parental investment. Trivers also used it as an argument to show that anisogamy should directly cause the evolution of sex roles: because the initial investment (the gamete energy expenditure) in one particular offspring is always higher in females, this will result in a female biased investment cascade. As the female already has spent more energy on producing gametes, an offspring’s will be more costly to the female, therefore the female should experience stronger selection on providing further parental care.

This idea relates strongly to Bateman’s in the sense that it provides a straightforward path from anisogamy to conventional sex-roles. However, as first pointed out by Dawkins ad Carlisle (1976), and later by Kokko and Jennions (2008), this self-reinforcing argument of female investment violates the “Concorde fallacy” because it assumes that the female strategy is based on past investment and not on future benefits. It also assumes that the production of one offspring strictly requires one egg and one sperm cell (rendering the male’s investment lower). However, if a high number of sperm cells are required to fertilize one egg (many will die without having a chance to), the energy expenditure of the male to produce one offspring may be equal or higher than the one of the female. In conclusion it seems like sexual dimorphism may not be explained solely as a consequence of an initially female biased investment due to anisogamy.

(iii) Operational sex-ratio and potential reproductive rate Starting from empirical observations that relative parental investment failed to directly explain sex roles as it had been proposed by Trivers (1972), especially in terms of within-sex competition, Clutton-Brock and Parker (1992) suggested an explanation. The potential reproductive rate (PRR) measures the time necessary for a given individual to produce offspring and go back to the mating pool, under the condition that mate availability is not limiting (hence the “Potential” in PRR). If one sex has a consistently lower PRR than the other, it will require more time to return to the mating pool after breeding and therefore the sex-ratio of the mating pool, also called operational sex-ratio (OSR, Emlen and Oring 1977), will become biased in favor of the sex with the highest PRR. As a consequence, the most common sex in the mating pool (the one with highest PRR) will compete more for access to matings and therefore experience stronger sexual selection (but see Kokko and Rankin 2006). This theory is not completely disconnected from Trivers’, as parental investment will strongly influence the PRR (higher energy expenditure per offspring generally implies a lower rate of offspring production, regardless of the mechanism involved (Clutton-Brock, 1991).

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What this particular metric made clear, and which Trivers’ ideas did not, is that it becomes very difficult to build a direct causal link from anisogamy to “conventional sex-roles”. For example: if females have a lower PRR due to higher energy expenditure in gametes, male reproduction becomes limited by female PRR. Males can return faster than females to the mating pool, and the operational sex-ratio will become highly male biased (Queller 1997). In such a situation however, it is not clear why males should return to the mating pool and suffer intense competition instead of caring for their offspring. Some theoretical work shows that the bias in parental expenditure imposed by anisogamy could in fact lead to more parental care in males (Kokko et al. 2006). Other factors may explain a lower parental care in males, such as uncertain paternity (see Queller 1997 and Kokko et al. 2006). Additionally, PRR can be very sensitive to environmental conditions (e.g. change in nesting site availability, resource dependent parental care) challenging the view of fixed “sex-roles”.(Example in blenny fish, Almada et al. 1995, and gobiid fish, Forsgren et al. 2004)

(iv) The opportunity for sexual selection Bateman (1948) was already interested in the sex differences in variance in mating success. He observed that while some males never mated, other ones were very successful (mating with up to five females). On the other hand, most females were mated but they rarely mated with multiple males. It is clear that this situation gives a higher “opportunity” for selection to act on males: if for example the very successful males have some trait in common that the non-mated ones miss, selection will be extremely strong to promote the expression of that trait. But since almost all females are mated once, there is little chance for (sexual) selection to act on females. For this reason, the standardized variance in mating success is called the opportunity for sexual selection (Shuster and Wade 2003). However, this variation in mating success is not a measure of selection, only of the “opportunity” for selection to act. For example, it is also possible that the huge variance in mating success observed in males is just due to chance, and that there is no consistent difference between successful and unsuccessful males (see Sutherland 1985 for a criticism of Bateman’s experiment). This measure should therefore be interpreted with care and not be confused with a direct measure of selection that should involve the correlation between trait and mating success or fitness (Krakauer & Webster, 2011). It is often argued that this measure should be used in combination with the Bateman gradient to avoid misinterpretation (Jones, 2009).

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The evolution of parental care, variance in reproductive success and sexual competition traits from anisogamy

In this paragraph, I will give a brief overview of the large body of theoretical work that has been devoted to understanding the evolution of sex-biased parental care, sex-biased selection and sex-biased competition and mate searching traits with the aim to relate those sex--biases to anisogamy.

(i) Parental care The evolution of parental care involves complex feedbacks and is dependent on historical contingencies, making it difficult to detect general patterns (Houston and McNamara 2005). Here, I will focus on simple theoretical argument regarding parental care. Queller (1997) developed a framework explaining why parental care should be female biased as a consequence of a higher variance in male reproductive success (and not as a consequence of anisogamy, the link between anisogamy and male variance in reproductive success is discussed below). According to this view, since less males than females end up reproducing (due to a higher variance in reproductive success in males, some males will not mate), the parental investment of a given male in a population’s offspring is scattered across more individuals than it is for a female. Therefore, the investment of a male in each particular offspring should be lower than the one of a female. Additionally, the benefit a male gets from caring may be reduced due to uncertain paternity (Queller 1997, Kokko and Jennions 2008). Another way of presenting this argument goes as follows: if a subset of males is consistently more likely to successfully mate (non-random ), the cost of caring for offspring is indeed higher for those males than it is for females (Queller 1997).

It is important to note that a sex-bias in parental care is unlikely to be the result of a biased OSR, as often assumed in verbal models. Indeed, Kokko and Jennions (2008) have shown that when applying the Fisher condition of equal adult sex-ratio to a population, a male biased operational sex-ratio should also select for parental care in males and prevent the evolution of sexual dimorphism in this trait. This can be understood quite easily, if one pictures a population where all males return immediately to the mating pool after mating, leaving females to care for offspring. The mating pool will therefore mainly be composed of males, and the chances of mating very low. An alternative male strategy would then be to care for offspring. In conclusion, no strong theoretical argument seems to explain a sex bias in parental care directly from anisogamy (for example as a result of the different energy investment in the single egg and sperm cell that form a zygote). A female biased parental care may be better explained by a 13 male-biased variance in reproductive success which in turn is likely not a direct consequence of anisogamy as discussed below.

(ii) Strength of selection/variance in reproductive success Pre-copulatory sexual selection makes male competition obvious. Many systems are observed in which a successful male can monopolize several females (harem, lek). This results in higher male variance in reproductive success as some males get a high number of matings and others almost none, whereas most females get mated. However, so far no empirical or theoretical work has indicated that this may be a direct consequence of anisogamy alone. Only anisogamy under specific conditions will lead to a sex-bias in variance in reproductive success. A male bias in the variance in reproductive success would more likely be the result of pre-existing competition traits developed more readily in males. The evolutionary origin of such traits and why they can develop more easily in males may in turn be a direct consequence of anisogamy, as discussed in the next paragraph.

(iii) Competition and mate-searching traits A recent paper by Lehtonen et al. (2016) provided a clear theoretical argument about the role of anisogamy in the evolution of male competition and mate searching traits in males. Interestingly, their results are affected by sperm limitation. In most internal fertilizers, sperm limitation is non-existent, meaning that there is more sperm than necessary to fertilize all the eggs produced by females. In this case, they showed that the sex producing the highest number of gametes experiences the strongest selection pressure in increasing the fertilization success of each gamete (a female gamete fertilization success is always 1 when sperm is not limiting, whereas many sperm cells will never fuse). Males should therefore experience stronger selection than females to develop competition and mate-searching traits when sperm is not limiting. However, if sperm is limiting, as not uncommon in external fertilizers (Levitan, 1998), the conclusion from Lehtonen et al.’s model are slightly different. They showed that under sperm limitation males and females should experience the same selection pressure to evolve competition and mate-searching traits because both male and female gametes have a sub- optimal fertilization success. Nevertheless, they argue males are still more likely to evolve competition traits than females, because males can reallocate energy from gamete production to competitive traits with a lesser cost than females (this last part relies on assumptions such as the nature of the gamete size to gamete survival relationship).

An important point to note here is that when reflecting on the mechanisms that may have led from anisogamy to any type of sex-bias (parental care, competition, etc.), one should probably 14 start off by imagining an organism for which anisogamy is the only sexual dimorphism to avoid confounding effects with other sexual dimorphisms already present. Incidentally, the usual example for such an organism is a sessile broadcast spawning marine animal such as described in Parker (2014). Empirical work has shown that for this type of organism the conditions for which females do not experience sperm limitation or negative consequences of are narrow (Levitan, 2004). Therefore, it seems clear that anisogamy alone does not necessarily set the stage for a stronger selection pressure on males to express competitive traits. Male and female may both experience selection pressures to increase their fertilization success, but the evolution of such traits is less constrained in males. increasing fertilization success, such as internal fertilization, may then create a situation where sperm is not limiting, therefore releasing females from the selection pressure to evolve further mate searching or competition traits.

Summary

I have surveyed measures that are available to characterize mating systems: the Bateman gradient, the operational sex ratio, potential reproductive rate and the intensity of sexual selection are among them and have been used with more or less success to explain observed patterns of sexual dimorphism.

For an evolutionary biologist the crucial question remains: Is there a discernable and explainable general pattern of sexual dimorphism? This is a question with dual perspective. On the one hand we might ask: can we explain the evolutionary cascade that led from anisogamy to the pattern we see today (see Parker 2014 for an attempt in that direction)? On the other hand, can we extrapolate from this pattern to further evolutionary developments?

Although there are consistent patterns of sexual dimorphism in parental care and variance in reproductive success observable across many taxa (Janicke et al 2016) it seems that a simple explanation invoking anisogamy as a direct cause as envisioned by Bateman and Trivers is missing a strong theoretical support (Kokko and Jennions 2008). However, a very recent paper (Lehtonen et al. 2016) proposes a model that may explain the evolution of competition and mate-searching traits more readily in males as a result of anisogamy, and anisogamy only. In turn, variance in reproductive success in males could be higher due to the existence of those competitive traits, a situation that may then result in a female biased parental care.

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Finally, the observed diversity of mating systems and sexual dimorphisms may also depend highly on evolutionary history and environmental conditions (for example vs fish parental care), even on a very short time-scale (availability of nesting sites). For this reason, a sampling bias in studied species may have important consequences on the observed patterns of sexual- dimorphism. It will surely be of great interest to follow the future development of this field as more and more species are being studied, adding up to the fascinating picture that is our understanding of sexual reproduction.

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ESSAYS IN THE SERIES ISSN 1404-4919

1. Reproductive patterns in marine animals on shallow bottoms. - Anne-Marie Edlund. 1979 2. Production in estuaries and saltmarshes. - Staffan Thorman. 1979 3. The evolution of life history traits. - Anders Berglund. 1979 4. in marine littoral communities. - Carin Magnhagen. 1979 5. Insular biogeographic theory, developments in the past decade. - Stefan Ås. 1979 6. Theories and tests of optimal diets. - Juan Moreno. 1979 7. Ecological characters in insular communities. - Mats Malmquist. 1980 8. / relationships: a synopsis. - Ola Jennersten. 1980 9. Sexual size dimorphism in birds of prey. - Per Widén. 1980 10. The evolution of avian mating systems. - Per Angelstam. 1980 11. Dispersal, dispersion and distribution in small populations. - Fredric Karlsson. 1980 12. Age-related differences of competence in birds. - Karin Ståhlbrandt. 1980 13. Respiration measurements as a tool in fish ecology. - Bengt Fladvad. 1981 14. Intraspecific variation; its and consequences. - Lars Gustafsson. 1981 15. Cooperative breeding in birds: theories and facts. - Mats Björklund. 1982 16. Some aspects of . - Göran Sundmark. 1982 17. Evolution and ecology of migration and dispersal. - Jan Bengtsson. 1982 18. Are animals lazy? - Time budgets in ecology. - Bodil Enoksson. 1983 19. Ecology of island colonization. - Torbjörn Ebenhard. 1983 20. Reproductive habits and parental care in some lacustrine African Cichlids (Pisces) with special reference to Lake Malawi species. - Ulrich Jessen. 1983 21. Monogamy or polygyny? - Mating systems in passerine birds. - Björn Westman. 1983 22. Distributional patterns in and . - Per Sjögren. 1983 23. Some theoretical considerations of dispersal. - Gunnar Nilsson. 1983 24. Interactions between animals and . - Urban Wästljung. 1984 25. Reproductive modes and parental care in . - Ingrid Svensson. 1984 26. Reproductive strategies in fishes. - Peter Karås. 1984 27. Sexual selection and female choice based on male genetic qualities. - Jacob Höglund. 1984 28. The timing of breeding in birds with special reference to the proximate control. - Mats Lindén. 1985 29. Philopatry and inbreeding versus dispersal and outbreeding. - Tomas Pärt. 1985 30. Evolution of sociality in Hymenoptera. - Folke Larsson. 1985

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31. Bird song and sexual selection. - Dag Eriksson. 1986 32. The energetics of avian breeding. - Lars Hillström. 1986 33. Sex role reversal in animals. - Gunilla Rosenqvist. 1986 34. Factors affecting post-fledging survival in birds. - Kjell Larsson. 1986 35. Quantitative genetics in evolutionary ecology: methods and applications. - Pär Forslund. 1986 36. Body size variations in small mammals. - Anders Forsman. 1986 37. Habitat heterogeneity and landscape fragmentation - consequences for the dynamics of populations. - Henrik Andrén. 1986 38. The evolution of predispersal predation systems in . - Mats W. Pettersson. 1987 39. Animal aggregations. - Anette Baur. 1988 40. Operational and other sex ratios: consequences for reproductive behaviour, mating systems and sexual selection in birds. - Jan Sundberg. 1988 41. in natural populations. - Annika Robertson. 1989 42. for a parasitic way of life. - Reija Dufva. 1989 43. Predator-prey coevolution. - Lars Erik Lindell. 1990 44. Parasite impact on host biology. - Klas Allander. 1990 45. Ecological factors determining the geographical distribution of animal populations. - Berit Martinsson. 1990 46. Mate choice - mechanisms and decision rules. - Elisabet Forsgren. 1990 47. Sexual selection and mate choice with reference to lekking behaviour. - Fredrik Widemo. 1991 48. Nest predation and nest type in passerine birds. Karin Olsson. 1991 49. Sexual selection, costs of reproduction and operational sex ratio. - Charlotta Kvarnemo. 1991 50. Evolutionary constraints. - Juha Merilä. 1991 51. Variability in the mating systems of parasitic birds. Phoebe Barnard. 1993. ISRN UU-ZEK-IRE--51—SE 52. Foraging theory: static and dynamic optimization. Mats Eriksson. 1993. ISRN UU-ZEK-IRE--52—SE 53. Moult patterns in passerine bird species. Christer Larsson. 1993. ISRN UU-ZEK-IRE--53--SE 54. Intraspecific variation in mammalian mating systems. Cheryl Jones. 1993. ISRN UU-ZEK-IRE--54--SE 55. The Evolution of Colour Patterns in Birds. Anna Qvarnström. 1993. ISRN UU-ZEK-IRE--55--SE 56. Habitat fragmentation and connectivity. Torbjörn Nilsson. 1993. ISRN UU-ZEK-IRE--56—SE 57. Sexual Selection. Models, Constraints and Measures. David Stenström. 1994. ISRN UU-ZEK-IRE--57—SE

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58. Cultural Transmission and the Formation of Traditions in Animals. Henk van der Jeugd. 1995. ISRN UU-ZEK-IRE--58—SE 59. Ecological Factors Affecting the Maintenance of Colour Polymorphism. Sami Merilaita. 1995. ISRN UU-ZEK-IRE--59—SE 60. The Evolution and Maintenance of Hermaphroditism in Animals. Anna Karlsson. 1996. ISRN UU-ZEK-IRE--60—SE 61. Costs and Benefits of Coloniality in Birds. Tomas Johansson. 1996. ISRN UU-ZEK-IRE--61—SE 62. Nutrient reserve dynamics in birds. Måns S. Andersson. 1996. ISRN UU-ZEK-IRE--62—SE 63. Nest-building for parental care, mate choice and protection in fishes. Sara Östlund. 1996. ISRN UU-ZEK-IRE--63—SE 64. Immunological ecology. Dag Nordling. 1996. ISRN UU-ZEK-IRE--64—SE 65. zones and speciation by reinforcement. Anders Ödeen. 1996. ISRN UU-ZEK-IRE--65—SE 66. The timing of breeding onset in temperate zone birds. Robert Przybylo. 1996. ISRN UU-ZEK-IRE--66—SE 67. Founder speciation - a reasonable scenario or a highly unlikely event? Ann-Britt Florin. 1997. ISRN UU-ZEK-IRE--67—SE 68. Effects of the Social System on Genetic Structure in Mammal Populations. Göran Spong. 1997. ISRN UU-ZEK-IRE--68—SE 69. Male Emancipation and Mating Systems in Birds. Lisa Shorey. 1998. ISRN UU-ZEK-IRE--69—SE 70. Social behaviours as constraints in mate choice. Maria Sandvik. 1998. ISRN UU-ZEK-IRE--70—SE 71. Social monogamy in birds. Kalev Rattiste. 1999. ISRN UU-ZEK-IRE--71--SE 72. Ecological determinants of effective population size. Eevi Karvonen. 2000. ISRN UU-ZEK-IRE--72—SE 73. Ecology of animals in ephemeral habitats. Jonas Victorsson. 2001. ISRN UU-ZEK-IRE--73--SE 74. Extra-pair paternity in monogamous birds. Katherine Thuman. 2001. ISRN UU-ZEK-IRE--74-SE 75. Intersexual communication in fish. Niclas Kolm. 2001. ISRN UU-ZEK-IRE--75—SE 76. The role of postmating prezygotic reproductive isolation in speciation. Claudia Fricke. 2002. ISRN UU-ZEK-IRE--76—SE 77. Host parasite interactions: Local adaptation of parasites and changes in host behaviour. - Lena Sivars. 2002. ISRN UU-ZEK-IRE--77—SE 78. The molecular clock hypothesis. Reliable story or fairy tale? Marta Vila-Taboada. 2002. ISRN UU-ZEK-IRE--78—SE 79. Chemical cues in mate choice. Björn Johansson. 2002. ISRN UU-ZEK-IRE--79—SE

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80. Does sexual selection promote speciation? A comparative analysis of the Family Labridae (wrasses). - Sarah Robinson. 2002. ISRN UU-ZEK-IRE--80—SE 81. Population bottlenecks and their effects on genetic diversity: introducing some recent methods for detection. Marnie H Demandt. 2003. ISRN UU-ZEK-IRE--81—SE 82. Immune response and its correlations to other traits in poultry. Joanna Sendecka. 2003. ISRN UU-ZEK-IRE--82--SE 83. Resistance of Hybrids to Parasites. Chris Wiley. 2003. ISRN UU-ZEK-IRE--83—SE 84. The Role of Genetics in Population Viability Analysis. Johanna Arrendal. 2003. ISRN UU-ZEK-IRE--84—SE 85. Sexual Selection and Speciation – The Scent of Compatibility. Nina Svedin. 2003. ISRN UU-ZEK-IRE--85—SE 86. Male-female coevolution: patterns and process. Johanna Rönn. 2004. ISRN UU-ZEK-IRE--86—SE 87. Inbreeding in wild populations and environmental interactions. Mårten Hjernquist. 2004. ISRN UU-ZEK-IRE--87—SE 88. – A topic of no consensus. Emma Rova. 2005. ISRN UU-ZEK-IRE--88—SE 89. Man-made offshore installations: Are marine colonisers a problem or an advantage? - Olivia Langhamer. 2005. ISRN UU-ZEK-IRE--89—SE 90. “Isolation by distance”: – A biological fact or just a theoretical model? Sara Bergek. 2006. ISRN UU-ZEK-IRE--90—SE 91. Signal evolution via sexual selection – with special reference to Sabethine mosquitoes. - Sandra South. 2007. ISRN UU-ZEK-IRE--91—SE 92. Aposematic Colouration and Speciation – An Anuran Perspective. Andreas Rudh. 2008. ISRN UU-ZEK-IRE--92—SE 93. Models of evolutionary change. Lára R. Hallson. 2008. ISRN UU-ZEK-IRE--93—SE 94. Ecological and evolutionary implications of hybridization. Niclas Vallin. 2009. ISRN UU-ZEK-IRE--94—SE 95. Intralocus sexual conflict for beginners. Paolo Innocenti. 2009. ISRN UU-ZEK-IRE—95—SE 96. The evolution of animal mating systems. Josefin Sundin. 2009. ISRN UU-ZEK-IRE—96—SE 97. The evolutionary ecology of host-parasite interactions. Katarzyna Kulma. 2011. ISRN UU-ZEK-IRE—97—SE 98. Sensory exploitation – trends, mechanisms and implications. Mirjam Amcoff. 2011. ISRN UU-ZEK-IRE—98—SE 99. Evolutionary biology of aging. Hwei-yen Chen 2012. ISRN UU-ZEK-IRE—99—SE 100. Gametes and Speciation: from prezygotic to postzygotic isolation Murielle Ålund 2012. ISRN UU-ZEK-IRE—100—SE

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101. Resting metabolic rate and speciation. Eryn McFarlane 2014. ISRN UU-ZEK-IRE—101—SE 102. Brain Evolution: Insights from comparative studies Masahito Tsuboi 2014. ISRN UU-ZEK-IRE—102—SE 103. Dispersal and hybrid zone dynamics. Jakub Rybinski 2015. ISRN UU-ZEK-IRE—103—SE 104. Parasitism and speciation in a changing world. William Jones. 2017 105. An evolutionary perspective on sex in animals. Ivain Martinossi-Allibert. 2017

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