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The Sexual Cascade and the Rise of Pre-Ejaculatory (Darwinian) Sexual Selection, Sex Roles, and Sexual Conflict

Geoff A. Parker

Department of Evolution, Ecology and Behaviour, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, United Kingdom Correspondence: [email protected]

After brief historic overviews of sexual selection and sexual conflict, I argue that pre-ejacu- latory sexual selection (the form of sexual selection discussed by Darwin) arose at a late stage in an inevitable succession of transitions flowing from the early evolution of syngamy to the evolution of copulation and sex roles. If certain conditions were met, this “sexual cascade” progressed inevitably, if not, sexual strategy remained fixed at a given stage. Prolonged evolutionary history of intense sperm competition/selection under external fertilization preceded the rise of advanced mobility, which generated pre-ejaculatory sexual selection, followed on land by internal fertilization and reduced sperm competition in the form of postcopulatory sexual selection. I develop a prospective model of the early evolution of mobility, which, as Darwin realized, was the catalyst for pre-ejaculatory sexual selection. Stages in the cascade should be regarded as consequential rather than separate phenomena and, as such, invalidate much current opposition to Darwin–Bateman sex roles. Potential for sexual conflict occurs throughout, greatly increasing later in the cascade, reaching its peak under precopulatory sexual selection when sex roles become highly differentiated.

exual selection and sexual conflict are vast changed through evolutionary time, from Sfields in evolutionary biology; when possi- mostly gamete competition in early unicellu- ble, here, I refer to reviews. I begin with brief lar eukaryotes, intense sperm competition in general historic overviews of sexual selection ancestral sessile and relatively immobile or- and sexual conflict; more detail can be found ganisms, to both pre-ejaculatory (Darwinian) in Andersson (1994), Simmons (2001), Chap- and postejaculatory sexual selection. These man et al. (2003), and Arnqvist and Rowe transitions in the evolution of sexual strategy (2005). Much of the current state of the field arise as logical consequences whenever certain of sexual conflict is covered in this collection. successive conditions are met, and together My principal aim, however, is to outline form what may be termed the “sexual cas- how sexual selection and sexual conflict have cade.”

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HISTORIC OVERVIEW: SEXUAL Despite the major early conceptual advances SELECTION after Darwin made by Fisher (1930), an explo- sion of interest, including attention to Bate- Precopulatory Sexual Selection man’s ideas, gained impetus much later during Darwin (1871, p. 256) defined sexual selection the behavioral ecology revolution of the 1970s as depending “on the advantage which certain (Parker 2006a), although the first signs came individuals have over other individuals of the earlier. Maynard Smith’s (1958) essay helped same sex and species, in exclusive relation to to clarify the different effects of natural and sex- reproduction.” Although his definition clearly ual selection, which were becoming confused, embraces all possible aspects of sexual selec- and Fisher’s (1930) work was republished in tion, Darwin’s evidence and discussions related 1958. For sexual selection by female choice, exclusively to competition over mating and Fisher had proposed (1) that females showing ejaculation. The past 40–50 years have seen a preference for males with traits indicating massive research efforts devoted to this subject. their biological fitness (“indicators”; see An- Darwin’s two major categories of pre-ejacula- dersson 1994) would be favored, which (2) leads tory sexual selection (male combat and female to positive feedback between the gene for the choice) are now described in all evolutionary preferred male trait and the gene for the female texts. The monograph by Andersson (1994) preference (“Fisher’s sons effect”), accelerating gives an excellent survey of all but the last two fixation of both genes, and (3) female choice decades. may exaggerate the development of the male Interest and controversy surrounded sexual trait beyond its natural selection optimum (the selection for half a century after Darwin, gener- “runaway” process) until natural selection fi- ating both detailed surveys (e.g., Richards 1927) nally prevents further development. Fisher’s and notable conceptual advances (Fisher 1930), last research student, Peter O’Donald, pioneered but attention faded after Huxley’s influence in population genetic models of female choice the 1930s (Huxley 1938a,b). Despite the occa- (O’Donald 1962, 1980), concluding that con- sional inspirational study (e.g., Jacobs 1955), ditions for runaway were restrictive. However, the subject languished for almost three decades, notably, more optimistic advances concerning probably because of the (implicit) group/spe- Fisher processes were made by Lande (1981; cies selection interpretations of adaptation pre- see also Kirkpatrick 1982). “Indicators” include vailing throughout that time. The notable ex- cues of “good genes” or immediate female ben- ception was Bateman’s (1948) now classic study efits such as good male territories or parenting of Drosophila melanogaster, which he used to (e.g., Williams 1966; Orians 1969; Trivers 1972), support his argument that sexual selection “handicaps” that signal “good genes” (Zahavi arises because male fitness typically increases 1975; Grafen 1990), and brightness of male col- more steeply with number of matings with dif- oration correlating with parasite resistance ferent females than female fitness mating with (Hamilton and Zuk 1982). Andersson (1994) different males, a fact that (following Darwin) gives an excellent review of the historical devel- he attributed ultimately to anisogamy. He used opment of these ideas. this to explain why males show “undiscriminat- Male–male competition for matings has at- ing eagerness” and females “discriminating pas- tracted less theoretical attention than female sivity,” behavioral characteristics of sexual selec- choice, possibly because it is simpler and less tion stressed by Darwin (1871) and considered interesting conceptually. Trivers’ (1972) pro- to be supported by general observation. The posal that relative parental investment (PI) de- relation between fitness and number of matings termines the intensity of sexual competition is now termed the “Bateman gradient,” and the undoubtedly catalyzed the sudden interest in predictions surrounding this classic view of sex- sexual selection that began in the 1970s. It was ual selection have been termed the Darwin– followed by suggestions that the operational sex Bateman paradigm or DBP (Dewsbury 2005). ratio (OSR) (Emlen and Oring 1977) or relative

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potential rates of reproduction (PRR) (Clutton- considering them to be unaffected by sexual se- Brock and Vincent 1991) represented the key lection: “In the lowest classes the two sexes are index. More recently, emphasis has been placed not rarely united in the same individual, and on the difference in variance of reproductive therefore secondary sexual characters cannot success of the sexes (Shuster and Wade 2003), be developed. In many cases in which the two an index expressing the opportunity for sexual sexes are separate, both are permanently at- selection and related to Bateman’s (1948) orig- tached to some support, and the one cannot inal predictions. All measures (PI, OSR, PRR, search or struggle for the other. ... Hence in and relative variance in reproductive success) these classes, such as the Protozoa, Coelenterata, are likely to covary with the relative “times in” Echinodermata, Scolecida, true secondary sex- and “times out” of the mating pool of the two ual characters do not occur; and this fact agrees sexes (Clutton-Brock and Parker 1992; see Par- with the belief that such characters in the higher ker and Birkhead 2013) and have good rea- classes have been acquired through sexual se- sons to correlate with sexual selection intensity lection, ...” (Darwin 1871, p. 321). Darwin de- (Jennions and Kokko 2010; Kokko et al. 2012; bated why bright coloration occasionally occurs Parker and Birkhead 2013), although debate still in some sessile or relatively immobile inverte- continues over exactly what measure best re- brates, concluding this to be the product of nat- flects the intensity of sexual selection (reviewed ural rather than sexual selection. Although he in Parker and Birkhead 2013). rejected the relatively mobile annelids and ceph- Qualitative evidence for male–male com- alopod mollusks as candidates for sexual selec- petition has always been very strong compared tion, he devoted much discussion to the various with female choice. My PhD studies of dung arthropod taxa, particularly in the insects, in flies, published mostly in 1970, may represent which copulation is often well developed and the first attempt to validate this aspect of sexual male fighting apparatus and bright coloration selection quantitatively (reviewed in Parker sometimes apparent. 1978a,b, 2006a). Field observations fitted well Arthropods aside, Darwin thus gave virtu- with predictions based on competitive optimi- ally all his attention to vertebrates, particularly zation models, suggesting that sexual selection those with copulation and internal fertilization. could indeed be the dominant selective force He did not mention competition between ejac- shaping male reproductive behavior. Males be- ulates or massive male gametic expenditure in haved so as to maximize fertilization rate given his “lowly organized” sessile or relatively immo- that other males do the same, that is, their be- bile animals. I argue here that such stages played havior patterns appeared to be evolutionarily a major role, with their high testes expenditure stable strategies (ESSs) (sensu Maynard Smith because of competition between ejaculates, in and Price 1973; Maynard Smith 1982) set by the the cascade of events in the evolution of sex- selective pressure of intramale competition (re- ual strategy that culminated in precopulatory viewed in Parker and Pizzari, in press). There sexual selection that Darwin so brilliantly per- can be little doubt that intrasexual selection has ceived and described in 1871. That he so posi- played a major part in determining male mate tively dismisses these taxa suggests that he did searching, contest, and mate-guarding strate- not suppress insights into ejaculate competition gies, something that has been rather overshad- simply because of the sensitivities of Victorian owed in recent decades by the focus on female culture. Remarkably, “Darwin probably never choice. made the intellectual leap that would have al- lowed him to identify the possibility of postcop- ulatory sexual selection” (Birkhead 2010) or Postcopulatory Sexual Selection competition between ejaculates in general. It is interesting that Darwin dismissed lower It is now well appreciated that sexual selec- invertebrates: “The lowest classes will detain us tion does not end when mating begins. Birkhead for a very short time....” (Darwin 1871, p. 300), (2010) gives an excellent account of the historic

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aspects of postcopulatory sexual selection. My ual selection when a mutation causes strategic review of sperm competition in insects (Parker changes that would increase fitness in one sex, 1970) is claimed to have stimulated develop- but decrease fitness in the other sex (a sexually ment of the field of postcopulatory sexual se- antagonistic mutation). In fact, sexual conflict lection (e.g., Birkhead 2000, 2010; Simmons concepts can be applied to all anisogamous sex- 2001; Eberhard 2009). Since 1970, enormous ual systems (Scha¨rer et al. 2014) Hermaphro- amounts of research, both empirical (e.g., Smith dites combine male and female in one indivi- 1984; Birkhead and Møller 1992, 1998; Sim- dual, and sexual conflict operates differently in mons 2001) and theoretical (reviewed in Parker sequential and simultaneous hermaphrodites and Pizzari 2010) have been devoted to the top- (Scha¨rer et al. 2014). At the level of nuclear ic. Later, attention also focused on female con- genes, conflict can be interlocus if it concerns trol of fertilizations, that is, “cryptic female traits determined by different loci or intralocus choice” in the form of sperm selection or ejacu- if it concerns a trait determined by alleles at late manipulation (Thornhill 1983; Eberhard a single locus (Rice and Holland 1997; Parker 1985, 1996, 2009). Sperm competition is now and Partridge 1998). Cytoplasmic genetic ele- seen as the postejaculatory analog of Darwinian ments are maternally inherited and require a male–male competition for mating and cryptic different logic (e.g., Zeh 2004; Hurst and Frost female choice, the analog of Darwinian female 2014). For interlocus conflict, a sexually antag- choice of males before mating. onistic mutation will spread unless a counter- Postcopulatory sexual selection, in fact, en- strategy evolves to prevent it at a locus expressed compasses adaptations both during and after in the other sex. Various definitions have been copulation (Eberhard 2009). Although catego- proposed (see Arnqvist and Rowe 2005; Kokko rization into pre- and postcopulatory sexual se- and Jennions 2014), but it is important to note lection serves a useful purpose, it presents prob- that sexual conflict in evolutionary biology re- lems for the many externally fertilizing taxa in lates to conflict in evolutionary time, which may which copulation is lacking; “pre- and post- or may not be manifest in the behavior observed ejaculatory” are more general terms. Competi- in male–female interactions. tion among ejaculates will normally be a strong Although Darwin (1871) appears not to selective force in external fertilizers, including have discussed sexual conflict directly, he was those that are sessile and weakly mobile (Levi- well aware that sex-limited inheritance could re- tan 2010). Failure to appreciate this not only late to different selective forces acting on males was an oversight by Darwin, but has also im- and females. For example, he envisaged that peded a full understanding of the succession of adult female sizewas often increased byselection evolutionary events (the “sexual cascade”) that to produce more ova and cryptic female colora- generated internal fertilization and precopula- tion could reflect camouflage against predators tory sexual selection. (i.e., because of natural selection), whereas in- creased male size, weaponry, and coloration often reflected the result of sexual selection. Dar- HISTORIC OVERVIEW: SEXUAL CONFLICT win–Bateman notions of indiscriminate eager- A detailed history of the field of sexual conflict ness in males and discriminating passivity in can be found in Arnqvist and Rowe (2005). “Bat- females also hint at mating conflict. tle of the sexes” concepts (the notion that males The concept that a gene may be beneficial and females have conflicting interests) go back in one sex but costly in the other was appre- into history and usually relate to the immediate ciated for many decades by population geneti- behavior associated with conflicts between the cists (e.g., Fisher 1931, p. 363), but little detailed sexes. In evolutionary biology, sexual conflict discussion of the opposing interests of the sexes concerns instances in which the evolutionary can be found before 1970 (Arnqvist and Rowe interests of males and females are different (Par- 2005); with rare exceptions, the prevailing view ker 1979) and arises very commonly out of sex- was that reproduction is an exclusively cooper-

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ative venture between the sexes. The modern “conflict zone” or “battleground”) within which rise of the concept of sexual conflict, as with sexual conflict will apply, given that the male sexual selection, is linked to the behavioral and female have shared offspring (see also An- ecology revolution that had its roots in the late dre´s and Morrow 2003; Parker 2006b). Consider 1960s and exploded in the 1970s (Parker a mutant gene that increases a male’s fitness 2006a). During this period, the concept became through sexual selection, but has a collateral quite widespread among those involved. Wil- cost via the female affecting their shared off- liams (1966) discussed an “evolutionary battle spring. If the cost is too high, there is no conflict, of the sexes” in which males may be adapted to and the gene will not spread. If the cost is suffi- overcome female resistance to mating, which ciently low and the benefit high, the gene will would generate counteradaptation in females. spread, and so will a gene that causes females to (Williams’ index includes the term “sexual con- prefer to matewith amutant male. But foralarge flict,” but in the sense of intrasexual competi- parameter space, there will be conflict; the male tion between males.) Clear expositions in the trait is favored, but so is female resistance to biological literature appear to be those by Triv- males with the trait, that is, the character is in ers (1972) and Dawkins (1976) (see also Daw- male,but not female, interests. The analysis went kins and Krebs 1979). on to define and analyze biological cases and Arnqvist and Rowe (2005) have claimed that conflict zones in which sexual conflict was likely, an important early foundation was my paper and two simulation models to investigate con- (Parker 1979) on sexual conflict and sexual se- flict resolution, one of which resulted in contin- lection, which was delayed in press (for historic ual cycling of coevolutionary strategies (“unre- accounts, see Arnqvist and Rowe 2005; Parker solvable evolutionary chases”). 2006a, 2010, 2013). It had been stimulated by This paper attracted little interest and, as a my dung fly research in the late 1960s in which subject area, sexual conflict remained inconspic- I analyzed male and female interest separately uous until the mid-1990s. Although exceptions and appreciated that they could often be in con- during this period were few (see Arnqvist and flict.Realizingthatthishadgeneralimplications, Rowe 2005), some were notable. For example, the final paragraph of my sperm competition laboratory studies showed significant costs to review concluded with (Parker 1970, p. 559): D. melanogaster females inflicted by males dur- ing mating (Partridge et al. 1986); these result The female cannot be regarded as an inert envi- from male accessory gland proteins, many of ronment in and around which this form of ad- aptation (male adaptation to sperm competi- which appear to benefit males, but conflict with tion) evolves. Supposing, for example, a mating female interests (reviewed by Simmons 2001 and plug reduces a female’s reproductive rate, this Chapmanetal.2003).Fieldstudiesalsooccasion- natural selection disadvantage will affect both ally provided strong evidence for sexual conflict male and female. Provided that the plug confers (a notable example is Davies 1992). a sexual selective advantage on the male, which A surge of activity, however, occurred in outweighs its natural selective disadvantage, it the mid-1990s. Key players were Bill Rice and should evolve or be maintained. Resultant mod- ifications within the female to prevent or reduce his student Brett Holland in America, Go¨ran the disadvantageous effects of the plug might be Arnqvist in Sweden, and Locke Rowe in Canada, expected; these adaptations may conflict with although manyothers contributed. Arnqvist be- the line of adaptation in the male sex. The fe- gan his study of sexual conflict by working on male, however, is not isolated from intramale mating systems of water striders, Gerris (Arnqv- selection because a female mating with a male ist 1989), as did Locke Rowe (Rowe 1992). They possessing a character of sexual selective advan- were quick to collaborate (Rowe et al. 1994) and tage will gain if the character is present in her male offspring. produced strong empirical evidence of a coevo- lutionary arms race between male-clasping de- This foreshadowed my 1979 analysis, which be- vices to overcome female resistance, and female gan by investigating the parameter space (the adaptations to aid in male rejection (Arnqvist

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and Rowe 1995). In addition to their indepen- cles in the same supplement; Tregenza et al. dent contributions to sexual conflict, their col- 2006 and articles in the same theme issue), the laborations, culminating in their major mono- prevailing view supporting the ubiquity of sex- graph (Arnqvist and Rowe 2005), have both ual conflict. Sexual conflict has, by now, become notably advanced and consolidated the field. an important and currently vigorous field in Bill Rice came to the subject through evo- evolutionary biology. lutionary genetics; his early theoretical work showed that sex chromosomes assist sexual di- EVOLUTION OF SEXUAL STRATEGIES: morphism evolution by enabling genes coding THE SEXUAL CASCADE for sexually dimorphic traits to accumulate on the X (or Z) chromosome (Rice 1984). He The various evolutionary adaptations sur- used genetic markers and experimental evolu- rounding sexuality have presented a formidable tion to create a new sex-determining locus in challenge for evolutionary biologists and many, D. melanogaster and elegantly showed that, as from meiosis to sexual selection and sexual con- predicted, genes detrimental to the homoga- flict, continue to generate debate. Here and else- metic sex accumulated close to this locus (Rice where (Parker and Pizzari, in press), a deductive 1992). Appreciating that male and female in- approach is developed that seeks to explain sex- terests often could not be satisfied simultane- uality as a sequence of events within a causal ously and that this may generate sexually antag- framework. It is important to distinguish be- onistic coevolution (a form of intraspecific Red tween irreversible evolutionary transitions that Queen) (Rice and Holland 1997; Holland and are ubiquitous and fixed in most extant ad- Rice 1998), Rice (1996) showed by experimen- vanced animal taxa and more labile transitions tal evolution that when female D. melanogaster that can be more readily reversed by ecological were prevented from coevolving with males, changes. The primary sexual step of meiosis and males quickly adapt, generating high costs to syngamy leads predictably to gamete competi- females. Holland and Rice (1999) showed that tion and (especially as organismal complexity in D. melanogaster populations in which mo- increases) to the evolution of two sexes (anisog- nogamy was enforced during experimental evo- amy), which generates unitary sex ratios. Ances- lution, males evolved to be less harmful to fe- tral forms of sexual selection (gamete competi- males, which evolved to be less resistant to tion and selection) would have been prevalent male-induced harm. Gavrilets (2000) devised in early external fertilizers. With the evolution an important formal model of “chase away” co- of mobility and behavioral complexity, copula- evolution similar to that envisaged by Rice and tion and “traditional” sex roles emerge inevita- Holland (1997) and Holland and Rice (1998), bly in most anisogamous systems lacking par- showing that this has the potential to drive spe- ental care (i.e., most animal species). However, ciation (although this depends on how conflict parental care of the zygote is a much more labile is resolved) (Parker 1979; Parker and Partridge transition that allows deviations from tradition- 1998). al sex roles through the evolution of paternal In the past decade or so, opposition to sex- investment. ual conflict interpretations has been spearhead- During this evolutionary succession (the ed by Bill Eberhard (e.g., Eberhard 2005), who “sexual cascade”), the opportunity for different proposed that apparent behavioral conflict is episodes of sexual selection changes dynami- often in female interests and represents a mech- cally, and alternative stable states occur at anism by which the female filters out (rejects) many steps. After the ancestral phase of gamete lower-quality males and “gains by losing” to and sperm competition under external fertiliza- persistent males of high mating advantage be- tion, precopulatory sexual selection eventually cause they generate high fitness progeny. This follows as a result of such features as multicel- catalyzed debate on the importance of sexual lularity, the unity sex ratio, enhanced mobility conflict (see Hosken and Snook 2005 and arti- and increased behavioral capacity for male–

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male competition, and the evolution of internal ker and Pizzari, in press). A more detailed ac- fertilization and is associated with a reduction count of some of the transitions is given in a in the strength of postcopulatory sexual selec- companion paper to the present article (Parker tion and an associated increase in precopulatory and Pizzari, in press). sexual selection, with a consequent higher dif- ferentiation of male and female sexual strate- Transition A: Events Leading to an Ancestral gies. There is a notable logical compulsion in Isogamous Eukaryote this sequence of events that flows inevitably from the early evolution of meiosis and gamete A suite of transitions in evolution, ranging from formation and eventually results in sex-role dif- the origin of life up to meiosis, recombination, ferentiation and its associated conflicts (Parker gametic fusion (syngamy), mating types, and and Pizzari, in press), supporting the view of the haploid–diploid cycle in eukaryotes (see Scha¨rer et al. (2012) that sex-specific selection, Maynard Smith and Szathma´ry 1995), are here arising ultimately from anisogamy, drives the all grouped together (transition A, Fig. 1). Much evolution sexual dimorphism, rather than of the evolution of these early stages remains chance differences in male–female life history shrouded in mystery, and interest in the selective and mating traits. advantage of sexuality over asexuality, which expanded in the 1970s (e.g., Williams 1975; Maynard Smith 1978), continues to preoccupy TRANSITIONS IN THE SEXUAL evolutionary biologists (Hartfield and Keightley CASCADE 2012). The main transitions in the cascade in Figure 1 are outlined below as a series of discrete steps. Transition B: Evolution of Gamete Size Although, in general, the evolution of one step Dimorphism (Two Sexes) precedes and creates the selective pressure for the next, some synchrony in adaptation across The sexual cascade in eukaryotes begins with an adjacent steps seems likely. The cascade is driven isogamous unicell (Fig. 1). Transition B, from initially by gamete competition and later (after isogamy to anisogamy, is the key transition in the evolution of anisogamy) by sperm compe- the cascade because it marks the origin of two tition. As Darwin (1871) surmised, it is the rise sexes (in my view, sexes should be defined in of mobility and complex behavior that catalyzes terms of gamete size produced and not con- the development of pre-ejaculatory (Darwini- fused with mating types) (Parker 2011; but see an) sexual selection; what Darwin missed was Hoekstra 2011 for an opposing opinion). An- the long preceding history of sexual selection on isogamy is often associated with an increase in gametes and gonads. As the importance of pre- cellular complexity and is universal in Metazoa ejaculatory sexual selection increases, the opti- (see reviews of Lessells et al. 2009; Parker 2011). mal economic balance between pre- and post- Lessells et al. (2009) review the three main ejaculatory expenditures shifts toward reduced theories for the evolution of anisogamy from an testes mass and sperm production (i.e., toward ancestral isogamous unicellular eukaryote. Be- lower precopulatory expenditure) (Parker et al. ginning with Cosmides and Tooby (1981), one 2013). theory proposes that anisogamy evolved in re- The sexual cascade (Fig. 1) provides a logi- sponse to conflict between nuclear genes and cal imperative for pre-ejaculatory (Darwinian) genes in cytoplasmic elements such as mito- sexual selection and for Darwin’s (1871) and chondria, chloroplasts, and intracellular para- Bateman’s (1948) claims about the link between sites (reviewed by Hoekstra 2011). Lessells the primary sexual differentiation (anisogamy) et al. (2009) conclude that cytoplasmic conflict and the evolution of traditional sex roles, which models are unlikely to be an adequate sole ex- has recently been challenged (in my view, un- planation of anisogamy, although they may help justifiably) (see Parker and Birkhead 2013; Par- to maintain it once evolved.

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Evolution of A Ancestral meiosis, sexual isogamous Retained in recombination, unicellular many protista and syngamy eukaryotes Increased zygotic reserves B favored, especially as multicellularity emerges Retained in Anisogamous many protista unicells Fisher’s C principle

Unity sex ratio D Complex multicellularity

Anisogamous Retained in most immobile multicells with external fertilizers high-gonad mass in both sexes Mobility and High sperm competition behavioral complexity (e.g., communal spawning)

Mobile anisogamous animals with Reduced sperm competition, high gonad mass in both sexes (e.g., noncommunal spawning)

Evolution of copulation and E internal fertilization; reduced sperm competition

Low male–male Mobile anisogamous competition; male animals with expenditure on reduced testes mass parental care Reduction in testes and sperm F production; increase in precopulatory competition Increased precopulatory sexual selection and evolution of Darwinian sex roles and sexual conflict

Figure 1. The sexual cascade (succession of evolutionary events leading to Darwinian sexual selection) (pink boxes and arrows) showing main transitions and selective forces (white boxes and black arrows) and alternative stable states (blue boxes and arrows). The transitions (A–F) are explained in the text.

Two other theories appear more plausible mus 1932) relates to the fact that anisogamy because both are based only on a trade-off be- could yield more surviving zygotes than isoga- tween size and number of gametes (inevitable in my. If some parents produce vast numbers of an ancestral unicell) and the fact that, over some tiny gametes, this increases the probability of range, the fitness (i.e., success or viability) of a fertilization of the relatively low number of large zygote must increase with its size. The “gamete gametes that survive well as zygotes. The “gam- limitation” theory (e.g., Levitan 1996; begin- ete competition” theory (Parker et al. 1972) re- ning with a population-level proposal by Kal- lates to the fact that gamete competition can

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generate disruptive selection on an isogamous Early gamete competition models assumed population leading to anisogamy (reviewed by simplistically that a gamete could survive suc- Parker2011).Again,largegametessurvivewellas cessfully provided it was above a critical mini- zygotes, but intermediate and small gametes mum size (Parker et al. 1972; Maynard Smith compete to gain most fusions with the large 1982); whether selection favors isogamy or an- gametes. The ESS does not depend on whether isogamy then depends critically on the impor- the model assumes random fusion between tance of zygote size. More recent models (e.g., gametes or begins with mating types. If selection Bulmer and Parker 2002) include a function favors increased complexity (e.g., toward multi- relating gamete survival to gamete size, as well cellularity), then higher zygote size is favored, as a function relating zygote fitness to zygote which increases the likelihood of anisogamy size. Which ESS (isogamy or anisogamy) is at- (Parker et al. 1972; Bulmer and Parker 2002). tained depends on how similar these two func- An elegant recent analysis (Lehtonen and tions are. If similar, the ESS is isogamy, but if the Kokko 2011) shows the relation between these zygote size-to-fitness function shifts away from two theories. Previously, both had been mod- the gamete size-to-fitness function, requiring eled as a large population of adults releasing much greater size to achieve the same fitness, gametes into an external medium (sea water). the ESS is anisogamy (Bulmer and Parker In Lehtonen and Kokko’s model, (1) the num- 2002; Lehtonen and Kokko 2011). Exactly this ber of adults in the local mating group could sort of change toward larger zygotes is likely to vary from two (i.e., no gamete competition) have accompanied increasing organismal com- to infinity (maximum gamete competition), plexity during the evolution of multicellularity, and (2) the rate of fusions of gametes could and there is also empirical evidence that this is also vary, either by reducing gamete produc- accompanied by a trend toward anisogamy (see tion rates or encounter rates or by increasing review of Parker 2011). However, if selective gamete mortality rates (see also Scudo 1967). pressures do not favor multicellularity, isogamy They showed that anisogamy could evolve should remain fixed if the two functions remain from isogamy through either gamete limitation rather similar, as seems likely in many unicells or competition, depending on these two factors. (although many show primitive forms of an- When gametes can fuse fairly readily, even low isogamy). levels of gamete competition (three or more Once sexual reproduction and syngamy adults per breeding group) generate anisogamy. have evolved, transition B (anisogamy) is thus However, gamete limitation (low gamete fusion likely to accompany the evolution of multicel- rates) can also generate anisogamy, provided the lularity and increased organismal complexity. number of adults per group remains low (i.e., It is associated with an immediate and primor- low gamete competition). Which effect (gamete dial sexual conflict. If gametes can fuse readily, competition or limitation) has had the larger protofemales do better when their ova are fer- influence on the origin of anisogamy (and hence tilized by other ova rather than by parasitic, two sexes) depends on conditions experienced noncontributing sperm (Parker et al. 1972; Par- in ancestral isogamous unicells, but gamete ker 1978c). Parker et al. (1972) proposed two competition appears the more robust selec- reasons why sperm producers were likely to tive force (Lessells et al. 2009) and one that leads win: (1) Because the available mutations would naturally to sperm competition under external be proportional to the number of gametes fertilization once anisogamy (and hence the produced, sperm may have achieved a higher two gamete-producing morphs, males and fe- adaptation rate in coevolutionary battles. (2) males) become established. Although this ques- If sperm–sperm fusions produced nonviable tion may be difficult to resolve, gamete (sperm) zygotes, sperm producers may have been under competition certainly offers a plausible solution stronger selection to avoid sperm–sperm fu- for the maintenance of anisogamy in most cur- sions and gain sperm–ovum fusions than rent populations (Parker 1982, 2011). ovum producers were to avoid sperm–ovum

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fusions. Parker (1978c, 2011) gives further rea- equilibrium. This selective constraint forms a sons why an ovum producer carrying a muta- vital part of sexual selection and conflict by en- tion that prevented sperm–ovum fusions is suring that (1) in sessile or weakly mobile ex- likely to have been unsuccessful. However, if ternal fertilizers, numerous sperm must com- gametes cannot fuse readily and there is lit- pete for rare ova, and (2) in internal fertilizers, tle gamete competition, anisogamy may evolve if males have less “time out” than females, males without conflict as a cooperative solution, as must compete for matings with females. an individual selection extension of Kalmus’ (1932) original proposal (Lehtonen and Kokko 2011). Transition D: Sperm Competition and Evolution of Complex Organisms with High Gonad Mass Transition C: Evolution of the Unity The evolution of multicellularity has been Sex Ratio much discussed; it has evolved at least 25 times The evolution of anisogamy may involve muta- including several times in eukaryotes, but only tions that change gamete size by altering the once in animals (e.g., Grosberg and Strathmann numberof cell divisions per unit of reproductive 2007; Bonner 1998), and involves many con- resource. Such a mutation would similarly affect flicts (reviewed by Grosberg and Strathmann all gametes produced by a given mutant indi- 2007). Complex multicellularity may be diffi- vidual, ultimately resulting in separate sexes cult to acquire, and its origin in plants and an- (gonochorism) arising from two mating type imals can be traced back to ancestral marine lineages. This argument suggests that separate forms. Marine plants and immobile or weakly sexes would typically be ancestral for anisogamy mobile invertebrates spend most of their repro- arising in unicells. However, some primitive co- ductive effort on gametes (see Parker and Piz- lonial forms such as Volvox include both her- zari, in press); other expenditures include pher- maphrodite and gonochoristic species, so that omones and various adaptations to enhance it is not immediately clear whether the ancestral fertilization such as spawning synchrony. Be- states would have been separate sexes or her- cause they have few other means of achieving maphroditism for anisogamy arising in multi- reproductive success, massive gametic expen- cells. Because a hermaphrodite individual re- diture in both sexes results in a high propor- quires two types of gonad, economy suggests tion of the total body mass (the gonado-somat- that specialism into separate sexes generally ic index or GSI) being expended on gonads would be favored (Heath 1977), with hermaph- and gamete production (Parker and Pizzari, in roditism (or more complex hermaphroditic press). Broadcast spawning, often synchronous, forms such as gynodioecyorandrodioecy) being results in intensive sperm competition, which favored only under certain special conditions is predicted to maintain male gonad expendi- (Charnov et al. 1976). ture at very high levels (Parker and Pizzari 2010). Under gonochorism, Fisher’s (1930) princi- It is interesting that male GSI in sessile or rela- ple immediately operates to favor and maintain tively immobile broadcast spawning marine an- equal numbers of males and females. Essential- imals can considerably exceed female GSI in ly, the rarer sex has a fitness advantage that is lost some taxa (Parker and Pizzari, in press). Why only when equality is attained. The unity sex this should be so is unclear; one might imagine ratio (transition C) is thus an immediate con- that GSI, here, would be equal, with males show- sequence for populations with two sexes (an- ing reduced GSI when expenditure increases isogamy) and arose in the original gamete com- on traits associated with precopulatory sexual petition simulations (Parker et al. 1972). Unless selection. In their vertebrate-dominated study, special circumstances apply (see Hamilton Hayward and Gillooley (2011) found similar 1967; Charnov 1982; West 2009), equal produc- GSI in both sexes, but much higher gamete pro- tion of the two sexes is maintained in a tight duction rates in females.

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At this ancestral stage of immobile (or rela- and behavioral complexity in external fertilizers tively mobile) marine broadcast spawners, sex- appears inevitably to be linked with female tar- ual selection is essentially postejaculatory and geting (e.g., amplexus behavior in anurans), al- sexual conflict relates mainly to fertilization though when sperm competition is intense, GSI conflicts. often remains high, reducing only as sperm com- petition reduces (e.g., for fishes, see Stockley et al. 1997; for amphibians, see Byrne et al. 2002). / Transition E: Mobility Behavioral Complexity An immobile broadcast spawner has little and Evolution of Reduced Sperm option other than to maximize gamete produc- Competition tion (in both sexes); males are thus committed Darwin (1871, p. 274) suggested that the rea- to expend all their reproductive effort on sperm. son male gametes are “brought to” female gam- The evolutionary steps by which increased mo- etes, rather than the reverse, relates to the rela- bility and behavioral complexity may, in some tive difficulty of transporting ova. Because of taxa, lead to reduced sperm competition and the risks of “at least a short transit through the testis expenditure are interesting to contem- waters of the sea,” he plausibly suggested that plate. A possible sequence is as follows: as soon as organisms evolved some mobility, males would be favored if they “were to acquire 1. The weakly mobile ancestor has broadcast the habit of approaching the female as closely as spawning with high GSI in both sexes. All possible” to reduce risk to unprotected gametes. reproductive effort is diverted to gametes, A transition from external to internal fertiliza- there is little secondary sexual dimorphism, tion (usually by copulation) is associated with and sperm limitation is relatively common. the colonization of the land (e.g., Dawkins and 2. Weak mobility permits and favors aggrega- Carlisle 1976). tion for synchronous spawning to increase There are probably many reasons why mo- fertilization probability for both sexes. The bility and behavioral complexity has arisen in sex ratio in spawning aggregations would be animals, including more efficient feeding and close to unity because both sexes expend escape from predators. However, once low mo- similarly on gametes. tility was possible in certain animal taxa, sperm competition may have been a potent selective 3. Mutant males showing primitive female tar- force favoring the evolution of increased mo- geting are favored because they achieve bility and “female-targeted” sperm release by sperm competition advantages (see below). males, leading ultimately to copulation with in- 4. As female targeting spreads and becomes ternal fertilization (Parker 1970, 1984), which more advanced, then, because the sex ratio all probably arose through combined selection on spawning grounds is close to unity, sperm to increase (1) fertilization gains in the intense competition decreases as many of the spawn- sperm competition conditions characteristic ings occur in pairs. of marine broadcast spawning and (2) the pro- portion of eggs fertilized, either through sperm 5. Close association of the sexes at spawning limitation or high gamete mortality (e.g., after decreases sperm limitation, reducing the ad- broadcast spawning). The dawn of mobility vantage of spawning aggregation and syn- and behavioral complexity is, thus, the catalyst chrony to females. that permitted the rise of pre-ejaculatory sexu- 6. Female targeting and pre-ejaculatory male al selection out of sexual selection by ejaculate competition advance further and costs to fe- competition. Mobile external fertilizers, such males of aggregation and male harassment as fishes and many amphibians, typically show favor female dispersion. high degrees of female targeting, and whereas sperm competition remains intense, male GSI 7. This further decreases sperm competition, scores remain relatively high. Thus, mobility reducing male GSI more and increasing

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G.A. Parker

male expenditure on pre-ejaculatory traits (Slattery and Bosch 1993), indicating that fe- such as mate searching and other forms of male harassment may be present. male–male competition. Reduction in sperm competition is predict- ed theoretically to reduce male gonad expen- In support, many of the above steps appear diture (see models reviewed in Parker and Piz- to be “fossilized” in modern species. For exam- zari 2010). There is some empirical evidence ple, following step 1, echinoderms are typically for this in external fertilizers and abundant ev- marine broadcast spawners with weak mobility, idence across many internally fertilizing taxa equal sex ratios, and GSIs; percentage fertil- (reviewed in Simmons and Fitzpatrick 2012), ization is very variable, so that sometimes there so that relative testes size is now commonly is considerable sperm limitation (Levitan and used as an index of the level of sperm competi- Petersen 1995). Obvious secondary sexual di- tion. However, the key to reduced sperm com- morphism is very rare and restricted to special petition in the above sequence of steps relates ecological conditions (Levitan 2005). As in step to female targeting coupled with spatial disper- 2, many species show synchronous spawning sion of females. Ejaculate and testis economy in aggregations (e.g., Himmelman et al. 2008), arise because expenditure devoted to finding in which fertility can then be high (Levitan and targeting sperm release toward females can 2010). Remarkably, steps 3–5 appear to be mim- yield higher fertilization gains than sheer nu- icked in the asteroid, Archaster typicus (Run et al. merical sperm productivity alone. But paradox- 1988). Here, especially, the males display in- ically, as pre-ejaculatory expenditure increases creased mobility as the breeding season begins at the expense of postejaculatory expenditure, and show female targeting; they seek out and the OSR is likely to become increasingly male- mount females and begin to release sperm im- biased, which can allow some restoration of mediately after the female spawns. Some 85% sperm competition level, depending on female of spawnings occur in this way at peak breed- propensity for multiple mating. ing season. Fertilization efficiency is very high Male GSI in broadcast spawners is typically (95% fertility occurred after pair spawnings). much higher than in taxa with copulation and Male GSI is much less than that of females. The internal fertilization (Table 1 in Parker and Piz- female/male GSI ratio ¼ 4.8, which is aberrant zari, in press). But is sperm competition gener- and the highest found in the literature for 18 ally reduced by internal fertilization? One argu- asteroid species (Table3 in Run et al. 1988), oth- ment might be that, in internally fertilizing erwise ranges from 2.1 to 0.4. Run et al. (1988), species, sperm is often provisioned within the suggest that this may relate to the trade-off female sperm stores, giving greater longevity of gonad against the energetic demands of high- and more opportunity for sperm competition er movement rates and female mounting in than external fertilizers, where the typical sperm males. Himmelman et al. (2008) commonly life is short. However, many external fertilizers witnessed similar “pseudocopulation” behavior have high spawning synchrony, sometimes in during spawning in the ophiuroids Ophiopholis mass aggregations, whereas internal fertilizers aculeata and Ophiura robusta, and (with much are often more dispersed. Furthermore, internal lower frequency, and in a less clearly defined fertilization gives females the opportunity to manner) in the sea star Asterias vulgaris (which resist copulations, and varying degrees of fe- had the second most reduced male GSI in Table1 male unreceptivity (often after an initial mat- in Run et al. 1988). The Antarctic sea star Neo- ing) are common in many species, probably be- smilaster georgianus, a brooding asteroid that cause the costs of polyandry to females are often probably reproduces continuously, may even significant, whereas the benefits are often (but have advanced to steps 6 and 7. Here the female not always) marginal. Thus, if females move to targeting behavior involves one or several males areas where males occur in high density, they mounting a reproductively active female for a often mate with one male and then leave. Very period of minutes to hours before spawning low sperm competition risk tends to occur in

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The Sexual Cascade

internal fertilizers that typically mate just once it is the transition to extensive male precopula- per reproductive cycle. When there is multiple tory expenditure that results in a high differen- mating, male GSI in internal fertilizers tends to tiation of sex roles as Darwin envisaged (i.e., the be rather comparable with that of aggregating DBP) and high levels of sexual conflict. Sperm mobile external fertilizers, but less than (and, economy results in a different balance between often, much less than) that of immobile or time spent on gametic investment for males and weakly mobile broadcast spawners (Table 1 in females (Williams 1966), which translates into Parker and Pizzari, in press). Thus, in general, the sexual asymmetry in parental investment sperm competition appears to be lower under (Trivers 1972), OSR (Emlen and Oring 1977), internal fertilization, although there is much and PRR (Clutton-Brock and Vincent 1991), all overlap depending on the mating system. of which can be related to times in or out of the Is male GSI high in broadcast spawners be- mating pool (Clutton-Brock and Parker 1992), cause of sperm limitation or competition? Note and generate divergence in sex roles envisaged that sperm limitation per se does not affect the by Darwin (see Parker and Birkhead 2013). level of sperm competition, which increases with It is important to separate the evolution of the number of non-self sperm in competition parental care, which is a labile, secondary phe- with self-sperm; even if only a small proportion nomenon that is actually relatively infrequent, of eggs are fertilized, with broadcast spawning, a viewed across the animal kingdom as a whole, given ejaculate may compete with many other from the primary, prezygotic parental invest- ejaculates for fertilizations. Whether species ment in gametes. It commonly involves sexual are subject to sperm limitation or competition, conflict and sometimes also cooperation (see then all else being equal, it pays for males to review of Sze´kely 2014). Gametic parental in- increase sperm numbers. Only when males vestment occurs symmetrically for parents in face neither sperm competition nor limitation isogamy, but for sound theoretical reasons (Par- can it pay to decrease sperm numbers. Immobile ker 1982; Lehtonen and Kokko 2011), it is con- species have little option other than to spend fined to female investment as ovum provision- their reproductive effort on gametes, but mobil- ing in species with advanced anisogamy (the ity can generate an alternative, more profitable selective forces underlying sperm and ovum expenditure on pre-ejaculatory traits associated size are reviewed in Parker 2011). In contrast, with female targeting. patterns of parental care of zygotes are highly diverse and have evolved many times indepen- dently (Clutton-Brock 1991), but maternal care Transition F: The Rise of Pre-Ejaculatory is much more common than paternal care. The Sexual Selection, Sex Roles, and Sexual selective mechanisms underlying parental care Conflict patterns are less clearly understood than those The above key transition E, that is, from broad- underlying gametic investment, and exactly cast spawning to searching for and targeting what shapes the form of parental care and how sperm release toward females, leading ultimate- it links to anisogamy (which, empirically, it ap- ly to the ubiquitous occurrence of copulation in pears to) remains controversial. The ecological most terrestrial animals, thus marks the rise of lability of parental care allows, not infrequently pre-ejaculatory (Darwinian) sexual selection. in certain taxa, deviations from traditional DBP As copulation and internal fertilization evolve, sex roles through the evolution of paternal care. relative potential gains through precopulatory Although Trivers (1972) linked the predomi- sexual competition can become more favorable nance of female care directly to anisogamy, this than sperm expenditure, especially if sperm has been disputed many times since. Dawkins competition reduces. Thus, precopulatory ex- and Carlisle (1976) pointed out that previous penditure rises at the expense of testis and ejac- investment does not a priori affect future invest- ulate expenditure. In contrast, female gametic ment, and argued plausibly that other biological expenditure typically remains high. Ultimately, circumstances, such as external versus internal

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fertilization, could affect the pattern of care. For tion of advanced mobility, transition E (Fig. 1). instance, males of internally fertilizing species Although the initial impetus for mobility could are typically not present when their young are have been related to pressures such as improved released, so male care is, here, harder to evolve food gathering and predator avoidance, these than in externally fertilizing species (see also are likely to have been greatly enhanced by intra- Maynard Smith 1977). Since then, the literature sexual selection on males to release gametes has expanded extensively (reviewed by Klug closer to females, and females to move closer et al. 2013a), and a direct effect of anisogamy to males to reduce sperm limitation (see above). in weighting parental care toward females has Because of the importance, as Darwin (1871) been increasingly questioned (see, e.g., Queller recognized, of the evolution of mobility and 1997; Kokko and Jennions 2008; Klug et al. behavioral complexity, I have investigated a sim- 2013a). Most recently, Klug et al. (2013a,b) ple prospective model to explain (1) the condi- have examined life history conditions favoring tions important for transition E through sexual transitions from existing states. When the ances- selection alone, and (2) why some invertebrate tral state is no care, although females initially groups remain fixed as sessile or weakly mobile invest more into each zygote than males, pater- external spawners with vast expenditure on tes- nal, maternal, and biparental care are equally tes and sperm production. likely to evolve if males and females are other- The model (for details, see Box 1) considers wise similar (Klug et al. 2013a). However, once a hypothetical marine invertebrate with weak some form of parental care has evolved, then as mobility in which males and females gather in male and female gametic investment becomes large groups to undergo broadcast spawning more disparate, with females investing heavily (Fig. 2). It calculates the initial “boost” to in- in eggs in away that decreases their future repro- creased mobility given by sexual selection on ductive success, transitions to increased mater- males to reduce sperm competition by examin- nal care (paternal ! maternal, paternal ! bi- ing the fitness of a rare mutant male that moves parental, biparental ! maternal) are more to “target” his sperm release toward spawning likely to be favored (Klug et al. 2013b) as the females. A biologically realistic interpretation stable state. This link with anisogamy may well of the model could be that both sexes use their help to explain the predominance of female care weak mobility to aggregate for spawning—they in nature. move closer together and then become station- When ecological or life history conditions ary, awaiting the start of gamete release. The do reverse sex roles, selection cannot produce a mutation we consider causes males to enhance drive back to isogamy by allowing males to in- this movement further; instead of remaining crease sperm size to assist in provisioning zy- stationary, the mutant moves toward spawning gotes, but males can instead evolve paternal in- females while releasing sperm. Although the vestment. An obvious reason for this is that model considers only the first step in female although paternal care can be focused on zy- targeting, it is easy to see how continued drive gotes, extra investment per sperm for zygote for such a process could lead to females con- provisioning would largely be wasted on the serving energy by reducing their aggregation be- vast numbers of sperm that do not fertilize havior, because as female targeting by males be- ova (Parker 1982, 2011; Lehtonen and Kokko comes more advanced, sperm limitation reduces 2011). Once attained and specialized, the two- (see above). This, in turn, increases the benefits sex state becomes highly stable. of mate searching by males, driving ultimately toward highly mobile mate searching and highly female-targeted sperm release, and often, ulti- THE EVOLUTION OF MOBILITY AND mately, copulation and internal fertilization. Itis FEMALE-TARGETED SPERM RELEASE not inconceivable that autosomal mutations for The key event leading to the rise of pre-ejacula- enhanced mobility that were initially favored in tory (Darwinian) sexual selection is the evolu- males through this form of sexual selection were

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The Sexual Cascade

M W M

Figure 2. Schematic representation of the model for the evolution of female-targeted sperm release. Wild-type males (blue male symbols) and females (brown female symbols) have low mobility and broadcast gametes. Males releasing sperm have a fertilization zone, b, depicted by the outer broken circles: In this zone, they compete with males with overlapping zones. They gain higher fertilization success with a proportion, a, of females (“nearby” females, represented as those within the blue shaded area around the focal wild-type male), but lower fertili- zation success with a proportion (12a) of females (“distant” females, represented as the white area between the concentric broken blue circles). A mutant male (pink male symbol) that moves to target females pays for this by having a reduced total sperm release, which changes zone b, but increases the proportion of nearby females.

also of benefit to both sexes for more efficient population because of the change in M and G, food foraging or predator avoidance. the ESS (at least in this simple model) does not Toreturn to the model: A male’s total sperm depend on b. Varying b changes the number of production is assumed to be proportional to his females, but similarly changes the number of expenditure G on gonad, and his sperm can competing males in the fertilization zone such fertilize eggs shed by spawning females in a that the two effects cancel each other out. Thus, zone b around him (Fig. 2). Within this zone, the ESS expenditure, M (see Box 1, Equation 3) he has higher fertilization success with a pro- depends only on (1) the total resources for re- portion a of females closest to him, and lower production, R, (2) f, an index of the fertiliza- success with the proportion (12a) of females tion skew toward nearby females (f ¼ 1 if there in b that are further away. The male can also is no fertilization difference between nearby and expend M on limited movement during the distant females, and rises above 1.0 as fertiliza- spawning period. This trades off with gonad tion skew toward nearby females increases), and expenditure within a fixed reproductive budget, (3) on a(M), which defines how mobility spent R (thus, R ¼ M + G). Suppose, now, that a mu- on female targeting increases the proportion of tant male arises that increases M so as to target nearby females in the fertilization zone b. females, that is, by moving toward spawning Some implications of this ESS were investi- females, its proportion a of “nearby” fertiliza- gated using exponentially diminishing returns, tions increases. The model, which is prospective that is, a(M) ¼ 1 2 exp(2mM), in which in- only, seeks the ESS expenditure (M) on this creasing m increases the rate at which a(M) primitive form of mate searching. approaches its asymptotic value of 1.0 (Fig. Despite the fact that the mutant’s fertiliza- 3A). Figure 3B shows how the ESS, M, changes tion zone b will deviate from the rest of the with the relative benefit of nearby females

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BOX 1. THE EARLY EVOLUTION OF FEMALE-TARGETED SPERM RELEASE

The following model examines the conditions that would favor the early evolution of female-targeted sperm release in an ancestral broadcast spawner; it makes a number of simplifying assumptions in the interest of mathematical tractability and is heuristic only. A schematic representation is given in Figure 2. Imagine a population of relatively immobile animals that shed gametes into the sea for fertiliza- tion. Each female releases E ova during spawning, and each male sheds s sperm. Adults have an amount of resource, R, to spend on reproductive effort, most of which (G units) is spent on gonad (and, hence, gametes) and rather little (M units) on (limited) mobility. Thus, R ¼ M + G, and for males, the number of sperm produced, s, increases linearly with the gonad investment as G ¼ gs.In this population, each wild-type (nonmutant) male releases ^s sperm and has allocations M^ , G^ . When such a male releases sperm, he is closer to a proportion a(M^ ) ¼ a^ of “nearby” females, and hence (per female) fertilizes relatively more of their ova, and relatively less (per female) with the proportion (1 a^) of “distant” females (Fig. 2). Suppose that there is a local spawning population density of m males and f females. Males gain fertilizations in a zone b around them and experience sperm competition depending on the number of other males with overlapping zones. The zone around each wild-type male increases with his sperm expenditure, G^ . We use the function b(G,M) to define the limits of the fertilization zone. For wild-type males, b(G^ , M^ ) ¼ b^, so that the zone overlaps with b^f spawning females and b^m spawning males (Fig. 2). We calculate fertilization gains using a loaded raffle model (Parker and Pizzari 2010). The sperm competition advantage in fertilization with nearby females is modeled by giving a focal male’s sperm a higher “competitive weight” with nearby females and a lower competitive weight with distant females by applying different loading factors to sperm in nearby and distant conditions (respectively, ^ hn and hd, where hn . hd). Thus, a wild-type focal male competing with (bm 1) similar males ^ ^ gains wn(^s, a^) ¼ bfEg^sa^hn=fg^s[a^hnþ(1 a^)]hd (bm 1)]g fertilizations with nearby females, and ^ ^ wd (^s, a^) ¼ b fEg^s(1 a^)]hd =fg^s[a^hnþ(1 a^)]hd (b m 1)]g with distant females, so that his total fertilizations are w(^s, a^) ¼ wn(^s, a^) þ wd (^s, a^) ¼ fE=m ¼ E if the sex ratio is unity ( f ¼ m). Now, consider the fertilization success of a mutant focal male with increased mobility (M . M^ ) that releases s , ^s sperm (because G , G^ ). He experiences two effects as a result of his increased mobility (see Fig. 2): (1) He targets his sperm release toward nearby spawning females by moving toward them and releasing sperm, thus increasing his proportion of nearby spawning females to a ¼ a(M) . a^, that is, a primitive form of mate searching, and (2) he alters his fertilization zone b,so that the population of individuals (of both) sexes overlapping with his zone changes to b ¼ b(G, M) = b^ compared with wild-type males. The nature of the change in b is harder to predict than that in a. If a male increases his mobility from M^ to M, he reduces the number of sperm he releases because of the trade-off, G ¼ R 2 M,so that s , ^s. This suggests that b , b^ because the mutant has a lower total sperm release, but because the mutant moves more through the spawning population, this assumption could be questioned. However, if we assume that the mutant experiences the same proportionate change in the number of male competitors and spawning females, he competes with (bm 2 1) males, each releasing ^s sperm, for fertilizations of bfE eggs, and we shall see later that the form of b(G ,M) does not influence the ESS. The mutant’s total fertilizations are

bfEgsðÞah þ ½1 a h w(s, ^s) ¼ n d : fgsg[ahn þ (1 a)hd ] þ ^sg[a^hn þ (1 a^)]hd (bm 1)

Dividing both numerator and denominator by hd and simplifying, we can write this as

bfEsg½a(f 1) þ 1 w(s, ^s) ¼ , (1) fgsg½þa(f 1) þ 1 ^sg½a^(f 1) þ 1 (bm 1)

where f ¼ hn/hd . 1, an index of the fertilization skew toward nearby females. Note that when the

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focal mutant plays the population strategy, that is, s ¼ ^s so that a ¼ a^, we see that again w(^s, ^s) ¼ fE=m. To find the ESS value for s, that is, s, we set

dw d 2w , ¼ 0, subject to 2 0, ds s¼^s¼s ds s¼^s¼s for a maximum, remembering that both a and b are functions of s. This differentiation of Equation 1 involves terms b and db/ds, but we eventually obtain

da(M) 1 s ¼ a(M) þ , (2) ds f 1

where the asterisks denote ESS values. Note that the b terms disappear. Effectively, decreasing b changes the number of females in the fertilization zone, but also similarly changes the number of males in competition, and the two effects cancel out each other. A more advanced model may examine this result in more detail, but we believe it to be a reasonable first approximation for this heuristic model. Allocations M and G trade off within the male’s reproductive budget, R. For simplicity, we have assumed that the amount of sperm released, s, is a linear function of the total mass of the gonad, that is, G(s) ¼ gs and M(s) ¼ R 2 gs. Thus,

da(M)=ds ¼g da(M)=dM:

Equation 2 then gives

da(M) 1 (R M) ¼ a(M) þ : (3) dM f 1

We now have a solution solely in terms of (i) the function a(M), which defines how female targeting increases the proportion of “nearby” females, (ii) f, which defines the fertilization skew toward nearby females, and (iii) R, the male’s reproductive budget. A plausible form for a(M) in this ancestral state would be an increasing function with diminishing returns. Setting a(M) ¼ 1 2 exp(2mM), m defines the rate of approach to the asymptotic value of a(M) ¼ 1.0 (Fig. 3A). We cannot obtain an explicit solution for M, but Equation 3 gives

exp ( mM)[1 þ m(R M)] ¼ f=(f 1), (4)

which can be used to iterate solutions for M (see Fig. 3B). As (f 2 1) increases, the ESS mobility level increases toward an asymptote determined by m. Note that highest ESS values for mobility and female targeting (M) are obtained when m is low and (f 2 1) high, although the range over which at least some degree of female targeting can be favored increases with m. We can ask what conditions permit the initial evolution of female targeting, that is, for a relatively immobile broadcast spawner to begin to move toward spawning females (the condition for M . 0). This depends only on the starting gradient of a(M), that is, on da(0)/dM. Applying either the expo- nential function above or the linear form a(M) ¼ mM to Equation 3, we find that the condition for female targeting to begin to evolve is simply that

m(f 1) . R1: (5)

The product of the marginal gain from increasing nearby females (m) and relative fertilization skew (f 2 1), must exceed the reciprocal of the male’s resource available for reproduction; if this can occur, the transition from sheer numerical sperm productivity toward sperm economy and female targeting begins.

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G.A. Parker

A 1.0 broadcast spawners? Many multicellular plants μ = 5 are sessile and fixed to the substrate, and hence 0.8 μ = 2 cannot move, as is the case for many marine μ = 1 invertebrates. Marine invertebrates with weak 0.6 μ = 0.5 or moderate mobility often have highly syn- α chronous spawning, which may reduce the ben- 0.4 efits of female targeting because gametes are shed very quickly and synchronously. Similarly, 0.2 if individuals are much dispersed, costs of mov- 0.0 ing to and targeting spawning females may be 0.0 0.5 1.0 1.5 2.0 2.5 3.0 high. Empirical studies of the relevant parame- M* ters in weakly mobile marine invertebrates B 3 would repay detailed investigation. μ = 0.5 This simplistic model thus shows the sort of μ = 1 conditions under which female-targeted sperm 2 release may have begun to evolve, and also why M* μ = 2 many taxa retain broadcast spawning. It predicts the initial rise of mobility for female targeting if 1 1 μ = 5 m(f 1) . R (Box 1, Equation 5). The three conditionsfavoring this crucial transition for pre- ejaculatory sexual selection are (1) high initial in- 0 10–2 10–1 100 101 creases in the proportion of nearby females by log(φ – 1) diverting resources from gonad to mobility (high m), (2) high relative fertilization benefits Figure 3. (A) Relation between a, the proportion of with nearby females (high f ), and (3) high re- “nearby” females and a male’s expenditure on mo- sources for reproduction (high R). The first two nility and female targeting, M.(B) Relation between requirements would seem more likely to be satis- the ESS mobility, M, and the log index of fertiliza- tion skew toward nearby females, log (f 2 1), at fied as behavioral complexity and high mobility different values for m, which defines the rate at which advance. A possibility is that an initial drive in a(M) increases to its asymptote. certain taxato increase mobility for food foraging purposesraisedresources(increasedR)andmade femaletargetingmoreeffective(raisedm),causing [log(f 2 1)]. If the relative fertilization benefit a sudden acceleration in female targeting. Selec- of nearby females is small (f ! 1), female tar- tion would then act to increase its effectiveness, geting will not evolve and the ESS is to remain as resulting in many taxa in a drive toward mate an immobile broadcast spawner, and if m is also searching by males, copulation and internal fer- low, even moderate benefit of nearby females tilization, and greatly reduced sperm competi- will not permit mobility to evolve. However, tion. This would be accompanied by greater po- high benefits of nearby females (f 1) result tentialforexpenditureonmoreintensepremating in significant mobility, generating very high M competition (M) with consequently reduced go- when m is low. When m is low, a(M) is slow to nad expenditure (G) (Parker and Pizzari 2010; approach its asymptote (Fig. 3A), so that the Parker et al. 2013). Effectively, this transition sig- marginal benefits of continued mobility invest- nifies the rise of pre-ejaculatory sexual selection, ment are high. When m is high, large amounts the form of selection discussed by Darwin. of female targeting can be achieved with low M, so high gonad investment can be maintained to SEXUALCONFLICTINTHESEXUALCASCADE aid in sperm competition. So, what biological conditions allow immo- Although pre-ejaculatory (Darwinian) sexual bility and high gonad mass to be maintained in selection appears only at late stages in the cas-

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The Sexual Cascade

cade (Fig. 1), sexual selection acting on gametes 1979, 2006b; Parker and Partridge 1998). How- begins after the evolution of syngamy and is ever, conflict will also arise from adaptations to likely to have been fundamental in generating sperm competition and may, too, be extensive two sexes (anisogamy). At this initial stage, sex- (reviewed by Stockley 1997; Edward et al. 2014). ual conflict concerns the fact that protofemales Recent critiques that DBP sex roles are un- share the high investment they put into proto- related to the primary sexual differentiation ova with protomales, whose gametes (proto- (anisogamy) are therefore unfounded (see also sperm) contribute little, and as anisogamy ad- Scha¨rer et al. 2012); sex roles flow logically from vances, nothing. This is essentially the twofold anisogamy as a consequence of the sexual cas- cost of sex (Maynard Smith 1978). The reasons cade and, as such, present no fundamental in- why males were likely to win this primordial consistency (Parker and Birkhead 2013; Parker sexual conflict, and why anisogamy is main- and Pizzari, in press). tained, are reviewed by Parker (2011). As com- plex multicellularity advanced, potent sexual selection persists as sperm/pollen competition ACKNOWLEDGMENTS and cryptic female choice in the two major I am grateful to Bill Rice and Sergey Gavrilets for kingdoms, with sperm/pollen competition the invitation to write this review, which has maintaining high relative male gonad invest- allowed me to elaborate on my ideas surround- ment unless (as in many animal taxa) mobility ing the sexual cascade that I developed for a evolves. In sessile animals, sexual conflict will monograph in the 1970s, but failed to complete, involve fertilization conflicts relating to, for ex- and ultimately abandoned. I am greatly indebt- ample, selection of favorable sperm, genetic ed to Hanna Kokko, Lucas Scha¨rer, and an compatibility, and prevention of polyspermy. anonymous reviewer for some very helpful sug- It will also concern parental care, which has gestions that have much improved the manu- evolved mainly (but not exclusively) as mater- script. I also thank Tom Pizzari for several ear- nal care in several sessile or weakly mobile in- lier discussions on this topic. vertebrates, but sometimes also as paternal care in mobile external fertilizers such as several am- phibians and many fish. REFERENCES With the evolution in many animal taxa of Reference is also in this collection. advanced mobility and female targeting, often involving copulation, testes reduction accom- Andersson MB. 1994. Sexual selection. Princeton University panies the rise of pre-ejaculatory (Darwinian) Press, Princeton, NJ. Andre´s JA, Morrow EH. 2003, The origin of interlocus con- sexual selection and evolution of sex roles. Tes- flict: Is sex linkage important? J Evol Biol 16: 219–223. tes reduction and the typical absence of male Arnqvist G. 1989. Multiple mating in a water strider: Mutual parental care result in male time in the mating benefits or intersexual conflict? Anim Behav 38: 749–756. pool greatly exceeding female time and relates to Arnqvist G, Rowe L. 1995. Sexual conflict and arms races high intensity of sexual selection on males (e.g., between the sexes: A morphological adaptation for con- trol of mating in a female insect. Proc R Soc Lond B 261: Clutton-Brock and Parker 1992; Kokko et al. 123–127. 2012; Parker and Birkhead 2013). Precopulato- Arnqvist G, Rowe L. 2005. Sexual conflict. Princeton Univer- ry sexual selection and the highly differentiated sity Press, Princeton, NJ. sex roles that often result from it, now generate a Bateman AJ. 1948. Intra-sexual selection in Drosophila. He- redity 2: 349–368. second dimension for sexual conflict: mating Birkhead TR. 2000. Promiscuity: An evolutionary history of conflict. Conflicts over mating decisions will sperm competition. Harvard University Press, Cambridge, most typically be of the DBP type with males MA. selected to persist and females to resist and may Birkhead TR. 2010. How stupid not to have thought of that: accompany mating decisions over inbreeding, Post-copulatory sexual selection. J Zool 281: 78–93. Birkhead TR, Møller AP. 1992. Sperm competition in birds: mate quality, and crosses between ecotypes, Evolutionary causes and consequences. Academic, Lon- and, hence, the probability of speciation (Parker don.

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The Sexual Cascade and the Rise of Pre-Ejaculatory (Darwinian) Sexual Selection, Sex Roles, and Sexual Conflict

Geoff A. Parker

Cold Spring Harb Perspect Biol published online August 21, 2014

Subject Collection The Genetics and Biology of Sexual Conflict

Mechanisms and Evidence of Genital Infanticide as Sexual Conflict: Coevolution of Coevolution: The Roles of Natural Selection, Mate Male Strategies and Female Counterstrategies Choice, and Sexual Conflict Ryne A. Palombit Patricia L.R. Brennan and Richard O. Prum The Evolution of Sexually Antagonistic Copulatory Wounding and Traumatic Phenotypes Insemination Jennifer C. Perry and Locke Rowe Klaus Reinhardt, Nils Anthes and Rolanda Lange Reproductive Parasitism: Maternally Inherited Sexual Conflict in Hermaphrodites Symbionts in a Biparental World Lukas Schärer, Tim Janicke and Steven A. Ramm Gregory D.D. Hurst and Crystal L. Frost Sex-Biased Gene Expression and Sexual Conflict Sexual Conflict and Sperm Competition throughout Development Dominic A. Edward, Paula Stockley and David J. Fiona C. Ingleby, Ilona Flis and Edward H. Morrow Hosken Human Homosexuality: A Paradigmatic Arena for Sexually Antagonistic Zygotic Drive: A New Form Sexually Antagonistic Selection? of Genetic Conflict between the Sex Andrea Camperio Ciani, Umberto Battaglia and Chromosomes Giovanni Zanzotto Urban Friberg and William R. Rice Sexual Conflict Arising from Extrapair Matings in Sex Chromosome Drive Birds Quentin Helleu, Pierre R. Gérard and Catherine Alexis S. Chaine, Robert Montgomerie and Bruce Montchamp-Moreau E. Lyon Sexual Conflict and Seminal Fluid Proteins: A Is Sexual Conflict an ''Engine of Speciation''? Dynamic Landscape of Sexual Interactions Sergey Gavrilets Laura K. Sirot, Alex Wong, Tracey Chapman, et al. Conflict on the Sex Chromosomes: Cause, Effect, Sexual Cannibalism as a Manifestation of Sexual and Complexity Conflict Judith E. Mank, David J. Hosken and Nina Wedell Jutta M. Schneider

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