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Sexual Selection, Sex Roles, and Sexual Conflict

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Sexual Selection, Sex Roles, and Sexual Conflict Downloaded from http://cshperspectives.cshlp.org/ on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press 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.” Editors: William R. Rice and Sergey Gavrilets Additional Perspectives on The Genetics and Biology of Sexual Conflict available at www.cshperspectives.org Copyright # 2014 Cold Spring Harbor Laboratory Press; all rights reserved. Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a017509 1 Downloaded from http://cshperspectives.cshlp.org/ on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press G.A. Parker 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 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a017509 Downloaded from http://cshperspectives.cshlp.org/ on October 1, 2021 - Published by Cold Spring Harbor Laboratory Press The Sexual Cascade 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-
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