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The Sexual Selection Continuum

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The Sexual Selection Continuum Received 23January 2002 Accepted 18March 2002 Publishedonline 11 June 2002 Thesexual selection continuum Hanna Kokko1*,Robert Brooks 2,JohnM. McNamara 3 and AlasdairI. Houston 4 1Division ofEnvironmentaland EvolutionaryBiology, Institute ofBiomedical and Life Sciences, University ofGlasgow, Glasgow G12 8QQ, UK 2Schoolof Biological, Earth and EnvironmentalScience, TheUniversity ofNew SouthWales, Sydney 2052,NSW, Australia 3Schoolof Mathematics, University ofBristol, University Walk,Bristol BS8 1TW, UK 4Schoolof Biological Sciences, University ofBristol, Woodland Road, Bristol BS8 1UG, UK The evolution ofmate choicefor geneticbene ts has becomethe tale oftwo hypotheses: Fisher’ s ‘run- away’and ‘ goodgenes’ , or viability indicators.These hypotheses are oftenpitted against eachother as alternatives, with evidencethat attractive males sire more viable offspring interpretedas support for good genesand with anegative ornull relationship betweenmating successof sons and other componentsof tnessinterpreted as favouring theFisher process.Here, we build ageneral modelof female choicefor indirect benets that capturesthe essence of both the‘ Fisherian’and ‘ good-genes’models. All versions ofour model point toa single processthat favours female preferencefor males siring offspring ofhigh reproductive value. Enhancedmating successand survival are thereforeequally valid geneticbene ts of mate choice,but their relative importance varies dependingon female choicecosts. The relationship betweenmale attractivenessand survival may bepositive or negative, dependingon life-history trade- offsand mating skew.This relationship canchange sign in responseto increased costliness of choice or environmental change.Any form offemale preferenceis subjectto self-reinforcing evolution,and any relationship (or lack thereof)between male display andoffspring survival is inevitably an indicator of offspring reproductive values.Costly female choicecan be maintained with or withouthigher offspring survival. Keywords: Fisher process;runaway evolution;good genes; mate choice;indirect benets; sexual selection 1. INTRODUCTION cessdemonstrated that in apopulation wheresome mate choiceoccurs already, andwhere preference and display Anytrait evolvesin directresponse to natural selection are heritable, thebuild-up of ageneticcorrelation between andin indirect responseto selectionon genetically corre- preferenceand display is inevitable (Lande1981) and lated traits. In thecase of mating preferencesfor exagger- leadsto runaway coevolution(Lande 1981; Kirkpatrick atedsexual displays, direct tnessbene ts and costs 1982). Positive preference–display geneticcorrelations imposedirect selection on mate-choice behaviour, but have beenfound in nature(Bakker 1993; Wilkinson & indirect selectiondue to geneticcovariation betweenmate Reillo 1994; Houde1994; Gray &Cade1999) andtheir choiceand other tnesscomponents is also thought tobe rapid build-upunder experimental conditionshas been widespread(Andersson 1994). Fisher (1930) pointedout empirically veried (Blows 1999). that it wouldbe adaptive for femalesto prefer mating with In recentyears, attention has shiftedagain tothe rst males that bear atrait that is favouredby natural selection. componentof Fisher’ s theory—the evolution ofprefer- Furthermore, Fisher recognizedthat asa preference encesfor male traits that indicate tnessin contextsother increasesin frequency,the attractiveness of thetrait itself than mate choice.This has beenspurred by many factors, will amplify theadvantage ofmate choice.The ensuing including thearticulation by Zahavi (1975) ofthe handi- ‘runaway’process of coevolution would exaggerate the cap principle, aconsiderablebody oftheoretical modelling display trait beyondits naturally selectedoptimum. Dis- (e.g.Pomiankowski 1988; Grafen1990 a,b; Iwasa et al. play exaggeration is halted by atrade-offbetween male 1991; Houle& Kondrashov2002), theobservation that attractivenessand other componentsof tness,and prefer- in many speciespreferred males are more vigorous and encesfail toexaggerate whenmale survival is socurtailed long-lived than non-preferredmales (Jennions et al. 2001) that thereis nolonger any benet tofemales of mating andoften produce offspring ofhigher viability (Møller & with attractive males. Alatalo 1999) andarguments that additive geneticvari- Fisher’s namehas becomeassociated in thesexual- ation in tnesscomponents can be maintained by pro- selectionliterature with thesecond component of his cessessuch as host– parasite coevolution(Hamilton &Zuk theory—the runaway coevolutionbetween preference and 1982), genotypeby environmentinteraction (Kotiaho et display (Fisher 1930). Early attempts tomodel this pro- al. 2001) andmutation– selection balance (Rowe& Houle 1996). Anunfortunate consequence of the success of good-genesindicators has beenan overemphasis ofthe * Authorfor correspondence (h.kokko@bio.gla.ac.uk). differencebetween these so-called ‘ goodgenes’ or ‘indi- Proc.R. Soc.Lond. B (2002) 269, 1331–1340 1331 Ó 2002 TheRoyal Society DOI10.1098/ rspb.2002.2020 1332H. Kokko andothers Thesexual selection continuum cator’ modelsand the Fisherian runaway process.One choiceevolution whetherthe viability ofattractive males couldbe forgiven for thinking, uponreading thecontem- is greater than,less than or equal tothat ofunattractive porary literature, that Fisherian runaway andgood-genes males. indicators werealternative theoriesfor theevolution of mate choiceand that themain goal ofthe eldis todis- 2. THE MODEL tinguish betweenthese as alternative hypotheses. Considerableempirical attentionhas focusedon the Weconsider a population in which births anddeaths phenotypic andgenetic relationships betweenmale sexual occurcontinuously and the primary sexratio is 1:1. Mate display andsurvival, becauseviability is oneof the most choicefor indirect bene tscan operate only whenmales important tnesscomponents that may beindicated by vary in someheritable trait. To provide aconceptually sexual displays. Alarge numberof studies estimate the simple example, weassume the existence of a genewith phenotypic (Jennions et al. 2001) orgenetic(Reynolds & twoalternative alleles, i = 0and2, that is expressedin Gross1992; Norris 1993; Petrie 1994; Jones et al. 1998; males only.The genein uencesthe male ’sappearance in Møller &Alatalo 1999; Wedell &Tregenza 1999; Brooks waysdescribed in thefollowing paragraphs, andit can 2000) associationbetween attractiveness, survival, fec- covary with survival positively, negatively or notat all. It undityand other tnesscomponents (Petrie 1994; canthus also bethought tore ect the ‘quality’ of a male. Møller &Alatalo 1999; Wedell& Tregenza 1999; Brooks However,to avoid any unnecessaryconnotations with ter- 2000). Apositive relationship betweenmale attractiveness minology that is biasedin favour ofone (runaway) or the andoffspring survival (or other aspectsof tness) is other (indicator) direction,we simply refer tomales carry- thought tosupport the good-genes hypothesis (Norris ing thesealleles asmale ‘types’ i = 1and2, andnote that 1993; Petrie 1994; M øller &Alatalo 1999; Jennions et al. wedo not necessarily assume a correlation betweenmale 2001), whereasa negative relationship combinedwith sig- type andsurvival. ni cantheritability ofattractiveness is interpretedas fav- Weassumehaploid inheritance ofthe gene. Any model ouring aFisherian mechanism alone (Etges1996; Jones et ofsexual selectionfor indirect bene tswill require a al. 1998; Wedell &Tregenza 1999; Brooks 2000). How- mechanism tomaintain variation in males.As our focus ever,it is conceivable within apurely good-genesframe- is noton solving thelek paradox, wesimply assumethat workthat males with thehighest geneticquality advertise sucha mechanism exists:allele 1mutatesto allele 2with sointensely that their survival becomesworse than that of a rate of m1 per generation,and allele 2toallele 1with males ofpoorer quality (Grafen1990 a;Kokko1998, a rate of m2 (seetable 1for afull list ofvariables and 2001; Eshel et al. 2000). their de nitions). In dealing with therelationship betweensexual attract- The type ofa male cannotbe observed directly. How- ivenessand survival, it is crucial toremember that costly ever,a male oftype i also expressesa sexually selected sexual advertisementis alife-history trait subjectto trade- trait denotedby Di (for ‘display’; if Di = 0themale lacks offswith other componentsof reproductive effortand with thedisplay trait). Additionally, both males andfemales futuresurvival andfecundity (Partridge &Endler1987; carry apreferencegene P that dictatesfemale preferences Grafen 1990a;Gustafsson et al. 1995; Kokko1997, 1998, for large values of Di.Female preferencescan vary con- 2001; Ho¨glund& Sheldon1998). Anegative relationship tinuouslyfrom absent( P = 0) tostrong (large P). A high betweenreproductive effort(including advertisement)and value of P meansthat afemale spendsmuch effort in her survival is consistentwith life-history theory (Hansen& mate choiceto nda male with alarge D,butthis effort Price 1995; Kokko1998). Thus,under many conditions, also reducesher fecundity, F(P): ¶ F/¶ P , 0(sothat the it is conceivable that apreferencefor males with high lev- costof choice C(P) = (F(0) 2 F(P))/F(0); see gure 1). elsof costly advertisement and poor survival prospectscan Basedon the function F(P),we distinguish betweentwo still deliver an indirect tness bene ttofemales,based on conceptsof costs of choice. The environmentally determ- superior tnessof offspring.It wouldfollow that adistinc- inedcostliness
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