The role of male contest competition over mates in speciation

UNCORRECTED PROOFQVARNSTRÖM A et al.: Male aggression and speciationThe role of male contest competition over mates in speciationAnna QVARNSTRÖM , Niclas VALLIN, Andreas RUDHAnimal Ecology/ Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36Uppsala, SwedenAbstract Research on the role of sexual selection in the speciation process largely focuses on the diversifying role of mate choice. Inparticular, much attention has been drawn to the fact that population divergence in mate choice and in the male traits subject to choicedirectly can lead to assortative mating. However, male contest competition over mates also constitutes an important mechanism of sexualselection. We review recent empirical studies and argue that sexual selection through male contest competition can affect speciation in waysother than mate choice. For example, biases in aggression towards similar competitors can lead to disruptive and negative frequencydependentselection on the traits used in contest competition in a similar way as competition for other types of limited resources. Moreover,male contest abilities often trade-off against other abilities such as parasite resistance, protection against predators and general stresstolerance. Populations experiencing different ecological conditions should therefore quickly diverge non-randomly in a number of traitsincluding male contest abilities. In resource based breeding systems, a feedback loop between competitive ability and habitat use may lead tofurther population divergence. We discuss how population divergence in traits used in male contest competition can lead to the build up ofreproductive isolation through a number of different pathways. Our main conclusion is that the role of male contest competition in speciationremains largely scientifically unexplored [Current Zoology 58 ( ): – , 2012].Keywords Male-male competition, Sexual selection, Speciation, Resource based breeding systems, Contest competition, Populationdivergence, Reproductive isolation1 IntroductionA major contemporary goal in speciation research is to investigate the mechanisms leading to population divergenceand reproductive isolation (Coyne and Orr, 2004; Dieckmann et al., 2004; Price, 2008). However, one mechanism ofselection, i.e. sexual selection through male contest competition, which can lead to fast evolutionary changes, hasreceived surprisingly little attention in the context of speciation. The aims of this article are to review studies on the roleof male contest competition in speciation and to pinpoint some major unexplored directions for future research.Natural selection leads to the evolution of traits that enhance their bearers’ survival chances and reproductive output intheir natural environment. Sexual selection also leads to the evolution of traits enhancing their bearers’ reproductiveoutput but in this case through access to mates, which can be viewed as a limiting resource for the sex with the highestpotential reproductive rate (Andersson, 1994). Due to their higher investment in gamete size and therefore in offspringquality (sometimes further increased by pregnancy and maternal care), females often have a lower potentialReceived Nov. 1, 2011; accepted Jan. 20, 2012. Corresponding author. E-mail: anna.qvarnstrom@ebc.uu.se© 2012 Current Zoology1

QVARNSTRÖM A et al.: Male aggression and speciationreproductive rate than males. This means that access to mates generally does not limit the reproductive rate of females,while the opposite is true for males (Trivers, 1972). For simplicity we will therefore focus our review on male contestcompetition over mates rather than on female contest competition over mates. However, some of the matters discussedin this article can also apply to female contest competition (see e.g. van Doorn et al., 2004)Both natural and sexual selection are known as important mechanisms underlying the process of speciation butnatural selection has received by far the most scientific attention. Speciation driven by divergent natural selection, oftenreferred to as ecological speciation (e.g. Schluter, 2000; Rundle and Nosil, 2005), has been identified as the underlyingforce driving whole adaptive radiations whereby a single ancestral species splits into a large number of new daughterspecies. Adaptive radiations have been documented in relation to entry into novel environments, for examples cichlidsin volcano lakes (Elmer et al., 2010) and finches exposed to climate change (Grant and Grant, 1993), or in relation tothe evolution of key innovations (i.e. evolution of traits that allow the use of novel resources, Berenbaum, 1983)whereby the ancestral species splits into daughter species that occupy a large number of previous unexplored niches.Strong competition over limiting natural resources can also by itself lead to splitting of populations. This is becauseindividuals that are able to utilize resources that are not used by most individuals in the population are favored byselection, i.e. there will be disruptive selection (Dieckmann and Doebeli, 1999).Sexual selection has also been acknowledged as an important evolutionary force driving speciation (West-Eberhard,1983; Price, 1998; Panhuis et al., 2001; Edwards et al., 2005; Ritchie, 2007; Kraaijeveld et al., 2011). There are at leastfour reasons to assume that sexual selection plays an important role in promoting genetic divergence betweenpopulations and the build up of reproductive isolation between them. First, competition over mates can be very intense(Andersson, 1994) and can lead to fast divergence in sexually selected traits as compared to naturally selected traits (butsee e.g. Svensson and Gosden, 2007). Second, closely related species often differ more in sexually selected traits than inother phenotypic traits, which is expected if these traits are subject to strong selection within species. In addition,divergence in sexually selected traits may have been further reinforced through selection against interbreeding betweenclosely related species (Dobzhansky, 1940; Coyne and Orr, 1989; Howard, 1993; Butlin, 1995; Hostert, 1997; Noor,1999; Ortiz-Barrientos et al., 2009). Third, sexually selected traits display extreme variation across animal taxa (West-Eberhard, 1983; Price, 1998; Panhuis et al., 2001; Edwards et al., 2005; Ritchie, 2007; Kraaijeveld et al., 2011)probably as a consequence of sexual selection operating in more arbitrary directions than natural selection. Fourth,because females often base their choice of mate on sexually selected traits, population divergence in such traits maydirectly lead to assortative mating (e.g. Lande, 1981; Higashi et al., 1999). This latter argument is the main reason whysexual selection is often acknowledged as an important component preventing homogenizing gene flow betweendiverging populations when speciation occurs in sympatry or at secondary contact.Sexual selection through mate choice is unlikely to by itself lead to speciation (reviewed in Ritchie, 2007). Sincesexual selection through mate choice is often unidirectional instead of bidirectional, the initiation and maintenance of adisruptive selection regime is rather unlikely. Many male display traits are condition-dependent and signal their bearers’ability to provide their mates with good genes or resources needed for reproduction (Andersson, 1994). Environmentspecific costs of mate choice may lead to different levels of sexual selection and divergence in male traits in allopatricpopulations (Maan and Seehausen, 2011), but would not ensure assortative mating at secondary contact. For example, iftwo populations diverge in male body size because female choice in favor of large body size acts as a weaker selectionpressure in one population, males belonging to the population with large individuals would nevertheless exert asupernormal sexual stimulus for females from the other population at secondary contact (see Labonne and Hendry,2010 for a similar case concerning color in guppies). However, Schluter and Price (1993) argued that female choicecould diverge between allopatric populations when several male traits indicate the same abilities but the perception of2

QVARNSTRÖM A et al.: Male aggression and speciationthese different traits varies across environments. Another recent model launched the idea that if only locally adaptedmales can develop large condition-dependent ornaments female discrimination against immigrant males would arise(van Doorn et al., 2009). Hence, female choice based on indicator traits could generate divergence in male traits orfacilitate assorative mating under certain conditions.The initiation of a disruptive selection regime may appear more likely when based on arbitrary Fisherian run-awayprocesses. Given sufficient initial genetic variation in female mate preferences several Fisherian run-away processesmay even operate within the same sympatric population (Higashi et al., 1999). In combination with elements of femalefemalecompetition and male-male competition, Fisherian processes could cause disruptive frequency dependentselection (van Doorn et al., 2004). Hence, sympatric speciation through Fisherian sexual selection is theoreticallypossible but in practice rather unlikely because it requires very specific conditions (van Doorn et al., 2004). Whenspeciation, at least partly, occurs with gene flow, there also need to be mechanisms that prevent the break down (due torecombination) of associations between traits causing selection against hybrids and the traits involved in pre-matingisolation (in this case between male display traits and female choice; Kirkpatrick and Ravigné, 2002; Gavrilets, 2004;Servedio et al., 2011). Thus, sexual selection through female mate choice is recognized as an important evolutionaryforce in the context of speciation, but there are several reasons for assuming that this force leads to speciation onlyunder a limited range of conditions.Sexual selection is driven not only through mate choice. Male contest competition over access to females orresources needed to attract females (i.e. breeding territories) is recognized as an important mechanism of sexualselection (Andersson, 1994). Male contest competition favors the evolution of a wide range of traits including weaponssuch as horns and spurs that are directly used in combat, sexual size dimorphism, and conspicuous body coloration andcalls that signal fighting ability. Many sexually selected traits have a dual function meaning that they are used both inmale contest competition and for female mate choice (Berglund et al., 1996; Wong and Candolin, 2005). In manymating systems, male contest competition overrides the effect of female choice and these two mechanisms of sexualselection can work in different or opposing directions (Qvarnström and Forsgren, 1998; Candolin, 2004; Hunt et al.,2009). Intensive male contest competition may even lead to evolution of traits that increases male mating success butreduces female fitness, which in turn may trigger an evolutionary arms race between the two sexes whereby femalesevolve counter adaptations (Arnqvist and Rowe, 2002). Thus, in a particular population, male contest competition overaccess to mates could be: a) the main mechanism of sexual selection, b) a mechanism that sets the stage for which traitsfunction as a target of female choice, or c) a mechanism that triggers a sexually antagonistic co-evolutionary arms-race.Still, the diversifying role of male contest competition has largely been ignored (but see e.g. Seehausen and Schluter,2004). The underlying reason for this ignorance is probably not the assumption that male contest competition is a lesspowerful mechanism of sexual selection than female mate choice. The strong focus on female choice is rather aconsequence of its intuitive role in causing assortative mating between diverging populations. Can male contestcompetition promote speciation while female choice for the same sexually selected character is absent or remainsunchanged? In this review we will argue that the answer to this question is yes.We will focus our discussion on four main aspects of male contest competition and speciation:1. Male contest competition and the evolution of novel traits.2. The link between ecology and male contest competition.3. Male contest competition and character displacement between populations.4. Male contest competition and reproductive isolation.3

QVARNSTRÖM A et al.: Male aggression and speciationWe conclude that sexual selection through male contest competition can play an important role in speciation. Basedon this and other conclusions (see below), we would like to encourage more studies focusing on male contestcompetition as a diversifying force and on the interaction between different mechanisms of sexual and natural selectionin the process of speciation rather than aiming at isolating their relative importance.2 Negative Frequency-dependent Selection and the Evolution of Novel TraitsSpeciation through sexual selection requires that at least one of the two splitting populations evolves a sexuallyselected trait that differs from the ancestral state. Many color patterns are largely affected by a relatively small numberof genes (Mallet, 1989; Grant and Grant, 1997; Hoekstra et al., 2006). Mutations in genes may frequently provide newphenotypic variation in coloration and hence potential new targets for sexual selection (Price, 2002; Hofreiter andSchöneberg, 2010; Manceau et al., 2011). Female choice may favor such new color patterns due to preexisting biases intheir sensory systems (Kirkpatrick, 1987), or through learning (Qvarnström et al., 2004). However, even if sensorybiases or learning can result in female mate choice in favor of novel traits, these mechanisms can hardly maintain stablepolymorphism. Stable trait polymorphism requires negative frequency-dependent selection, i.e. sexual selectionfavoring rare male phenotypes. There are some exceptional cases reported of female preferences for rare malephenotypes, e.g. in guppies (Farr, 1977) but rare phenotypes often suffer decreased mating success meaning that matechoice instead generates stabilizing sexual selection (Kirkpatrick and Nuismer, 2004). By contrast, male contestcompetition has been suggested to more often fulfill this requirement as males generally bias their aggression towardsrivals that are most similar to themselves since such males are most likely to share important resources (van Doorn et al.,2004; Mikami et al., 2004; Seehausen and Schluter, 2004, see Figure 1). This means that males with a rare new traitshould receive less aggression from other males and thereby experience an advantage when establishing breedingterritories. They are also less likely to become injured or to waste their time by fighting with other males instead ofcourting females (Huntingford and Turner, 1987). Thus, a bias in male aggression towards similar competitors has thepotential to facilitate both the invasion of a new trait into the population and to promote stable coexistence of differentphenotypes.Pioneering empirical work on the diversifying role of male contest competition through negative frequencydependentsexual selection has been done on African cichlids. The high diversity of haplochromine cichlids in LakeVictoria appears to originate from only a few ancestors less than 200 000 years ago (Nagl et al., 2000). Although theseyoung cichlid species have diverged ecologically (Bouton et al., 1997; Seehausen and Bouton, 1997), the fact that thereare striking differences in male nuptial coloration has lead to the conclusion that sexual selection has played a centralrole in this speciation process. Sibling species within genera, in fact, tend to be rather ecologically similar but stronglydifferent in male nuptial coloration (Seehausen and Schluter, 2004). While sexual selection through female choice hasbeen given much attention (e.g. Dominey, 1984; Seehausen and van Alphen, 1999; Knight and Turner, 2004), the roleof male aggressive interactions for access to mates and/or resources necessary to attract mates was suggested morerecently. Seehausen and Schluter (2004) examined the distribution of coloration in rock-dwelling haplochrominecichlids and found that the occurrence of species in habitat patches was negatively correlated with closely relatedspecies with similar color. Similar patterns of non-random distribution of males depending on their color pattern havebeen found in Lake Malawi (Young et al., 2009). Dijkstra et al. (2007) carried out aggression tests in response to blueand red phenotypes of the cichlid species complex Pundamilia (Figure 2). The male cichlid fish used in theseexperiments had been caught from three different types of wild populations. During the experimental trials, the wildcaughtfish were placed in a test aquarium and allowed to establish a territory. Territorial intrusions were then simulatedthrough placing two transparent watertight tubes containing one red and one blue intruder in the aquarium together withthe focal fish. The outcome of these trials differed depending on where the territorial fish had been caught in nature. As4

QVARNSTRÖM A et al.: Male aggression and speciationexpected, blue male Pundamalia cichlids from populations with either a continuous color morph distribution or with alack of intermediate forms displayed more aggressive behaviors towards intruders belonging to their own color morphthan to the other intruder. By contrast, blue male cichlids from a population with intermediate forms but without acontinuous distribution of color morphs biased their aggression towards red intruders. Why did not blue male cichlidsfrom this latter location also bias their aggression towards males belonging to their own color morph? The authorssuggested a possible explanation. Red male cichlids in general behave more aggressively than the blue ones and bluemale cichlids may therefore have learnt from previous experiences of interacting and competing with such aggressivered males. This explanation is based on the assumption that blue males from the three different populations hadexperienced different levels of previous competition with red color morphs depending on where they had been caught inthe wild. Dijkstra et al (2007) concluded that their results suggest that a new red morph should be able to invade a bluepopulation but that a stable coexistence of phenotypes would require additional mechanisms. Hence, social dominanceeffects and learning seem to play an important role in haplochromine cichlid fish (Dijkstra et al., 2007; Dijkstra andGroothuis, 2011) implying that the frequency-dependent selection caused by male contest competition often isasymmetric between sibling species. Thus, two important take home messages are that there may be intrinsicdifferences in aggressiveness between color morphs and that individuals may adjust their level of aggression towardsparticular color morphs depending on previous experiences.Experimental work on birds has yielded similar results, i.e. asymmetric color effects on winning contest competition.Recently, Pearce et al (2011) investigated the aggressive response to simulated territory intrusions in two competingspecies of birds. Male gouldian finches Erythrura gouldiae were found to be more aggressive towards conspecificintruders than towards heterospecific intruders and the red head-color morphs were more aggressive than the blackmorphs. By contrast, long tailed finches Poephilia acuticauda were more aggressive towards gouldian finches thantowards conspecific models. An intrinsic difference in aggression between the two species is therefore a likelyexplanation for why long-tailed finches have an advantage in competition over the limited nest sites needed to attractfemales (Brazil-Boast et al., 2011).The links between sexually selected traits, male aggressive behavior and competitive ability become even moreobvious when the sexually selected trait itself directly affects fighting ability and/or is used as a weapon, e.g. body sizeor horns and spurs. Should we then expect male contest competition to work in a unidirectional way with the mostaggressive males always getting access to most of the females? Intensive interactions between males in densepopulations may cause disruptive selection and favor males with alternative reproductive tactics, e.g. a competitiveversus a sneaker tactic (Figure 1). Such different tactics are generally associated with differences in whole suites ofmale traits associated with fighting ability including behavioral, morphological and physiological traits (Gross, 1996).A striking example is dung beetles that dig burrows underneath animal excrement in which they bury portions of thedung with eggs attached to them. The young will feed on the dung after emerging from the egg. How much dung theparents have put together for a male offspring will determine whether he will adopt a competitive or a sneaking tacticwhen reaching sexual maturity. This is because the size of the dung ball determines the adult size of the beetle and onlymales that have reached a certain threshold size will develop horns (Moczek and Emlen, 1999; Hunt and Simmons,2000). The horns are used in contest competition with other males and large horn size is associated with increasedreproductive success. Hornless males seek mating with females inside tunnels while avoiding aggressive interactionswith guarding males (Mozek and Emlen, 2000). The two reproductive tactics used by male dung beetles reflectphenotypic plasticity but may represent the first step towards genetically determined polymorphism. There are severalreported cases of genetically determined polymorphism (Zimmerer and Kallman, 1989; Shuster and Wade, 1991; Lank5

QVARNSTRÖM A et al.: Male aggression and speciationet al., 1995; Sinervo and Lively, 1996; Tuttle, 2003; Hurtado-Gonzales and Uy, 2009), which may in turn represent afirst step towards speciation.In conclusion, the role of male contest competition in promoting and maintaining variation among and betweenpopulations remains a modestly explored scientific area. Since aggression from competitors is considered to be onemajor cost associated with having many competitors with similar fighting ability, male contest competition may resultin disruptive selection favoring males with extreme strategies (i.e. often a dominant versus a sneaking strategy) andnegative frequency-dependent selection on discrete morphs. There are many possible directions for future research butwe would like to pinpoint three questions that we find particularly interesting. While it is intuitive that sexually selectedtraits directly used in combat (e.g. horns) are associated with dominant strategies, a remaining question is to what extentthere are pre-existing physiological biases making certain colors more likely to become associated with dominantstrategies (e.g. red color may be perceived as more threatening than blue color). Another unexplored area of research isto investigate the possible role of learning from previous interactions with competitors in reinforcing asymmetries inaggression and/or in the outcome of contests. Finally, more research aimed at revealing the costs and benefits associatedwith different strategies (i.e. including differences in whole suites of male traits that influence fighting ability orsneaking ability) and how these depend on the social and ecological environment is needed.3 The Ecological ContextStable co-existence between species is facilitated by differences in niche use. A relevant question then becomes howmay divergence in sexually selected traits used in male contest competition influence niche use and vice versa? Whenmale contest competition causes negative frequency-dependent selection, it will facilitate the maintenance ofpolymorphism with little divergence in niche use. Males with more different sexually selected traits will be able to usemore similar niches under sympatric conditions (see example of cichlids above).When divergence in traits used in male contest competition is associated with differences in aggression and/orfighting ability, this will also influence access to other resources. Aggressive interspecific interference has for examplebeen shown to drive divergence in habitat use by two species of land snails: Euhadra quaesita and E. peliomphala.Members of the less aggressive species, E. quaesita, are more terrestrial when they live in allopatry as compared towhen they live in sympatry with E. peliomphala (Kimura and Chiba, 2010). In general, when males fight over resourcesnecessary to attract females, the outcome of such contests often determines in what type of environment their offspringare being raised in. Habitat imprinting can then promote the association between competitive strategy and habitat useacross generations (see e.g. Vallin and Qvarnström 2011).An association between divergence in sexually selected traits used in male contest competition and divergence inniche use is also expected because the costs and benefits of using a dominant versus less competitive strategy shouldvary across ecological contexts. To understand population divergence in male traits used in contest competition overaccess to mates a wide range of costs associated with possessing such traits needs to be taken into account. Individualsin allopatric populations most likely experience different selective regimes due to differences in the ecological andsocial environment, which in turn result in differences in the adaptive optima of traits used in contest competition (Fig.3). It has been suggested that the level of sexual competition should be higher in stable and resource rich environmentswhile harsh environments limit sexual selection, which seems intuitive since there is a high cost of contest behavior(Briffa and Sneddon, 2007; Chellappa and Huntingford, 1989). However, under stressful conditions, where the lifeexpectancy is lower, an evolutionary switch to higher allocation of resources to increase reproductive success is alsoknown to occur (Birkhead et al., 1999; Polak and Starmer, 1998). Thus, it may be hard to predict the direction of theevolutionary response of traits involved in male contest competition in stressful environments.6

QVARNSTRÖM A et al.: Male aggression and speciationOne important stress factor that often varies considerably across both time and space is parasites. Aggressivebehavior is known to be associated with high testosterone levels (e.g. Martinez-Sanchis et al., 2003) and a majorphysiological cost of high testosterone levels is impaired immune function. Several elegant studies have been performedin specific populations. Testosterone implants have been shown to increase parasite infection in red grouse, for example(Mougeot et al., 2004, 2005). Elevated levels of testosterone may also result in higher exposure and transmission ofparasites through changes in behavior (Grear et al., 2009). Thus, aggressive behavior in itself may lead to higherexposure to parasites. In any case, the main prediction would be that high levels of parasites in the environment shouldselect for reduced levels of aggression.Another commonly discussed negative effect of secondary sexual traits, which is also likely to differ betweenenvironments and populations, is the increased risk of predation. Engagement in intrasexual contests has been shown toincrease predation risk (e.g. Jakobsson, 1995; Dunn, 2004), and thus, predation is assumed to limit both the degree ofintrasexual contest competition and the degree of intersexual signaling. The relationship between predation pressure andaggressive behaviour has recently been studied in Strawberry poison frogs Dendrobates pumilio. Populations of thisspecies in the Archipelago of Bocas del Toro in northwestern Panama have gained special attention because of theirgreat divergence in body color (Summers et al., 2003; Siddiqi et al., 2004) and because the color present in this speciesis shown to be involved in predator interactions (Summers and Clough, 2001; Saporito et al., 2007). Populations rangefrom cryptic to highly conspicuous (Wang, 2008, Fig. 2). Strawberry poison frogs show strong territoriality with highlevels of aggression (Pröhl, 2005) but the main focus in studies on interactions between natural and sexual selection inthis species has been directed to female mate choice (Summers et al. 1999; Reynolds and Fitzpatrick, 2007; Maan andCummings, 2008). Based on the hypothesis that coloration differences in D.pumilio reflect predation avoidancestrategies, Rudh et al (2011) argued that aposematic individuals should be relieved from the behavioral constraints thatcryptic individuals suffer and that the evolution of aposematic coloration could therefore be facilitated through the jointaction of natural and sexual selection. The authors suggest that due to the loss of aposematic coloration in thecryptically colored populations, the predation constraint on aggressive behavior is restored, which causes lower levelsof behaviors that affect exposure to predators. This idea was supported by the finding that males in more conspicuouspopulations of D.pumilio show higher levels of exposure while calling (Rudh et al., 2011). Male calling in this speciesserves both as an intersexual signal to attract females and as an intrasexual aggressive signal to defend territories. In astudy by Crothers et al (2011), males from an island population with aposematic red individuals were tested forintraspecific aggression. Using two-way experimental setups, the authors found that not only did more brightly coloredmales act more aggressively in general, but there was also a higher level of aggression directed towards males withartificially increased brightness. These findings suggest that even small differences in color stimuli may have significanteffects on male aggression levels. Rudh et al (manuscript) compared male-male aggression in several populations witheither cryptic or conspicuous individuals. Their results showed a higher level of aggression of individuals belonging toconspicuous populations than in individuals from cryptic populations.To conclude, there are many reasons why adaptation to different environments should commonly coincide withsome divergence in male contest competition ability and vice versa. Males using dominant strategies often behave moreaggressively, have higher testosterone levels and are in many cases larger than males using a sneaker strategy (Gross,1996). The costs and benefits associated with these various traits are known to vary across ecological contexts.Although costs associated with male contest competition are documented in the literature, surprisingly little researchhas been performed on how such costs influence population divergences and the build up of reproductive isolation.Examining how divergence in traits used in male contest competition influence the build up of reproductive isolationtherefore provides a major challenge for future studies.7

QVARNSTRÖM A et al.: Male aggression and speciation4 Male Contest Competition and Character DisplacementThe importance of disruptive selection caused by competition over limiting resources (Dieckmann and Doebeli,1999) is not limited to the situation of speciation under constant sympatric conditions. Since the development ofcomplete reproductive isolation is often a slow evolutionary process, many populations that start diverging in allopatryspend at least some time at secondary contact zones before they have developed complete reproductive isolation.Harmful interspecific interactions such as competition over mates and/or resources can be reduced by divergence inresource-use or in reproductive phenotypes, i.e. character displacement (Brown and Wilson, 1956). Characterdisplacement is often further divided into reproductive character displacement (character displacement in traitsassociated with reproduction) and ecological character displacement (character displacement in traits associated withresource use). As character displacement favors the evolution of novel resource use or reproductive traits, it can bothinitiate and finalize the speciation process and is potentially a leading cause of adaptive diversification (Pfennig andPfennig, 2009; Schluter, 2000). Displacement of reproductive characters through heterospecific competition betweenmales is likely when; a) the level of pre-mating isolation is low and males belonging to the two different populationscompete over females, b) females of both populations use the same types of resources for their reproduction, whichmales in turn compete over, or c) when there is misplaced aggression towards heterospecific males that resembleconspecific males and therefore are perceived as competitors (i.e. reproductive interference, Gröning and Hochkirch,2008). Character displacement at secondary contact is facilitated if the characters involved have already to some extentdiverged between the two populations in allopatry (Milligan, 1985; Schluter, 2000). Abundant standing variation alsopromotes character displacement (Pfennig and Pfennig, 2009), and further divergence in sympatry can then proceedrapidly as selection acts on phenotypes already present. Another general pattern is that the strength of selection to avoidreproductive interactions at secondary contact often differs between the two populations, resulting in asymmetriccharacter displacement. Such asymmetries can be interpreted as a trade-off between the benefits of avoidingcompetition with heterospecifics and the costs of having a displaced character (Cooley, 2007; Pfennig and Pfennig,2009).Several elegant studies have examined the role of male contest competition in driving reproductive characterdisplacement in damselflies. Male damselflies defend small mating territories close to open water (Alcock, 1987). Acompelling example of asymmetric reproductive character displacement driven by heterospecific male competition isthe wing spot of the damselfly Calopteyrx splendens The size of the wing spots are smaller in males belonging to C.splendens populations that are living in sympatry with the dominant C. virgo, which display higher levels of aggressiontowards C. splendens with large black spots (Tynkkynen et al., 2004; 2005; 2006; Fig. 2). Selection againsthybridization provides a non-mutually exclusive additional explanation for the observed pattern since wing colorationalso functions as a cue in mate choice (Svensson et al., 2007). Anderson and Grether (2010) focused on the effect ofcompetitor recognition failure in Hetaerina damselflies by manipulating conspecific intruders to resembleheterospecific males. This treatment lowered the aggressive response of territorial males in areas where suchheterospecific males naturally occurred, while no reduction in aggression was observed in allopatric sites. Theseexperiments imply an increased ability to avoid heterospecific aggression in sympatric populations. An excitingquestion is to what extent variation in competitor recognition (i.e. conspecific males) is a genetically determined trait orreflects learning. Since the relative species abundance changes within sites (Anderson and Grether 2010), learning fromprevious experiences is likely to be important.The relationship between reproductive character displacement and ecological divergence has recently beenexamined in a young Ficedula flycatcher hybrid zone. Collared flycatchers colonized the Swedish island of Öland in theBaltic Sea about 50 years ago and are now rapidly excluding their pied flycatcher predecessors from the preferred8

QVARNSTRÖM A et al.: Male aggression and speciationbreeding sites (Qvarnström et al., 2009). The main mechanism driving this exclusion is that young male pied flycatchersfail to establish breeding territories as the density of male collared flycatchers increases (Vallin et al., 2011a), resultingin a shift in the breeding habitats of pied flycatchers from deciduous forest towards mixed or coniferous forest (Vallin etal., 2011b). Because the peak in food abundance differs between habitats, the spatial segregation is paralleled by anincreased divergence in timing of breeding between the two species (Vallin et al., 2011b). Male pied flycatchers varyfrom black and white to brown and white throughout their range (Fig. 2), but the brown coloration is more common inareas where they co-occur with the black and white collared flycatchers (Drost, 1936; Roskaft and Järvi, 1992; Sætre etal., 1993; Alatalo et al., 1994; Huhta et al., 1997). Previous experiments have shown that interspecific aggression isrelaxed for browner male pied flycatchers (Král et al., 1988; Gustafsson and Pärt, 1991; Sætre et al., 1993), and brownmale pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition(Vallin et al., 2011b). Moreover, relatively brown male pied flycatchers were found to settle in habitats most differentfrom the ones defended by collared flycatchers and to breed relatively late (Vallin et al., 2011b). Thus, pied flycatcherswith the most divergent breeding strategy compared to collared flycatchers appear to be favored by selection in thehybrid zone. However, because divergent plumage characters promote local co-existence between the two flycatcherspecies, it increases the risk of hybridization in this young hybrid zone (Vallin et al., 2011b). The findings from thestudies on the Ficedula flycatchers lead to the idea that interspecific competition among males over resources necessaryto attract females (i.e. suitable nest sites in high quality habitat) may in general give rise to a feedback loop betweenecological divergence and reproductive character displacement (Fig. 4; Vallin et al., 2011b). This is because ecologicaldivergence in allopatry is likely to influence aggressive competitive abilities. At secondary contact, the subdominantspecies is displaced into a poorer habitat, which in turn leads to further divergence in competitive ability.In conclusion, although most studies of reproductive character displacement have focused on the role ofreinforcement, i.e. selection against hybridization driving divergence (Noor, 1995; Sætre et al., 1997; Nosil et al., 2003;Hoskin et al., 2005) there is an increasing awareness that other species interactions may also cause this pattern (Hoskinand Higgie, 2010). In particular, the importance of interspecific aggression is gaining increasing support (Seehausenand Schluter, 2004; Tynkkynen et al., 2004; 2005; Grether et al., 2009; Anderson and Grether, 2010, Vallin et al.,2011b). However, these two selective processes are not mutually exclusive and we would like to encourage futureresearch on their possible interaction.5 How Can Male Contest Competition over Mates Influence the Evolution ofReproductive Isolation?Speciation is defined as a split of one species into two or more new species that follow independent evolutionarypathways (Dobzhansky, 1935). In sexually reproducing organisms, the development of reproductive isolation is aprerequisite for the occurrence of this process. Therefore, finding out how population divergence through naturalselection, sexual selection and/or genetic drift leads to the build up of reproductive isolation lies at the heart of researchon the mechanisms of speciation. The two most straightforward pathways to population divergence driven by malecontest competition is that there is disruptive selection in sympatry i.e. hybrids receive a disproportionate amount ofattack from both species (Fig. 1), or divergence in allopatry caused by differences in the balance between the costs andbenefits associated with different male competitive tactics across different ecological conditions (Fig. 3). Since malecontest abilities often include a number of behavioral, morphological and physiological traits, there may be strongselection against hybrids and backcrossed individuals with mismatched trait combinations.9

QVARNSTRÖM A et al.: Male aggression and speciationThere are several potential evolutionary pathways to reproductive isolation when there is population divergence inmale traits associated with fighting abilities in resource based breeding systems. Apart from causing post-zygoticreproductive isolation through selection against hybrids, divergence in ability to compete over resources used to attractfemales can also lead to pre-zygotic reproductive isolation as a by-product, e.g. through displacement in habitat choice(e.g. Feder et al., 1994; Schluter, 2000) or breeding time (Théron and Combes,1995; Hendry and Day, 2005). Anexample of habitat segregation driven by male contest competition over nest sites is provided by the flycatcher examplementioned above. Habitat segregation has increased reproductive isolation between the two flycatcher species (Vallinand Qvarnström, 2011); male pied flycatchers that are displaced into the less preferred coniferous habitat are also lesslikely to hybridize. A cross-fostering experiment of nestlings and eggs between the two flycatcher species suggestedthat learned habitat choice further strengthens the barrier between the two species (Vallin and Qvarnström, 2011). Alink between divergence in coloration, level of aggression and segregation between calling and/or breeding sites hasbeen suggested to increase the likelihood of assortative mating in D. pumilio (Rudh et al., 2011). Thus, divergence intraits used in male contest competition can lead to both pre- and post- zygotic reproductive isolation and these traitsmay hence sometimes function as “magic traits” (Gavrilets, 2004; Servedio et al., 2011).Another pathway to reproductive isolation is if divergence in traits used in male contest competition is linked withdivergence in female choice based on these traits. There are several comprehensive review articles on the interactionbetween male contest competition and female choice in causing evolution through sexual selection (e.g. Berglund et al.,1996; Qvarnström and Forsgren, 1998; Wong and Candolin, 2005; Hunt et al., 2009). However, there has been a lack ofattempts to investigate how the interaction between these two mechanisms of sexual selection may influence thespeciation process. Below we outline a few possible scenarios, but we would like to emphasize that there is too littleresearch done in this field to draw major conclusions.In some species, e.g. with large sexual size dimorphism, male contest competition has the largest impact on pairingpatterns, leaving little or no scope for females to freely exert mate choice. Since the costs of heterospecific mating oftenare expected to be higher for females than for males, females should develop species recognition abilities faster thanmales (Wirtz, 1999). As a consequence, heterospecific pairings may be more common between young species whenfemales are unable to exert free choice. In resource based breeding systems, male competition often determines amongwhich males females can choose, e.g. making the two mechanisms of sexual selection work in a sequential manner. Ifmale competition results in a sorting of males of different species into different habitat types, it may facilitate femalechoice of conspecific males (e.g. Vallin and Qvanström, 2011).When both male competition and female choice occur (in sequence or in parallel), a relevant question becomeswhether the two mechanisms of sexual selection will work in the same direction on the male traits. As mentioned in theintroduction, female choice is generally assumed to operate in a unidirectional manner. Does this mean that femalechoice should act against population divergence in sexually selected traits? Divergence in traits used in contestcompetition could quickly lead to population assortative mating if sexual imprinting has a large impact on pairingpatterns. Sexual imprinting means that individuals learn characteristics of their parents that enable them to find asuitable mate during adulthood (e.g. Bateson, 1966; Clayton, 1993). One reason why sexual imprinting may play animportant role in speciation is that it works as a one-allele mechanism. The same allele in each of the divergedpopulations promotes assortative mating based on the traits that separate the two populations. This means thatdevelopment of assortative mating is not sensitive to gene flow (Irwin and Price, 1999; Servedio, 2009). However, thistype of one-allele mechanism cannot explain population divergence in the first place (Servedio, 2009), making thecombination of this mechanism and population divergence through male contest competition a particularly goodcandidate as an engine of speciation. Cross-fostering experiments using birds living in natural populations have shown10

QVARNSTRÖM A et al.: Male aggression and speciationthat exposure to heterospecific parents during the nestling stage may result in a sexual preference for heterospecificindividuals when adult (Harris, 1970; Fabricius, 1991), implying high importance for sexual imprinting in assortativemating under normal conditions. Recently, sexual imprinting was also found to promote assortative mating betweenbenthic and limnetic sticklebacks (Kozak et al., 2011).Intensive male contest competition may lead to the evolution of traits that increase male mating success but reducefemale fitness, which in turn may trigger an evolutionary arms race between the two sexes whereby females evolvecounter adaptations (Arnqvist and Rowe, 2002). Population divergence driven by such arms races may lead toreproductive isolation as a side effect. Sexual conflict is defined as a conflict between the evolutionary interests of thetwo sexes (Parker, 1979) and can be further classified into intra- or interlocus sexual conflicts. An intralocus sexualconflict arises when a particular allele increases fitness when expressed in individuals belonging to one of the two sexesbut decreases fitness when expressed in individuals belonging to the other sex (Rice and Chippendale, 2001). Aninterlocus sexual conflict arises when an adaptation in males causes reduced fitness in females and females respond byevolving counter-adaptations. This latter situation may result in co-evolutionary arms-races between the two sexesinvolving genes at different loci in each sex (Arnquist and Rowe, 2005). Genes underlying male traits used in contestcompetition over females are likely to reduce fitness when expressed in females. The inter-sexual genetic correlation forfitness may therefore be expected to be lower in species with more extreme sex-roles (Qvarnström et al., 2006). Anevolutionary solution to this situation is that genes underlying traits used in male contest competition, such as largebody size and horns, are only expressed in males resulting in pronounced phenotypic sexual dimorphisms. Evolutiondriven by male contest competition may also cause a number of inter-locus sexual conflicts. Apart from triggering tightintersexual co-evolutionary arms-races, increased adaptation to contest competition may occur at the expense of othertraits in males, such as reduced paternal care. Females may, in turn, be selected to reduce their litter/clutch size. Sexualconflict arising through adaptations related to male contest competition should be expected to cause fast evolutionarychanges in the genetic regulation of traits (reflected by sexual size dimorphisms) and in whole suites of traits in bothsexes. The likelihood of evolution of reproductive isolation between populations experiencing different levels of malecontest competition should therefore be relatively high. Theoretical modeling has shown that sexual conflict canpromote speciation by leading to fast changes in traits involved in reproduction such as egg-sperm proteins (e.g.Gavrilets, 2000), but there should be many more unexplored pathways to reproductive isolation driven by sexualconflict.The role of intrinsic genetic incompatibilities in the process of speciation is debated. This is because the evolutionof hybrid sterility is a slow process compared to the rate of speciation in several taxa (Price and Bouvier, 2002;Mendelson, 2003). Can male contest competition influence the speed by which genetic incompatibilities accumulate?Intrinsic sources of hybrid dysfunction are assumed to arise through epistatic interactions between genes from differentgenomes (Dobzhansky, 1940; Muller, 1940). A general pattern is that there is a greater fitness reduction in hybrids ofthe heterogametic sex, i.e. Haldane’s rule (Haldane, 1922). The faster male hypothesis builds on the idea that Haldane’srule is a consequence of intensive sexual selection on males leading to a faster incompatibility of male limited traits(Wu and Davies, 1993; Wu et al., 1996). These male traits are primary sexual traits and not secondary sexual traits suchas horns and spears that have a direct function in contest competition. However, investigating the role of male contestcompetition in driving divergence in male competitive tactics (which often also include differences in primary sexualtraits such as sperm characteristics) would be highly relevant. Recent developments in genomics and high-throughputtechnologies are opening novel possibilities to reveal links between divergence between natural populations and thebuild up of genetic incompatibilities (Rice et al., 2011).11

QVARNSTRÖM A et al.: Male aggression and speciationIn conclusion, there are many potential ways in which male contest competition can influence populationdivergence and the build up of reproductive isolation. For example, in resource based breeding systems, pre-zygoticisolation through habitat segregation may arise as a side effect of biases in male competitive abilities betweenpopulations. There are however also possible ways by which male contest competition can prevent pre-zygotic isolation.Male contest competition can sometimes limit female ability to choose conspecific mates. How the two mainmechanisms of sexual selection (i.e. male contest competition and female choice) interact during the speciation processin general remains a largely unexplored research area. We would also like to encourage future research on the role ofmale contest competition in the evolution of post-zygotic isolation. Aggression between males can lead directly toselection against hybrids if hybrids receive a disproportionate amount of attack by males of both parental species.Population divergence in traits used in male competition can also lead to selection against hybrids as side effects. Futureinvestigations of the relative importance of divergence in traits used in male contest compared to population divergencein other traits are needed if we want to understand the role of male competition in the speciation process.6 Conclusions and future prospectsThe whole speciation process, from the initial start of divergence between populations to the evolution of competereproductive isolation between them, often takes a very long time. Researchers interested in the mechanisms driving theprocess of speciation are therefore, based on the current stage of population divergence that they study, faced with theproblem of either having to predict the future and/or reconstruct history.The role of male contest competition in promoting and maintaining diversity remains a little explored scientific area.Most studies carried out so far have focused on the effects of male aggression towards similar competitors at earlystages of population divergence (Seehausen and Schluter, 2004; Dijkstra et al., 2006; Young et al., 2009). The majorconclusions are that aggression towards similar competitors may facilitate both the establishment of new color morphsand the maintenance of polymorphism. However, there are also possible ways by which such negative frequencydependentselection may prevent population divergence. It would, for example, promote successful immigration ofmales between populations that have started to diverge in allopatry, since rare phenotypes are favored. Thehomogenizing effects of gene flow could then prevent population differentiation (Mayr, 1963; Felsenstein, 1981; Coyneand Orr, 2004). Future studies on the effects of male aggression towards similar competitors at different stages ofpopulation divergence and under different geographical conditions are needed.As populations adapt to their environment, complexes of traits may change non-independently of each other, eitherdue to genetic correlations between these traits or because they have synergistic effects on fitness. The more traits thatdiverge between populations, the more likely is the build up of reproductive isolation between them (Nosil et al., 2009).One question that we raised here was how adaptation to different ecological environments coincides with divergence intraits used in male contest competition and vice versa. Since aggressive abilities are likely to trade-off against a numberof other crucial abilities such as parasite resistance, protection against predators and general stress tolerance, we expectwhole suites of traits to diverge non-randomly across populations experiencing different ecological environments. Wewould like to encourage more future studies examining how divergence in traits used in male contest competition, ascompared to other traits, influences the build up of reproductive isolation. However, the key to understanding the role ofmale contest competition in speciation probably lies in the examination of how the different selection pressures(including natural selection and the two main mechanisms of sexual selection) interact during the different stages ofpopulation divergence.When populations diverge in sympatry, harmful interspecific interactions such as competition over mates and/orresources can be reduced by divergence in resource-use or in reproductive phenotypes, i.e. character displacement12

QVARNSTRÖM A et al.: Male aggression and speciation(Brown and Wilson, 1956). The importance of interspecific aggression in driving character displacement is gainingincreasing support (Seehausen and Schluter, 2004; Tynkkynen et al., 2004; 2005; Grether et al., 2009; Anderson andGrether, 2010, Vallin et al., 2011b). One particularly interesting open research question is how character displacementthrough interspecific aggression influences reinforcement, i.e. selection against hybridization driving divergence inmating traits.Male contest competition over females (or over resources needed to attract females) can facilitate speciation bycausing direct selection against hybrids or by leading to fast population divergence, which in turn may lead toreproductive isolation as a side effect through a number of different pathways. However, we would also like to stressthat male aggression under certain conditions may also limit assortative mating and/or population divergence. In thisreview, we have outlined some examples of how sexual selection through male competition can influence speciation.There is plenty of empirical evidence showing that male contest competition can cause rapid evolutionary changes, buthow these evolutionary changes influence speciation remains surprisingly unexplored.Acknowledgements We would like to thank M. Servedio, A. Rice and three anonymous reviewers for constructive comments. Weare supported by the Swedish Research Council, the Royal Swedish Academy of Sciences and the European Research Foundation bygrants to AQ.ReferencesAlatalo RV, Gustafsson L, Lundberg A, 1994. Male coloration and species recognition in sympatric flycatchers. Proc. R. Soc. Lond. B. 256:113–118.Alcock J, 1987. The effects of experimental manipulation of resources on the behavior of two calopterygid damselflies that exhibit resource–defense polygyny. Can. J. Zool.-Rev. Canad. De Zool. 65: 2475–2482.Anderson CN, Grether GF, 2010. Interspecific aggression and character displacement of competitor recognition in Hetaerina damselflies.Proc. R. Soc. Lond. B. 277: 549–555.Andersson M, 1994. Sexual Selection. Princeton, NJ: Princeton University Press.Arnkvist G, Rowe L, 2002. Antagonistic coevolution between the sexes in a group of insects. Nature 415: 787–789.Arnqvist G, Rowe L, 2005. Sexual Conflict. Princeton, NJ: Princeton University Press.Bateson PPG, 1966. The characteristics and context of imprinting. Biol. Rev. 41: 177–220.Berenbaum M, 1983. Coumarins and caterpillars: A case for coevolution. Evolution 37: 163–179.Berglund A, Bisazza A, Pilastro A, 1996. Armaments and ornaments: An evolutionary explanation of traits of dual utility. Biol. J. Linn. Soc.58: 385–399.Birkhead TR, Martinez JG, Burke T, Froman DP, 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl.Proc. R. Soc. Lond. B. 266: 1759–1764.Bouton N, Seehausen O, van Alphen JJM, 1997. Resource partitioning among rock dwelling haplochromines (Pisces: Cichlidae) from LakeVictoria. Ecol. Freshw. Fish 6: 225–240.Brazil-Boast J, van Rooij E, Pryke SR, Griffith SC, 2011. Interference from Long-tailed finches constrains reproduction in the endangeredgoldian finch. J. Animal. Ecol. 80: 39–48.Briffa M, Sneddon LU, 2007. Physiological constraints on contest behaviour. Func. Ecol. 21: 627–637.Brown WL, Wilson EO, 1956. Character displacement. Syst. Zool. 5: 49–64.Butlin RK, 1995. Reinforcement: An idea evolving. Trends. Ecol. Evol. 10: 432–434.Candolin U, 2004. Opposing selection on a sexually dimorphic trait through female choice and male competition in a water boatman.Evolution 58; 1861–1864.13

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QVARNSTRÖM A et al.: Male aggression and speciationFig. 1 Disruptive selection in a continuous trait (Left) and relationship between male-male aggression and the frequency ofpre-existing color-morphs (Right)Due to high cost of male contest competition among the most common phenotypes (purple), extreme phenotypes (blue and red) are favored, changingthe population from a unimodal to a bimodal trait distribution. These color-morphs could have evolved either through disruptive selection of acontinuous trait (see left) or through a discrete phenotypic shift caused by e.g. a single mutation causing a change in coloration. The cost ofintrasexual antagonism is expected to be inverse to the frequency of a given color-morph if there is greater aggression among males of similarphenotypes. Such negative frequency-dependent selection predicts stable coexistence of two or more color morphs.19

QVARNSTRÖM A et al.: Male aggression and speciationFig. 2 Study systems where male aggression has been suggested to be involved in population divergence and speciationTop left: Pied flycatcher males. Left, black and white male. Right, Grey/brown male plumage coloration, which is more common and pronounced insympatry with the closely related collared flycatcher. This is likely due to less aggressive interactions with collared flycatchers. Photo credit JavierBlasco Zumeta. Top right: Red and blue morph of Lake Victoria Pundamilia cichlid fishes. Colour differences, and differences in local species- andcolour-morph composition affect male contest competition. Photo credit Peter Dijkstra. Bottom left: Damselflies in the genus Calopteryx showingvariation in wing dots involved in male expression of aggression. Photo credit Erik Svensson. Bottom right: Strawberry poison frogs from twopopulations with extremely different colour-morphs. Colouration co-varies with male-male aggression, which could be important, both as a possibledriver of phenotypic divergence, and through effects on reproductive isolation.20

QVARNSTRÖM A et al.: Male aggression and speciationFig. 3 Fitness effects and trait optima for a trait involved in male contest competition over matesSuggested fitness effects caused by natural (grey lines) and sexual selection (black lines) of a given trait value. The first graph shows a referencescenario of natural and sexual selection with the trait optima (0). The second and third graph each show two scenarios of changed fitness effectsthrough changed sexual and natural selection respectively. The second graph shows (A) a scenario where the level of the trait value does not alterfitness effects through sexual selection and (B) an increased benefit of a higher trait value. These situations could represent e.g. differences inpopulation densities where (A) low densities lead to male competition not affecting the reproductive success and (B) the opposite. The third graphshows scenarios of increased (C) and decreased (D) cost from a higher trait value, through natural selection. This situation could represent e.g.increased (C) or decreased (D) predation pressure on conspicuous behaviors or ornaments. Trait optima for each scenario are shown by arrows andcorresponding letters in the grey box.21

QVARNSTRÖM A et al.: Male aggression and speciationFig. 4 Feedback loop between reproductive character displacement and ecological character displacement at secondarycontact between two young species exhibiting male resource defence breeding systemsWhen allopatric populations experience different environments (a) some degree of asymmetry in male resource defence abilities is likely to evolve.At secondary contact (sympatry) such asymmetries in male resource defence abilities may facilitate reproductive character displacement and habitatsegregation (b), which in turn cause an increased asymmetry in male resource defence ability (c).22