The Evolution of Female Sex Pheromones

Current Zoology 59 (4): 569–578, 2013

Ally R. HARARI*, Hadass STEINITZ Department of Entomology, The Volcani Center, Bet Dagan, Israel

Abstract The role of female sex pheromones in natural selection, particularly as a means for species recognition to avoid the generation of hybrid offspring with low fitness, has been widely explored and is generally accepted by scholars. However, the significance of sex pheromones in shaping mate choice (sexual selection) and in competition over breeding resources (social selection) has been largely ignored. The effect of sexual selection on sex pheromones as a sexually dimorphic signaling trait has been discounted because the amount of pheromone released by females is typically minute, while the role of sex pheromones in competition over breeding resources (other than mates) has not yet been considered. As a result of natural selection, variation in sex pheromones among females is expected to be low, and males are not expected to choose their mates among pheromone-releasing conspecific females. Sexual selection, on the other hand, should drive the increase in pheromone variance among females, and males are expected to choose females based on this variation. Moreover, social selection resulting from more general social interactions, for example competition among females for breeding sites and food, should also promote variance among female sex pheromones. Here, we review the current evidence for each of the three selection processes acting on sex pheromones of female moths as an advertising trait. We suggest that the three selection types are not mutually exclusive but rather act together to promote different fitness components in diverse ecological situations [Current Zoology 59 (4): 569–578, 2013]. Keywords Sex pheromone, Natural selection, Sexual selection, Social selection, Competition, Mate choice

Pheromones are chemical signals produced by an or- when are used to attract mates, provide information ganism that can elicit, even in small quantities, a be- about the species and the gender of the signaler havioral or physiological response in another individual (Svensson, 1996; Johansson and Jones, 2007). However, of the same species (Wyatt, 2003). Pheromones may be the following questions about the nature of pheromones used for a variety of purposes. For example, phero- are still somewhat ambiguous. Are sex pheromones mones may be used to alert conspecifics of danger, as shaped by natural selection to prevent interspecific information for orientation and foraging (Holldobler et mating and the resulting production of hybrid offspring al., 2001), to aggregate in attempt of resource exploita- (Paterson, 1985; Löfstedt et al., 1991; Baker, 2002; Mas tion (Borden, 1989) and as a social or recognition cue and Jallon, 2005)? Did pheromones evolve via sexual for kin or familiar individuals (Penn and Potts, 1999; selection aimed at facilitating the competition for mates Brennan and Kendrick, 2006). Pheromones are also (Martin and Lopez, 2006; Harari et al., 2011)? Have sex used to attract or repel mates (for review, see Johansson pheromones evolved through social selection in the in- and Jones, 2007), to mark territories (for review, see traspecific competition over resources other than mates, Mason and Parker, 2010), and to advertise the status or such as direct competition for food and nest sites condition of the signaler (Olsson et al., 2003; Martin (Goekce et al., 2007; Harari et al., 2011; Tobias et al., and Lopez, 2006; Harari et al., 2011). In general, 2012)? Is it possible that sex pheromones are affected pheromones are communication tools used by many by all three kinds of selection (natural, sexual, and so- taxa to convey information among individuals of the cial), depending on the species and the environment? same species (Karlson and Luscher, 1959; Wyatt, 2003). The debate on the distinctions between the different Insects, in particular, have mastered the olfaction chan- selection mechanisms began with publication of The nel as a means for communication using volatile, task- Descent of Man, and Selection in Relation to Sex by specific substances. The properties of the pheromone Darwin (1871) and Darwinism by Wallace (1890). Ever allow for diverse information to be bounded to the re- since, the debate has not lost its passion (Endler, 1986; ceiver detecting and processing capabilities. Grafen, 1987; Andersson, 1994; Clutton-Brock, 2004; Researchers generally agree that sex pheromones, Lessells et al., 2006; Roughgarden et al., 2006; Carranza,

2009; Clutton-Brock, 2009; Shuker, 2010). Darwin 1871; Andersson, 1994; Shuker, 2010). Competition for himself addressed these difficulties by distinguishing ecological resources other than mates is attributed to between the effects of sexual selection from natural se- social selection (Tobias et al., 2012), and obtaining a lection (Darwin, 1871, page 257; and see Box 1). mate of the right species (Dobzhansky, 1937), is attribu- The evidence that females also have a say in adver- ted to natural selection. These three types of selection tising traits and in competition for mates has further are not mutually exclusive. On the contrary, they may complicated the view of the classic Darwinian mecha- all contribute to the shaping of female pheromones in nisms operating on sexual selection, namely male-male relation to the various ecological contexts. In all selec- competition and female choice (Darwin, 1871). As tion types, the fitness coin by which the success of the pointed out by Clutton-Brock (2009), females may be individuals is determined is the number or quality of subject to selection similar to that operating on males offspring they leave (Box 1, Table 1). under various ecological conditions, such as a female- 1 Female Sex Pheromones and biased operational sex ratio that generally promotes reversing sex roles either fully or partly (Vincent et al., Natural Selection 1992; Vepsalainen and Savolainen, 1995; Butchart, Pheromones may have evolved by natural selection 2000). when no benefit is expected by choosing a particular Besides its central role in reviving the field of sexual conspecific mate (i.e., absence of mate choice). selection, the natural/sexual/social selection debate is Dobzhansky (1937) postulated that natural selection acts important for understanding how repeated patterns in against hybrids through adaptive behavioral changes evolution arose in light of the variable selection pres- and sexual traits. As such, traits that avoid interspecific sures. The evolution of female ornaments is one bio- mismatched matings are shaped by natural selection logical pattern that is currently at the crux of the discus- because males and females of the same species have a sion, although similar traits in males are generally ac- mutual interest in nullifying the risk of producing no or cepted and are attributed to sexual selection (for review, infertile hybrid offspring (Paterson, 1985; Löfstedt et al., see Clutton-Brock, 2007, Clutton-Brock, 2009). 1991; Baker, 2002; Mas and Jallon, 2005). Accordingly, Here, we discuss the possible selection types operat- sex pheromones are expected to be under strong stabi- ing on female moth pheromones as a sexually dimorphic lizing selection to prevent changes in the exact signal secondary trait. In doing so, we adopt the suggestions of because slight deviations from the species code may Shuker (2010) and Tobias et al. (2012) to categorize the lead to interspecific mating. operating selection pressure based on the type of re- Evidence for natural selection operating on species- sources the organisms are competing for. Competition specific sex pheromones is scarce but does exist. As a over mates is attributed to sexual selection (Darwin, product of natural selection, differences in phero-

Box 1 Definitions

Darwin (1871) distinguished between two selection types that promote the evolution of phenotypic traits: (1) natural selection, which acts on characters that involve the "struggle for existence", and (2) sexual selection, which acts on characters in relation to competition for mates. West-Eberhard (1983) introduced a third type of selection (3), social selection, which acts on traits that promote the competition among conspecifics over resources that are not directly associated with mates. According to these definitions, sexual selection acts in the context of mate choice and competition over mates, social selection contributes to the evolution of traits in the context of competition for resources other than mates, and natural selection affects characters that involve solitary individuals or individuals in the solitary phase of their life cycle and traits that are not directly affected by competition with conspecifics. In the context of evolution of female sex pheromones, natural selection shapes the pheromone for species recognition (it stabilizes selection), sexual selection promotes differences in pheromone blend (mainly in the amount and ratio of components) among conspecific females, and social selection affects female perception (auto-detection) of the pheromone and behavior that increases reproductive success in the presence of competing females. The selection types are not mutually exclusive and may act simultaneously, reflecting pheromone plasticity in response to ecological constraints, resulting in pheromone plasticity in relation to ecological constraints. For example, the female sex pheromone of Heliothis viresence may change when the moth is sympatric with a closely related species (Groot et al., 2005), thereby responding to the pressures of natural selection. At the same time, the pheromone is costly to produce (Foster and Johnson, 2010) and thus can serve as an honest signal of female size and age, thereby responding to sexual selection.

HARARI AR, STEINITZ H: The evolution of female sex pheromones 571

Table 1 Examples of selection type, the affected trait, and the fitness gained Selection Species Character Fitness component Reference type Natural Bark beetles Pheromone plasticity Avoidance of hybrids Symonds and Elgar, 2004 Natural Hemileuca eglanterina (Lepidoptera) Pheromone plasticity Avoidance of hybrids Mcelfresh and Millar, 2001 Natural Lymantria monacha (Lepidoptera) Pheromone plasticity Avoidance of hybrids Gries et al., 2001 Natural Heliothis virescens (Lepidoptera) Pheromone plasticity Avoidance of hybrids Groot et al., 2005 Natural Drosophila serrate (Diptera) Pheromone plasticity Avoidance of hybrids Higgie et al., 2000 Sexual Lobesia botrana (Lepidoptera) Pheromone characteristics Honest advertisement Harari et al., 2011 Sexual Neoleucinodes elegantalis (Lepidoptera) Pheromone characteristics Honest advertisement Jaffe et al., 2007 Sexual Mamestra brassicae (Lepidoptera) Pheromone characteristics Honest advertisement Noldus and Potting, 1990 Sexual Heliothis zea (Lepidoptera) Pheromone characteristics Honest advertisement Raina et al., 1986 Palaniswamy and Sea- Sexual Choristoneura fumiferana (Lepidoptera) Calling behavior Competition for mates brook, 1985 Sexual Adoxophyes Sp (Lepidoptera) Calling behavior Competition for mates Noguchi and Tamaki, 1985 Sexual Homona magnanima (Lepidoptera) Calling behavior Competition for mates Noguchi and Tamaki, 1985 Palanaswamy and Sea- Social Choristoneura fumiferana (Lepidoptera) Egg laying Competition for resources brook, 1978 Social Choristoneura rosaceana (Lepidoptera) Egg laying Competition for resources Goekce et al., 2007 Social Lobesia botrana (Lepidoptera) Egg laying Competition for resources Harari et al., 2011 mone characteristics in related sympatric species, such sent (in Bohemia, the Czech Republic) (Gries et al., as those sharing geographical zones or the same host 2001). In their influential studies, Groot and her col- species, are expected. In bark beetles, the most pro- leagues (2005; 2006; 2007; 2009) found temporal varia- nounced differences in the pheromone blends have been tion in the pheromone blend of Heliothis virescens and found among the most closely related beetles in each H. subflexa, suggesting that the pheromone composi- genus (Symonds and Elgar, 2004). Similarly, species tion may be altered based on the female experience from species-rich moth families tend to have more concerning the risk of mating mistakes in sympatric components in their female-released pheromone blend populations and the risk of sexual harassment by Heli- than do species from species-poor families, allowing for coverpa zea males. a larger number of unique blends (Byers, 2006). It is An additional mechanism that may have evolved to useful to consider species that occur in allopatric and reduce interspecific matings is the development of spe- sympatric populations with close relatives. For example, cific chemical receptors that have higher affinity to females of the sheep moths Hemileuca eglanterina and components in the pheromone of a sympatric sister spe- H. nuttalli in allopatry produce the same active com- cies. Adding these components to the otherwise typical pound in their sex pheromone blend (acetate ester). species-specific sex pheromone often reduces male at- When these species are sympatric, H. eglanterina fe- traction to the female (Löfstedt, 1990; Löfstedt et al., males do not produce this component, and H. eg- 1990). lanterina males actively avoid females, which retain this Phelan and Baker (1987) supported the view that sex component in their pheromone blend (Mcelfresh and pheromones have an adaptive role in preventing mating Millar, 2001). Another example is provided by the fruit mistakes. They demonstrated that pheromone-releasing fly Drosophila birchii and D. serrata (Higgie et al., organs in males are more common in closely related 2000). The sex pheromone blend (cuticular hydrocar- species, sharing the same host, than in species in distinct bons) of D. serrata is plastic and differs when in sym- populations. Tortricid moths, for example, lack phero- patry or allopatry with D. birchii. The pheromone blend mone-emitting organs, and only a small portion of this of allopatric D. serrata was altered after breeding for moth family shows host overlap. nine generations in the vicinity of D. birchii. When functioning to prevent mistakes in mating, sex For the forest defoliator nun moth Lymantria pheromones are expected to be under stabilizing selec- monacha, the ratio of the female sex pheromone com- tion (Löfstedt, 1993; Linn and Roelofs, 1995; Butlin and ponents and time of activity are different when its close Trickett, 1997; Phelan, 1997; Zhu et al., 1997; Shaw and relative L. fumida is present (in Honshu, Japan) vs. ab- Parsons, 2002). Indeed, females of the European corn

572 Current Zoology Vol. 59 No. 4 borer moth Ostrinia nubilalis produce two types of sex according to their part in mate choice with respect to pheromone blends that differ only in the ratio of the two species recognition, mate recognition, and mate assess- major components (Linn et al., 1997). As a result, males ment. The first two categories, choice of the correct of one population are less attractive to females in the species and mating status, do not take part in the com- other population (Liu and Haynes, 1994; Linn et al., petition for mates per se, and we have discussed them in 1997; Zhu et al., 1997). Restricted male response to a the current review as part of natural selection (see change in a female pheromone blend was also demon- above). Regarding pheromone-based mate assessment, strated in other species (Löfstedt, 1990; Linn and Table 2 in Johansson and Jones (2007) lists 21 species Roelofs, 1995; Zhu et al., 1997). These findings, how- in which males advertise their quality (fluctuating ever, are in contrast with other studies that demonstrate asymmetry, major histocompatibility complex, immuno- individual variation in female sex pheromones in a competence, competitive ability, aggressiveness, domi- population, both in the quantity and the ratio of compo- nance, and attractiveness) but only two species in which nents (Collins and Cardé, 1985; Witzgall and Frérot, females signal their condition (age and size) through 1989; Löfstedt, 1990; Jaffe et al., 2007; Harari et al., sex-specific pheromones: the copepod Tigriopus ja- 2011). Furthermore, contrary to the prediction evoked ponicus (Ting et al., 2000), and the snake Thamnophis by natural selection, males often respond to a wide array sirtalis (Lemaster and Mason, 2002). of the sex-specific pheromone blends (Löfstedt, 1990; Johansson and Jones (2007) attribute the dearth of Linn and Roelofs, 1995; Roelofs et al., 2002). studies demonstrating the use of sex pheromones as The latter findings, which counter the view that sex advertising traits by female moths to the minute amount pheromones are highly conserved, have led to the in- of sex pheromone typically released (El-Sayed, 2010) ference that changes in pheromone characteristics and its low cost of production (Cardé and Baker, 1984; (within an individual life time and at the population Kokko and Wong, 2007), thus, "…seems an unlikely level) can influence mate choice. Hence, the concept of result if they were subject to mate choice" (Johansson sex pheromones as a secondary trait that is shaped by and Jones, 2007, page 257). Johansson and Jones agree sexual selection has been increasingly considered with the general view that females signal to males when (Johansson and Jones, 2007). the cost of advertising is low, while males signal to fe- 2 Female Sex Pheromones and Sexual males when the cost of advertising is high (Greenfield, 1981; Svensson, 1996; Landolt and Phillips, 1997; Selection Johansson and Jones, 2007). According to this line of According to the broad definition of sexual selection reasoning, female sex pheromones cannot serve as sec- (Andersson, 1994; Shuker, 2010; Tobias et al., 2012), a ondary, extravagant traits that reveal female quality be- sexually selected trait is one that influences intraspecific cause a substantial cost of the trait or of its maintenance competition for mates. This includes competition for the is a prerequisite of honest advertising (Zahavi, 1977; number or quality of mates and for resources that di- Kotiaho, 2000, 2001, 2002). rectly influence the probability of mating. Although the In general, the elaborate traits of females have at- role of chemical signals in sexual selection was first tracted considerably less research attention than those of suggested by Darwin (1871) (Box 1), sex pheromones males (Amundsen, 2000), although the females of many were not often recognized as traits that affecting compe- species do have such traits (Andersson, 1994; Clutton- tition for mates. In his book Sexual Selection, Andersson Brock, 2004; Kraaijeveld et al., 2007). The origin of this (1994) cited less than a handful studies on phero- research bias lays at the feet of Darwin, who suggested mone-mediated mate choice. Similarly, in their review that female secondary traits are derived from the showy of the various ecological, behavioral, and biochemical secondary traits of males (Darwin, 1871; Lande, 1980). aspects of hydrocarbons in insects, Howard and Blom- In the last decade, accumulating research has demon- quist (2005) did not consider the role of hydrocarbons in strated that, like the ornaments of males, those of fe- sexual selection. males may have been selected by female-female compe- More recently, Johansson and Jones (2007) have ad- tition over mates and by male choice of females, i.e., by dressed the challenge to review the rapidly increasing sexual selection (see examples in Clutton-Brock, 2007, number of studies concerning the role of sexual selec- 2009; Rosvall, 2011; Tobias et al., 2012). tion in shaping sex pheromones (Johansson and Jones, Competition among females for mates is expected 2007, Page 265). They categorized sex pheromones when male quality varies and when the operational sex

HARARI AR, STEINITZ H: The evolution of female sex pheromones 573 ratio is female-biased. Evidence from non-pheromone (as suggested by Atema 1986 and demonstrated by Jaffe signals is plentiful (see Rosvall, 2011). In the case of the et al. 2007 and Harari et al. 2011). That pheromones deep-snouted pipefish Syngnathus typhle, for example, advertise female quality is often demonstrated by quan- females compete for mates, displaying their ornamenta- tifying the cost of advertising (Foster and Johnson, 2011; tion to establish a dominance hierarchy, and males con- Harari et al., 2011). Quantity and ratio of components in sider the female hierarchy when choosing their mates the female moth sex pheromone may reveal female size (Berglund and Rosenqvist, 2001). Similarly, female age (Jaffe et al., 2007; Harari et al., 2011) and age (Miller in the pinyon jay Gymnorhinus cyanocephalus is corre- and Roelofs, 1980; Raina et al., 1986; Noldus and Pot- lated with malar and head coloration, which are used to ting, 1990). Cost of pheromone production was behav- assess dominance in female competition for mates iorally demonstrated, i.e., mortality rates were higher (Johnson, 1988). and fecundity was lower for females that released Accepting that sex pheromones function as secon- pheromones than for those that did not (Foster, 2009; dary traits subject to sexual selection (Darwin, 1871; Harari et al., 2011). There is also evidence that females Andersson, 1994; Shuker, 2010), one can make three investing in resistance to insecticides produce reduced predictions. First, females vary in the trait under selec- amounts of pheromones (Campanhola et al., 1991; tion (i.e., the emitted pheromone). Second, females Delisle and Vincent, 2002), indicating a high metabolic compete for mates, advertising their quality via the sex cost of pheromone production (Foster, 2005, 2009; pheromone. Third, males are influenced by the message Foster and Johnson, 2010). conveyed through the pheromone. Concerning the first Female advertising and male mate choice are pre- prediction, individual variation in pheromone characteri- dicted when mating is costly for males (Zahavi, 1977; stics (i.e., the amount and ratio of components) has been Kokko and Monaghan, 2001; Byrne and Rice, 2006), documented for several insect species (e.g., for bark which is often associated with female phenotypic varia- beetles: Birgersson et al., 1988; and for moths: Miller tion (Harari et al., 1999; Kvarnemo and Simmons, 1999; and Roelofs, 1980; Haynes et al., 1984; Safonkin and Jaffe et al., 2007; Harari et al., 2011) and female-biased Bykov, 2006). The variations may include the overall sex ratios (Parker, 1983; Owens and Thompson, 1994; amount of the pheromone and/or a different ratio of the Johnstone et al., 1996). Mating cost for males may in- components in the pheromone blend (Collins and Cardé, clude energetic courtship displays (Segoli et al., 2006), 1985; Witzgall and Frérot, 1989; Löfstedt, 1990; presenting the females with nutritive nuptial gifts Svensson et al., 1997; Jaffe et al., 2007; Harari et al., (Thornhill, 1980; Dewsbury, 1982), intense intrasexual 2011). competition for mates (Bonduriansky and Brooks, 1999; Concerning the second prediction, there is evidence Fromhage and Schneider, 2005), and in the case of all that female moths use female sex pheromones to com- moth species, limited sperm supply (Friedlander et al., pete for mates. For example, females increased calling 2005; Teng and Zhang, 2009). behavior when they sensed pheromones released by In species in which females have multiple mates, conspecific females (Palaniswamy and Seabrook, 1985; sperm competition may affect the reproductive output Stelinski et al., 2006). These females may be attempting of the males. If the pheromone signals the female re- to attract early mate-searching males. Females of other productive state, males may allocate resources, increas- moth species delay calling when exposed to conspecific ing their reproductive potential accordingly. Males of pheromone (Noguchi and Tamaki, 1985; Weissling and the white widow spider, Latrodectus pallidus, for exam- Knight, 1996). These and other examples suggest that ple, performed a significantly shorter display when ap- female calling alters the calling of other conspecific proaching mated females because the risk of cannibali- females and that such changes may affect future repro- sm is considerably reduced (Harari et al., 2009). Addi- ductive success (Goekce et al., 2007; Yang et al., 2009). tionally, the amount of sperm that male moths transfer As is the case for other extravagant traits (Zahavi, to females is correlated with female mating experience 1977), female sex pheromones are expected to honestly and age (Wedell and Cook, 1999; Teng and Zhang, reveal the signaler’s physiological state through rapid 2009). changes in the quality and quantity of their pheromone As opposed to males of most other taxa, male moths (Aliniazee and Stafford, 1971; Webster and Cardé, 1982; stop producing fertile sperm in the pupal stage (Fried- Liu and Haynes, 1994). Thus, the signal should allow lander et al., 2005). As a consequence, sperm reserves males to discriminate among females for reproduction are diminished after each copulation, and the potential

574 Current Zoology Vol. 59 No. 4 number of females that can be inseminated is limited schistus microps, for example, exhibit antagonistic be- (Callahan and Cascio, 1963; Friedlander et al., 2005; havior at sites with a shortage of nests (Borg et al., Teng and Zhang, 2009). In addition, females suffer re- 2002), and only winners of aggressive interactions be- duced reproductive success after mating with experi- tween individuals of the parasitoid Pachycrepoideus enced, polygynous males (Torres-Vila and Jennions, vindemmiae gain access to oviposition sites (Goubault 2005; Lauwers and Van Dyck, 2006; Marcotte et al., et al., 2007). 2006) and thus may discriminate against them. Indeed, Like morphological and behavioural traits, sex males prefer larger, more fecund females (Torres-Vila et pheromones may play a role in intrasexual competition al., 2002), as indicated by the features of the pheromone over breeding resources. Females can detect their air- emitted by the female (Jaffe et al., 2007; Foster and borne species specific pheromone (Palanaswamy and Johnson, 2011; Harari et al., 2011). Seabrook, 1978; Noguchi and Tamaki, 1985; Goekce 3 Female Sex Pheromones and Social et al., 2007). There is evidence that the release of pheromone by females affects the oviposition of con- Selection specific females. Exposure of the female to the sex The currently understood definitions of natural selec- pheromone of its own species stimulates oviposition for tion and sexual selection (Darwin, 1871; Andersson, some moth species, e.g., Choristoneura fumiferana; 1994; Shuker, 2010) leave some behaviors in a grey area. (Palanaswamy and Seabrook, 1978) but deters oviposi- Males and females may differ in their struggle for in- tion by other moth species (Palanaswamy and Seabrook, creased reproductive success. In general, males compete 1978; Goekce et al., 2007; Harari et al., 2011). In both for access to females, while females compete for access cases, mated females compete for oviposition sites. The to resources (Rubenstein, 2012; Tobias et al., 2012). airborne pheromone released by the female provides Although both males and females often use ornaments information about the signaler’s physical condition to achieve higher fecundity, male extravagant traits are (Jaffe et al., 2007; Foster, 2009; Harari et al., 2011) and used to obtain mates directly (e.g., through male-male thus provides information about the forthcoming inten- fighting) or indirectly (e.g., by defending territory), sity of offspring competition for food. This behavior is while females traits are often used to obtain resources similar to female competition at time of pregnancy or other than mates (e.g., food patches and nest sites) that maternal care (Wolff and Peterson, 1998; Rodel et al., are needed for offspring welfare after competition over 2008). mates has ended successfully (Carranza, 2009; Clutton- 4 Summary Brock, 2009). Tobias et al. (2012) followed West- Eberhard (1983) in suggesting that intraspecific compe- Substantial evidence indicates that sex pheromones tition for resources other than mates represents a diffe- in general and female-produced sex pheromones in par- rent form of selection that they termed social selection. ticular function as secondary (signaling) traits. The na- In this context, signaling traits (e.g., ornaments, weap- ture of the selection acting on the female trait should be ons, elaborate displays) may be involved in direct or defined in terms of the resource being competed for. indirect competition for resources other than mates or The definition of the operative selection pressure is not used in non-sexual contests (Moore et al., 1997; Wolf et simply semantic but is relevant to the trait’s potential al., 1999; Mcglothlin et al., 2010; Rosvall, 2011) and adaptive (or non-adaptive) significance. As demon- yet still provide relevant information about the signaler. strated in this review, the female sex pheromone is an One such example of a socially selected trait is the adaptive trait that is moulded by three selection pres- horn of the female dung beetle. The female dung beetle sures: natural, sexual, and social selection. Natural se- uses its horn in intrasexual competition for breeding lection acts on species recognition and reduces the resources (Watson and Simmons, 2010) which affects probability of mismatched matings. Sexual selection the number and quality of surviving offspring. Another acts through female intraspecific competition for mates example may include competition by tropical streak- and male choice of females (although mutual choice is backed orioles for foraging territory during breeding also possible because females still heavily invest in the and non-breeding seasons (Murphy et al., 2009). Fe- offspring). In social selection, females use the trait to males may also benefit from aggressive behavior toward compete against conspecific females for ecological re- conspecific females when breeding opportunities are sources. The contribution of social selection to evolu- costly to find. Females of the common goby Pomato- tion of the female sex pheromone as a signaling trait is

HARARI AR, STEINITZ H: The evolution of female sex pheromones 575 difficult to assess because the evolution of pheromones over attractive females. Behav. Ecol. 12(4): 402–406. has been traditionally attributed to either natural selec- Birgersson G, Schlyter F, Bergstrom G, Lofqvist J, 1988. indivi- tion or sexual selection. However, recent papers demon- dual variation in aggregation pheromone content of the bark beetle Ips typographus. J. Chem. Ecol. 14(9): 1737–1761. strate that female moths use sex pheromones to adver- Bonduriansky R, Brooks RJ, 1999. Why do male antler flies Pro- tise their reproductive potential, and that males use this topiophila litigata fight? The role of male combat in the struc- information when choosing females as mates. Thus, it is ture of mating aggregations on moose antlers. Ethol. Ecol. not unreasonable to hypothesize that female sex phero- Evol. 11(3): 287–301. mones provide information about the intensity of the Borden JH, 1989. Semiochemicals and bark beetle populations: impending competition among offspring for essential Exploitation of Natural phenomena by pest management strategists. Ecography 12(4): 501. resources. There is growing evidence that females can Borg AA, Forsgren E, Magnhagen C, 2002. Plastic sex-roles in detect airborne, species-specific pheromone produced the common goby: The effect of nest availability. Oikos 98(1): by conspecific females and use the information to com- 105. pete for resources or take flight in a search for resources Brennan PA, Kendrick KM, 2006. Mammalian social odours: elsewhere. Attraction and individual recognition. Philos. Trans. R. Soc. B. 361(1476): 2061–2078. It is interesting and perhaps initially perplexing that Butchart SHM, 2000. Population structure and breeding system of the exact same trait, the female sex pheromone, may be the sex-role reversed, polyandrous bronze-winged jacana subjected to three different selection pressures. Moreo- Metopidius indicus. 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