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The Evolution of Female Sex Pheromones

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The Evolution of Female Sex Pheromones Current Zoology 59 (4): 569–578, 2013 The evolution of female sex pheromones 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 se- lection) 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 phero- mone-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 fe- male 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, Received Apr. 8, 2013; accepted July 8, 2013. ∗ Corresponding author. E-mail: [email protected] © 2013 Current Zoology 570 Current Zoology Vol. 59 No. 4 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 con- specifics 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
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