- Top of page
Sexual isolation may arise when male mating traits and female preferences differ between species. Such divergence in mating traits is likely to occur when the strength or targets of sexual selection differ. Therefore, by comparing the traits under sexual selection in closely related species and the nature of preference for those traits, we can gain insight into when sexual selection contributes to sexual isolation and how it does so. Collecting these data is no easy undertaking. To simplify this comparison, I use the presence and extent of condition dependence in traits to determine whether directional sexual selection is acting on them. Condition dependence thus serves as a signature of sexual selection. I investigate differences in sexual selection on red nuptial colour in limnetic–benthic species pairs of three-spined sticklebacks. I evaluate condition dependence by comparing the strength of the relationship between colour and condition, and the magnitude of variance in red nuptial colour to other colour traits and to nonsexual traits. I find that limnetic males have strong condition-dependent expression of red nuptial colour whereas benthic males have at most weak condition-dependent expression. Ancestral anadromous males show no condition dependence. This suggests that colour is under strong directional sexual selection only in limnetics and that this is the derived state. Moreover, I find that the strength of female preference for red is related to the extent of condition dependence. The extent of condition dependence is also associated with the importance of colour differences to mate recognition. These results show that differences between these species in the action of sexual selection underlie their sexual isolation.
- Top of page
Sexual selection is thought to be involved in speciation, and there is a recent upsurge of interest in testing this idea. One of the first steps has been to investigate differences in male mating traits and female preferences between species and ask if those traits are involved in reproductive isolation. Evidence of this type is accumulating (Seehausen & van Alphen, 1999; Shaw, 2000; Boughman, 2001; Couldridge & Alexander, 2002; Masta & Maddison, 2002; Knight & Turner, 2004; Mendelson & Shaw, 2005), although counterexamples also exist (Price, 1998; Gage et al., 2002; Ritchie et al., 2005b). Implicit in this approach is that sexual selection is acting in a different way in species to cause differences in mating traits. This could occur if the mode of sexual selection varies from directional (with open-ended preferences) to stabilizing (with unimodal preferences). In addition, preferences may differ in their strength (Boughman, 2001), or in the values of a specific trait preferred by females (Endler & Houde, 1995; Wells & Henry, 1998; Uy & Borgia, 2000; Naisbit et al., 2001). The actual targets of preference may also differ, for example if one species focuses on colour and another on courtship behaviour. Any of these differences in sexual selection could cause divergence in mating traits, resulting in sexual isolation. Ultimately then, to assess the ability of sexual selection to drive speciation we need to know whether sexual selection operates differently between closely related species.
Yet, how can we do this? One promising approach is to find ‘signatures’ of sexual selection and compare those across populations or species. We can infer that sexual selection acts differently when species differ in the presence or magnitude of the signature. Sexual dimorphism has been used this way repeatedly to infer the action of sexual selection in speciation (Mitra et al., 1996; Price, 1998; Panhuis et al., 2001; Gage et al., 2002; Morrow et al., 2003; Gonzales Zuarth & Macias Garcia, 2006). Yet, sexual dimorphism is a fairly gross indicator that sexual selection is either present or absent in a species or clade. A potentially more sensitive signature of sexual selection is the degree of condition dependence in sexual traits. Variation in the extent of condition dependence should correlate with variation in how sexual selection is acting in a particular species. This is true because the action of sexual selection itself can generate condition dependence in male trait expression (Price et al., 1993; Iwasa & Pomiankowski, 1994; Rowe & Houle, 1996; Houle & Kondrashov, 2002). Patterns of condition dependence should be able to tell us not only whether sexual selection is acting, but also details of its how it plays out in a particular species; for example, whether it varies in strength, direction, or mode.
Condition dependence can be used this way because directional sexual selection is predicted to generate strong linear condition dependence in the male traits that are the focus of mate choice (Price et al., 1993; Iwasa & Pomiankowski, 1994; Rowe & Houle, 1996; Houle & Kondrashov, 2002); whereas stabilizing and disruptive sexual selection are not. Traits on which sexual selection is not acting should show little relationship between the trait and condition (Bonduriansky & Rowe, 2005). Traits under stabilizing sexual selection – when females prefer males with the mean value of a trait – should show either low condition dependence or a curvilinear relationship between the trait value and condition. Disruptive sexual selection can be caused by several processes, including alternative mating strategies, and should result in a weak or curvilinear relationship between a trait and condition, but with curvature in the opposite direction from that resulting from stabilizing sexual selection (Candolin, 1999). These expected relationships allow us to use the presence and shape of condition dependence to infer the presence of directional sexual selection. We can do this within a single species to compare several traits putatively under sexual selection. Those experiencing strong directional sexual selection are predicted to show high condition dependence whereas those experiencing no directional sexual selection are predicted to show low condition dependence (Wilkinson & Taper, 1999; Bonduriansky & Rowe, 2005).
The value of this approach for speciation studies is that the prediction should also hold when comparing the same trait between closely related species. If species differ in the extent of condition dependence for a trait, we can infer that they also differ in the strength of sexual selection on the trait, or in the nature of sexual selection (e.g. whether it is directional or stabilizing). Open-ended and unimodal preferences are likely to differ in their capacity to cause divergence in male mating traits (Ritchie, 1996; Price, 1998; Shaw & Herlihy, 2000), and therefore, the nature of preference has consequences for speciation via sexual selection. This approach investigates a particular kind of sexual selection, which is not to say that other kinds of sexual selection are not involved in the evolution of sexual isolation; only to test the role of directional sexual selection leading to condition dependence.
I use this approach to study the contribution of sexual selection to reproductive isolation in species pairs of limnetic and benthic three-spined sticklebacks (Gasterosteus spp.) in which male nuptial colour and female preference for colour differ (Ridgway & McPhail, 1984; Boughman, 2001). These are good biological species because they are isolated by strong premating and post-mating barriers and thus, have little gene flow. Sexual selection may have been especially important in the evolution of sexual isolation. The extent of difference in colour and preference between replicate populations of each species correlates to the degree of reproductive isolation between them, demonstrating that divergence in these traits does indeed contribute to reproductive isolation between the species (Boughman, 2001). In addition, reproductive isolation depends on different combinations of traits for the two species; body size and odour are paramount for benthics (Nagel & Schluter, 1998; Rafferty & Boughman, 2006) and a combination of colour and size for limnetics (Boughman et al., 2005). We know already that female limnetics have different colour preferences than female benthics. We also know that male limnetics have more colour than male benthics. The species also differ in size. Differences in colour, size, and preference suggest that sexual selection differs between species.
If the strength or mode of sexual selection on colour differs between limnetics and benthics, the extent of condition dependence is predicted to differ. Specifically, one predicts that limnetic males will have high condition-dependent expression of red nuptial colour because limnetic females have strong directional preference for red. In contrast, benthic males will have low condition-dependent expression because benthic females have weak or no preference for red. Obtaining mates which are currently in high condition is likely to benefit female sticklebacks directly because males provide all parental care. High condition males are more likely to survive the parental phase and have been shown to have a higher probability of successfully rearing offspring than low condition males (Candolin, 2000). They are also less likely to eat eggs (Manica, 2002). Females may also gain indirect benefits if high condition males carry good genes.
To test condition-dependent expression of red nuptial colour I test three primary predictions. I also test one prediction specific to its role in speciation. In each case I test predictions for condition dependence within each species, and then compare across species. The within-species comparisons allow me to determine whether red nuptial colour is in fact, condition dependent. The between-species comparisons allow me to determine whether sexual selection is acting differently in the species. To infer the direction of evolutionary change in condition dependence, I investigate condition-dependent expression of red nuptial colour in the ancestor, the anadromous three-spined stickleback (Gasterosteus aculeatus). This allows me to determine whether condition dependence has increased or decreased in the descendent species.
First, I test the prediction that traits under directional sexual selection will have higher condition dependence than traits that are not (Grafen, 1990; Price et al., 1993; Iwasa & Pomiankowski, 1994; Rowe & Houle, 1996; Houle & Kondrashov, 2002; Cotton et al., 2004). Therefore, to determine whether red nuptial colour is condition dependent in each species I compare the extent of condition dependence for red nuptial colour to nonsexual traits. I also compare red to other colour traits to assess the strength of sexual selection on each. Condition dependence has been shown to vary among traits in other taxa (Bonduriansky & Rowe, 2005), suggesting that sexual selection targets some of these traits and not others. Secondly, condition-dependent traits are expected to have higher phenotypic and genetic variance than traits that are not condition dependent through a process known as genic capture (Rowe & Houle, 1996). Essentially, when trait values depend on condition, genetic variance in condition translates into genetic variance in the male trait. To test this prediction, I compare the magnitude of phenotypic variance in red nuptial colour to other colour traits and to nonsexual traits. Thirdly, if female choice has been involved in the evolution of condition dependence, then the extent of condition dependence in the male trait should be related to the strength of female preference. Here, I test whether the extent of condition dependence in red nuptial colour is related to the strength of female preference for red. These three predications test whether red nuptial colour is condition dependent and whether it is under directional sexual selection in each species. Finally, if sexual isolation evolves from differences in sexual selection, then differences between species in the strength of sexual selection on a trait should be related to the trait's importance in sexual isolation. To test this prediction I ask whether differences in the importance of red nuptial colour in sexual isolation for sympatric pairs of limnetics and benthics are related to the extent of condition dependence.