When different populations experience different selective environments, they often diverge in traits that influence survival and reproductive success (Schluter, 2000). This adaptive population divergence often occurs in parallel for different lineages (e.g. species) arrayed across the same range of selective environments. That is, different lineages settle on similar adaptive solutions to the same spatial patterns of variation in selection. This parallel (or convergent) evolution in response to environmental gradients may be a general evolutionary principle given its prevalence at a variety of taxonomic scales (Harvey & Pagel, 1991; Jones et al., 1992; Schluter, 2000; Langerhans & DeWitt, 2004; Schluter et al., 2004). But to what extent does this principle also hold for males and females of the same species? The present paper outlines issues relevant to parallel evolution of the sexes, and then tests for its importance within a natural system.
Environmental gradients may impose divergent selection among populations in a manner that is broadly parallel for males and females. If so, the sexes might show similar patterns of population divergence, given that they also share the majority of their genome (Lande, 1980). All else being equal, the sexes might therefore exhibit parallel patterns of population divergence along environmental gradients. But all else is not equal. For example, males often exhibit exaggerated displays that enhance their competitive ability or attractiveness to mates (Andersson, 1994), whereas females often develop specialized morphologies for egg storage, egg laying or offspring provisioning. The sexes can also differ in behaviour, even outside of a reproductive context (Magurran & Maciás Garcia, 2000). For example, males and females can be spatially segregated, prefer different microhabitats, and use different food resources (Shine, 1989; Magurran, 1998; Temeles et al., 2000; Butler & Losos, 2002; Reimchen & Nosil, 2004). Critically from the perspective of parallel evolution, these differences in sexual selection, reproductive morphology, and behaviour may interact with environmental gradients. As one example, the more conspicuous mating displays of males than females may make males more susceptible to predation than are females (Magnhagen, 1991; Kotiaho et al., 1998; Quinn & Buck, 2001). In the case of such interactions, males and females may be subject to different spatial patterns of variation in selection along the same environmental gradients. If so, they may settle on different adaptive solutions: i.e. ‘nonparallel’, ‘sex-specific’, ‘independent’ or ‘unique’ population divergence.
Sex-specific aspects of population divergence may thus be the result of sex-specific divergent selection. They may also be the result of sex-biased dispersal, sex-specific plasticity or sexual niche partitioning. First, sex-biased dispersal might weaken population divergence for the sex with higher dispersal. For example, Moore & Hendry (2005) suggested that this phenomenon might explain sex-specific morphological clines in threespine stickleback, Gasterosteus aculeatus. Second, sex-specific plasticity (e.g. Robinson & Wilson, 1995) might enhance phenotypic divergence for the sex that matches the environment more precisely. This greater plasticity, however, might weaken divergent selection and therefore decrease genetically based phenotypic divergence along the same gradient (Price et al., 2003). Third, sexual niche partitioning may contribute to deviations from parallelism if competition between the sexes favours different forms of partitioning in different environments (Butler & Losos, 2002).
Few studies have explicitly examined parallel evolution of the sexes, but some have presented relevant data. As one example, Drosophila subobscura are distributed along broad latitudinal gradients in Europe, South America and North America (the latter two because of introductions). Gilchrist et al. (2004) found that both sexes show increases in body size with latitude on all continents, but that the trend in South America is weaker for males than for females. Weaker latitudinal clines in males than females have also been noted for houseflies, Musca domestica (Alves & Bélo, 2002). As another example, among-population variation in the body depth of breeding sockeye salmon (Oncorhynchus nerka) is negatively correlated with the intensity of bear predation, but the trend is stronger for males than for females (Quinn et al., 2001). As these examples illustrate (see also Brinsmead & Fox, 2002; Butler & Losos, 2002; Stuart-Fox et al., 2004), some aspects of population divergence can be shared between the sexes (parallelism) and some can be unique to each sex (independence). We here quantify the parallel and independent components of population divergence for male and female guppies (Poecilia reticulata) arrayed across environmental gradients.
Guppies are a live-bearing poeciliid fish native to Trinidad and parts of northern South America. Populations of this species are distributed across a well-studied predation gradient (reviews: Endler, 1995; Reznick & Travis, 1996; Houde, 1997; Magurran, 1998). Guppies at low elevations are typically exposed to strong predation from several fish species (‘high predation’), whereas guppies at high elevations are typically exposed to weak predation from few fish species (‘low predation’). Guppy populations in high- vs. low-predation environments have diverged in many traits, as illustrated by the following examples. High-predation guppies spend more time in shoals, inspect predators more carefully, swim faster, and are better at escaping predators (e.g. Magurran & Seghers, 1994a; O'Steen et al., 2002; Kelley & Magurran, 2003; Ghalambor et al., 2004). High-predation females mature earlier, have greater reproductive effort, and produce more but smaller offspring (e.g. Reznick & Endler, 1982; Reznick et al., 1996b). High-predation males are less colourful (Haskins et al., 1961; Endler, 1980; Millar et al., in press). All of these differences have a genetic basis and are adaptive, as revealed by common-garden experiments, laboratory predation experiments, and introductions in nature (see above citations).
In contrast to the above traits, population divergence in guppy body shape has received comparatively little attention. And yet, size and shape present excellent opportunities to test for parallel population divergence of the sexes. First, body size and shape influence swimming ability and therefore predation risk in fishes (e.g. Walker, 1997; Ghalambor et al., 2004; Langerhans et al., 2004). Second, guppies are sexually dimorphic for size and shape. For body size, females have indeterminate growth whereas males have largely determinant growth, leading to a larger size at maturity for females than males (Reznick, 1983). For body shape, females have increasingly distended abdomens as their young develop (Ghalambor et al., 2004). Third, males and females differ critically in behaviours that may influence selection on size and shape. For example, females spend most of their time feeding, whereas males spend most of their time courting and attempting to copulate with females (Magurran & Seghers, 1994b; Houde, 1997; Magurran, 1998). Also, males forage less on the benthos and are generally more mobile than females (Magurran, 1998; Croft et al., 2003).
As noted above, sex-specific divergent selection should arise from interactions between environmental gradients and sex-specific morphology or behaviour. These interactions appear likely for guppy size and shape in relation to predation. As one example, increasing abdomen distension in females decreases swimming performance (Ghalambor et al., 2004), which should increase mortality at high-predation sites. As another, males from high-predation, but not low-predation, sites prefer shallower water than do females when both are exposed to predation risk (Croft et al., 2004), which may then influence selection on shape imposed by hydrodynamics. The sexes also differ in overall predator-induced mortality rates, which may then alter the nature of selection on size and shape. Specifically, mortality in high-predation sites is greater for males than for females (Reznick et al., 1996a), perhaps because males spend less time in anti-predator behaviour and are more conspicuous than females (Endler, 1980; Magurran & Seghers, 1994b). Environmental gradients other than predation may also influence the evolution of guppy size and shape. Foremost among these gradients are canopy openness (Grether et al., 2001; Reznick et al., 2001), water flow (Nicoletto & Kodric-Brown, 1999) and stream size (Grether et al., 2001; Reznick et al., 2001). Like predation, these habitat features impose selection on size and shape that may differ between the sexes.
We studied 31 different sites across two Trinidadian watersheds. For each site, we characterized the predation regime (‘high’ vs. ‘low’) and quantified habitat features: canopy openness, water flow, water depth and stream width. We then used geometric morphometrics (Rohlf & Marcus, 1993) to quantify the size and shape of 715 females and 620 males from these sites. The parallel and independent aspects of population divergence were then assessed based on two complementary approaches. On the one hand, we used path models to determine the significance of factors influencing among-site variation in size and shape. On the other hand, we partitioned the total variation in size and shape (e.g. Langerhans & DeWitt, 2004) into (1) the effects of sex that are shared across environmental gradients, (2) the effects of environmental gradients that are shared between the sexes (parallel population divergence) and (3) the effects of environmental gradients that are unique to each sex (independent population divergence).