Even though male sexual ornaments are well documented in many species (Jennions & Petrie, 1997), their adaptive significance for males and signalling value for females remains a subject for considerable debate (Houle & Kondrashov, 2002; Kokko et al., 2003). Although there is significant interest in showing that sexually selected male ornaments indicate heritable genetic quality, the evidence that such indirect benefits can outweigh the direct costs of choosing or of mating with males is equivocal (Cameron et al., 2003; Kokko et al., 2003). Several recent reviews have underscored the need for more empirical work on the ultimate causes of choice and consequent dimorphisms that arise through sexual selection (Chapman et al., 2003; Kokko et al., 2003; Pizzari & Snook, 2003).
One particularly promising avenue of research concerns investigations of the relatively rare systems featuring elaborate ornaments in females (Kokko & Johnstone, 2002), in part because the balance of direct and indirect benefits available through mate choice is significantly different for males compared with that of females (Bonduriansky, 2001). Whereas in many species males provide very little direct investment in offspring production, the minimum investment by females is still substantial: the size and quality of the eggs themselves. This level of investment in offspring may be enough to constrain the evolution of elaborate female ornaments in most species, because females that invest in ornaments at the expense of offspring lose direct fitness, and males should prefer to mate with females that invest in offspring rather than ornaments (Fitzpatrick et al., 1995; Berglund et al., 1997).
Given the potential trade-off between offspring and ornaments, why are females of some species elaborately ornamented? One possibility is that ornamentation has evolved because such a trade-off is resolved through the investment of different kinds of resources in ornaments as opposed to offspring (Fitzpatrick et al., 1995). An alternative view (Chenoweth & Blows, 2005; Chenoweth et al., 2006) is that a resource trade-off between ornamentation and offspring does not prevent the evolution of female ornaments in some species for which direct assessment of females is difficult, e.g. in mating swarms. If ornaments have arisen as a signal of fecundity to males, Chenoweth et al. (2006) predict stabilizing selection on ornament expression, such that males mate females with intermediate investment in ornaments over those that invest so heavily in ornaments that they incur a fecundity cost. Finally, female ornaments that impair fecundity could also evolve in spite of male interests if they are favoured by nonsexual selection (Heinsohn et al., 2005; LeBas, 2006). In these cases, the signalling value of the ornament in other contexts would presumably offset fecundity costs, and male choice for ornamentation could arise as an adaptation to reap the benefits of these signals, or maladaptively if the males are caught in a sensory trap that causes them to favour ornamented females in spite of their reduced fecundity (Heinsohn et al., 2005; LeBas, 2006).
Whether or not they involve conspicuous ornamentation, the evolution of sexual dimorphisms requires that selection on morphology is different across the sexes (Lande, 1980). Few studies have attempted to measure selection on the same traits across the sexes in any species (Chenoweth & Blows, 2005), much less in species showing sex role reversal (but see Kraaijeveld et al., 2007 for a review of empirical studies examining the causes of ornamentation in both males and females of a species). Dance flies (Diptera: Empididae) are well suited for this research (LeBas et al., 2003). Within the subfamily Empidinae, in particular, there is considerable variation in both mating system and the level of female ornamentation of wings, legs and abdomens (Downes, 1970; Svensson & Petersson, 1987; Cumming, 1994; Svensson, 1997). Cumming (1994) has estimated that 28% of almost 600 identified species within the related Empidine genera Empis and Rhamphomyia show some form of female ornamentation, including wing colouration (Svensson, 1997), exaggerated wing size (Svensson & Petersson, 1987), pinnate scales on female tibiae (LeBas et al., 2003) and in some cases elaborate eversible pleural sacs on the abdomen (Funk & Tallamy, 2000). Female ornamentation appears to have resulted from sexual selection in the context of female competition for ‘nuptial gifts’ of prey (Cumming, 1994); mating is thought to be the only occasion for female empidines to acquire dietary protein as adults (Downes, 1970; Cumming, 1994).
Mating opportunities for females of the long-tailed dance fly, Rhamphomyia longicauda are particularly limited as the swarms where matings originate convene for less than an hour just after dawn and just before dusk. Swarms consist predominantly of females flying up to two metres above the ground in gaps in the tree canopy along rivers (Newkirk, 1970). Sexually competitive females in these swarms possess large pleural sacs, enlarged wings and pinnate tibial scales; mating behaviour appears to be sex role-reversed (Funk & Tallamy, 2000). Females within the swarms compete for access to the male nuptial gifts provided during mating. The sexually dimorphic abdomens, wings and legs of this species probably exaggerate female size to males that ascend from below, presumably to assess the fecundity of females above them silhouetted against the light in canopy gaps. Funk & Tallamy (2000) demonstrated that choosy males favoured larger silhouette models in the swarm, and argued that the female traits disguised female fecundity to some degree, and thus may represent deceptive signalling.
In this study, we set out to compare sexual selection on phenotypic traits shared by male and female R. longicauda in the wild. We used multivariate selection analysis to determine whether mating success was associated with different suites of phenotypic traits in males and females, to test the prediction that contrasting patterns of sexual selection have driven the evolution of sexual dimorphism in these traits. We also tested for patterns of assortative mating by examining whether the phenotypes of mated individuals were related to those of their mating partners or to the nuptial gift provided by the male to the female during mating. Finally, given that males of other species sometimes compete within all-male swarms for optimal mate-obtaining swarm positions (e.g. in a bibionid fly, Thornhill, 1980), we tested whether female dance fly morphology was associated with lower positions in mating swarms, which might be advantageous because this is the part of the swarm from which prey-carrying males enter.