- Top of page
- LITERATURE CITED
- Supporting Information
In the seaweed fly, Coelopa frigida, a large chromosomal inversion system is affected by sexual selection and viability selection. However, our understanding of the interaction between these two selective forces is currently limited as research has focused upon a limited range of environments. We allowed C. frigida larvae to develop in two different algae, Fucus and Laminaria, and then measured viability and body size for each inversion genotype. Significant male-specific genotype-by-environment interactions influenced viability and body size. For males developing in Laminaria, the direction of viability selection acts similarly on the inversion system as the direction of sexual selection. In contrast, for males developing in Fucus, viability selection opposes sexual selection. These results demonstrate that through considering viability selection in different environments, the costs and benefits associated with sexual selection can be found to vary.
Sexual selection and viability selection can often be found to act in opposing directions. Classically, the exaggeration of secondary sexual ornaments by sexual selection is held in check when viability becomes sufficiently compromised (Andersson 1994). In contrast, it is also proposed that sexual selection can act in concert with viability selection (Darwin 1859), for example, to promote local adaptation (van Doorn et al. 2009), to increase the spread of beneficial alleles within a population (Whitlock 2000; Proulx 2001, 2002; Lorch et al. 2003), or to help purge deleterious alleles (Whitlock and Agrawal 2009).
A key challenge for evolutionary biologists is to understand the interaction between sexual selection and viability selection. For example, sexual selection was not found to increase the rate of adaptation of the fruit fly, Drosophila melanogaster, to either thermal stress (Holland 2002) or a novel food source (Rundle et al. 2006). In contrast, more recent work using the same species demonstrated rapid elimination of a deleterious allele under sexual selection (Hollis et al. 2009). Such diverse results highlight that the interaction between sexual selection and viability selection is not fixed, either within or between species. Apparently, conflicting results in fact prompt a more interesting question—under what conditions will sexual selection either assist or oppose viability selection? In this study, we show that, within a single species, sexual selection can assist viability selection in one environment yet oppose viability selection in another.
Variation in the fitness of sexually selected genotypes in different environments, known as genotype by environment interactions (G×Es), can contribute to our understanding of the relationship between sexual selection and viability selection (Ingleby et al. 2010). For example, in the lesser wax moth, Achroia grisella, female choice leads to the production of higher quality offspring under favorable conditions, but lower quality offspring under unfavorable conditions (Jia and Greenfield 1997). The seaweed fly, Coelopa frigida, is an ideal species to study G×Es as both viability and sexually selected fitness can be attributed to a large chromosomal inversion system (Butlin et al. 1982a,b).
Coelopa frigida are dependent, as adults and larvae, upon decomposing marine algae washed up on beaches (Dobson 1974). The C. frigida mating system is characterized by a sexual conflict over mating frequency as males harass females intensely to coerce them into mating (Blyth and Gilburn 2006). Male ability to overcome female resistance increases with body size, hence sexual selection favors larger males (Butlin et al. 1982b; Crean and Gilburn 1998). A large inversion system is a major determinant of male body size and occurs in two forms, α and β (Butlin et al. 1982b; Day et al. 1982). αα-homokaryotypes are the largest, ββ-homokaryotypes are smallest, and heterokaryotypes are of intermediate size (Day et al. 1980; Butlin et al. 1982b). Sexual selection for large male size therefore exerts significant selection for male inversion genotype (αα > αβ > ββ; Butlin et al. 1982b).
The inversion system also influences egg to adult viability, which is characterized by strong heterokaryotype advantage, or “heterosis” (Butlin et al. 1982a). Consequently, sexual selection and viability selection can act in different directions, thus maintaining multiple forms of the inversion (Butlin et al. 1982a). αα females are predicted to experience greater costs of this mating bias, as they are less likely to produce heterokaryotype offspring when mating with larger males. However, these conclusions are limited as previous studies have not considered variation in viability selection among different environments.
A principal source of environmental variation is the algae present in wrack beds. Two genera, Fucus and Laminaria, are commonly found in varying proportions, yet the majority of studies have used only Fucus in experiments and for laboratory culture. However, it has been found that females will oviposit more readily (Phillips et al. 1995) and males increase mating effort (Edward and Gilburn 2007) when exposed to Laminaria. The objective of this study is to measure viability selection on the genetic inversion system when C. frigida larvae develop in either Fucus or Laminaria. We also compare the size of adults as a plastic response to developing on either Fucus or Laminaria.
- Top of page
- LITERATURE CITED
- Supporting Information
In this study, we found significant fitness benefits for C. frigida of development in Laminaria compared to Fucus. Larval to adult viability was greater and body size was greater when larvae developed in Laminaria. However, these benefits appear to be at the expense of a longer development time. The potential benefits of larval development in Laminaria help to explain previous reports of increased female oviposition and male reproductive effort within this environment (Phillips et al. 1995; Edward and Gilburn 2007). Results also demonstrate two significant male-specific G×Es. The first G×E is a difference in male viability among inversion genotypes during development in each alga (Fig. 1). The second G×E is a difference in the influence that the inversion system has in determining male body size during development in each alga (Fig. 2). Both of these G×Es are of interest because both inversion genotype and male body size are already known to be targets of sexual selection.
The proportions of each female genotype were approximately the same following development in either alga. Heterokaryotype females were most abundant, followed by ββ, and then αα genotypes (Fig. 1). This indicates that viability selection for female genotype was the same on each alga. However, a male-specific G×E is identified because the proportion of male genotypes differed following development in either alga. Following development in Fucus, heterokaryotype males were most abundant, followed by αα, and then ββ genotypes (Fig. 1). In contrast, following development in Laminaria, αα-homokaryotype males were most abundant, followed by heterokaryotype, and then ββ genotypes (Fig. 1). Because the starting proportion of each genotype was the same on both algae, this shows that viability selection for male genotype differed in each environment. This G×E is important because it influences the relationship between viability selection and sexual selection. Relative to a Fucus environment, αα-homokaryotypes are favored by viability selection in a Laminaria environment. Thus, the direction of viability selection and sexual selection, which is also known to favor larger αα-homokaryotype males, is more similar in a Laminaria than a Fucus environment. In contrast, greater selection for heterokaryotypes in a Fucus environment, relative to Laminaria, is more likely to conflict with the direction of sexual selection.
The different relationship that is predicted between viability selection and sexual selection in each of these environments is central to considering how this species will adapt to each environment. Sexual selection is more likely to aid adaptation to a Laminaria environment as a mating bias toward larger males that increases the likelihood of producing αα offspring will be less costly to females. This is because αα males are more likely to survive in this environment when compared to a Fucus environment. In contrast, sexual selection is more likely to hinder adaptation to a Fucus environment as heterokaryotypes of both sexes are known to prosper, when compared to development in Laminaria. A further consideration is that in a Laminaria environment, as both sexual and viability selections are more likely to favor αα males, the β form of the inversion could be lost completely. Nevertheless, heterokaryotype females are still the most abundant genotype in both environments. This means that the optimal inversion genotype, according to the combined effects of viability selection and sexual selection, will differ for each sex in each environment. There is currently no evidence for sex linkage of the inversion system (Day et al. 1982), however we would predict that sex linkage is more likely to evolve in environments that are dominated by Laminaria, than Fucus.
This G×E has further implications for predicting the sexual conflict load of male harassment for females with different inversion genotypes. It was previously thought that αα females experience the greatest conflict load as they are less likely to produce heterokaryotype offspring when mating with larger males that are likely to share the same genotype. This is in contrast to ββ females that were predicted to indirectly benefit from mating with larger males through the greater probability of producing more viable heterokaryotype offspring. However, these predictions were based upon an assumption of viability selection favoring heterokaryotypes, which we now demonstrate as being environmentally dependent. Instead, the conflict load for αα females is expected to be lower in a Laminaria environment, than a Fucus environment, as αα male offspring are more likely to survive. This environmental variation in conflict load could explain why the resistance of αα females can vary between populations from a mating bias toward large males (Gilburn et al. 1992, 1993) to a mating bias toward small males (Gilburn et al. 1993, 1996; Gilburn and Day 1994; Day and Gilburn 1997; Blyth and Gilburn 2011).
The second G×E to be discussed is variation in the degree of influence the inversion system has on male body size during development in each alga (Fig. 2). Even though the reaction norms do not cross in this instance, that is, the rank order of male size across genotypes is unaltered, this still constitutes a G×E because the reaction norms are nonparallel (Ingleby et al. 2010). The effect of this G×E is that the range of male body size across the three inversion genotypes is greater when males develop in Laminaria than when they develop in Fucus. This will influence the likelihood that female resistance will bias matings in favor of a particular male genotype, because male size is a better predictor of genotype in Laminaria. In essence, whenever a genotype has greater influence upon a phenotype, any selection acting upon that phenotype is more likely to influence those genes. In many respects, this is analogous to the finding that G×Es can influence the reliability of sexually selected traits to signal potential fitness benefits of mating (Greenfield and Rodriguez 2004; Higginson and Reader 2009). In C. frigida, this is important because, following development in Laminaria, αα males are more likely to be larger than other males, hence more likely to succeed at overcoming female resistance and will be more likely to mate. The sexual selection differential is therefore predicted to be greater following development in Laminaria.
In this study, differences in male viability selection and adult size have been identified that predict alternate relationships between viability selection and sexual selection following development in different environments. This example is not expected to be unique and reiterates the need for further investigation of G×Es in relation to sexual selection (Ingleby et al. 2010). It is evident from many studies that the relationship between sexual selection and viability selection is not a fixed property. Future work would therefore benefit our understanding of sexual selection most by trying to understand the conditions and circumstances that can influence this relationship.