MALE-SPECIFIC GENOTYPE BY ENVIRONMENT INTERACTIONS INFLUENCE VIABILITY SELECTION ACTING ON A SEXUALLY SELECTED INVERSION SYSTEM IN THE SEAWEED FLY,COELOPA FRIGIDA

Abstract

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. K E Y W O R D S :Coelopid, Fucus, Laminaria, natural selection, sexual selection, viability selection.

Karyotype-environment associations support a role for a chromosomal inversion in local adaptation in the seaweed flyCoelopa frigida

“…Our data suggest that the relative proportions of seaweed species vary with habitat on which each karyotype is preferentially adapted. Both in Europe and America, an increased abundance of Laminariaceae is associated with an increased proportion of αα karyotypes (Fig.S9), a result which is consistent with better survival of αα on Laminariaceae in the laboratory [38]. Mixed wrackbeds or accumulations of plant debris favours heterokaryotypes while wrackbeds of Fucaceae or other seaweeds are associated with increased proportions of ββ.…”

“…The DNA marker consisted of two single-nucleotide polymorphisms that were associated with the different inversion rearrangements, and these were genotyped with two restriction enzymes (whole procedure detailed in part 1 of Supplementary Materials, Table S1, Fig.S1). It was validated with 44 samples previously karyotyped with the allozyme procedure as described by Edwards et al [38] (Table S2) and subsequently used to characterize the karyotype of 1988 wild North American samples of C. frigida (89-117 individuals/population, Table S4). For each population, the frequency of α rearrangement and the proportion of each karyotype was calculated in males and females separately, and then estimated for both sexes pooled at a sex-ratio of 1:1.…”

“…The amount of resources available in each substrate may be one of the factors explaining the different karyotype proportions. In fact, in the laboratory, Laminariaceae sustain a greater viability and a larger size than Fucaceae [38], which suggests it is a richer substrate, facilitating the long larval development and the large size of αα. In the wild populations investigated here, higher αα proportions are also found in populations with large flies (all karyotypes/sexes), and insect size is generally a good indicator of larval growth conditions [74].…”

“…The seaweed fly Coelopa frigida provides a suitable model to understand how inversions facilitate adaptation to heterogeneous environments because it carries a large inversion on chromosome I, with the two forms called α and β [34], that is polymorphic in all populations sampled so far. Studies on European C. frigida have shown that the inversion frequency varies along a latitudinal cline in Scandinavia which follows a natural gradient of temperature, salinity and seaweed composition, that the inversion has large phenotypic effects, particularly on male size, development time, viability and fertility, and that heterokaryotes generally have a higher egg-to-adult viability than homokaryotes [35][36][37][38][39][40].…”

Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

“…Although those factors may correlate with the duration of the wrackbed stability, they are also known to modulate the genotype-phenotype relationships and therefore the associated fitness. Controlled experiments in C. frigida show that substrate composition, temperature and density affect the relationship between genotype and survival, development time, body weight and body size (GxE effect) (37,41,55,56). In nature, this translates into geographic variation in adult size differences among genotypes and between the sexes (30,40), which may modify the reproductive advantage associated with the α allele.…”