Background:

Complex polymorphisms observed in nature are often governed by supergene architecture^1,2. A supergene is a tightly linked cluster of loci, inherited as a single locus that includes several genes regulating different aspects of the complex trait, which are held together by genetic rearrangement and structural variation^1,2. Supergenes regulate myriad traits from wing patterns in butterflies^3,4 and mating plumage in birds^5,6 to social polymorphism in ants⁷. The individual morphs in a polymorphism are usually governed by alternative variants of the supergene, which are maintained under balancing selection driven by negative frequency dependent selection⁸, heterozygote advantage⁹ or disassortative mating¹⁰.

Among seaweed flies, Coelopa frigida, mating is driven by female preference, often resulting in mate rejection response upon mounting by males. This has led to sexual selection for larger males⁹. A large supergene spanning 60% of chromosome 1 (Cf-Inv(1)) includes several inversions and produces two haplotypes, α and β, which are associated with adult size. αα individuals are generally the largest in size, followed by αβ individuals, which are intermediate in size, and ββ individuals, which are the smallest⁹. These differences are more prominent in males than in females. In addition, the supergene shows overdominance and heterozygote advantage due to longer development time and high mortality rate accompanying αα homozygotes. Female choice drives disassortative mating based on whether females dislodge mounted males. The preprint examines whether chemical cues or different cuticular hydrocarbon composition (CHC) might be perceived by females, whether they play a role in mate choice, and whether the supergene Cf-Inv(1) regulates both male traits and female preference.

Key findings:

1.       Cuticular hydrocarbon composition is distinct between αα and ββ males, with αβ males showing intermediate profiles.  First, the authors measured the CHC profiles of 276 C. frigida specimens using gas chromatography and mass spectrometry (GC-MS).  They sampled 20-25 individuals of each sex, genotype, and population from North America and Norway.  Analysis using PCA, OPLS-DA and PERMANOVA in homozygous males showed robust differentiation of cuticular hydrocarbon profiles between the two genotypes. Females, on the other hand, showed overlapping cuticular hydrocarbon profiles that explained very little difference between genotypes. Thus, females may be choosing males based on their cuticular hydrocarbon profiles.

2.       Females can sense male cuticular hydrocarbons, including individual compounds unique to each genotype. When males mount females, their forelegs come into contact with female antennae. The authors tested whether female antennae could detect male cuticular hydrocarbons by measuring the perception of different compounds with gas chromatography-electroantennographic detection (GC-EAD). Females of all genotypes responded to 36 compounds in a combined extract from males of different genotypes. Males, on the other hand, could sense only 3 of these compounds. On closer examination, the authors found that perception of the cuticular hydrocarbons varied with the genotypes of females. Four compounds were detected by αα females exclusively, one by αα and αβ females, two exclusively by ββ females and seven by αβ and ββ females. This suggests that the supergene composition governs perception of male traits by females in addition to regulating the male trait itself.

3.       Genes involved in cuticular hydrocarbon biosynthesis and odorant detection are differentially expressed between genotypes. Differential expression analysis between males and females of different genotypes showed 29 transcripts were differentially expressed between αα and ββ individuals. Contributions from genes involved in cuticular hydrocarbon biosynthesis were largely observed in males, while differential expression of odorant receptors was not restricted to a single sex. Of these genes, one CHC biosynthesis pathway gene and nine odorant receptor (OD) genes mapped to the Cf-Inv(1) supergene, while the rest mapped to regions widespread across the genome. Therefore, genes involved in cuticular hydrocarbon profiles across males of different genotypes appear to be acting in trans with the supergene. The large number of OD genes located within Cf-Inv(1) indicates the effect of this supergene on female perception. Additionally, the authors also found three paired transcripts with overlapping coordinates (a characteristic of tandem duplication which is frequently observed in odorant detection proteins) that may show differential expression of alternatively spliced isoforms, with one transcript successfully assembled from αα and another from ββ individuals. The α and β variants of the supergene show higher genetic divergence in this region compared to the rest of the supergene. This divergence is comparable to those between sister species and indicates that supergene architecture may facilitate faster evolution of certain genes, such as the OD genes observed here.

Why is this work important?

Although supergenes are commonly associated with complex polymorphic traits and may include several hundred genes, the mechanism by which genes within a supergene regulate different aspects of a phenotype is not fully understood. Similarly, it is unclear to what extent traits are shaped by the genes within the supergene architecture compared to genes outside the supergene. Studies such as this can help bridge this gap in our understanding of how supergenes act in regulating complex phenotypes. The study provides an example of a trait and its preference being governed by a supergene and the underlying genetic architecture. In studies focusing on divergence and speciation, such traits are referred to as “magic traits” as they provide a common genetic bases for population divergence and evolution of reproductive isolation. However, in this example, the magic trait is associated with disassortative mating, resulting in maintenance of the supergene by balancing selection.

Questions for authors:

1.       Among the genes differentially expressed between genotypes αα and ββ, do those that did not map to the supergene show high genetic divergence between the genotypes?

2.       Do males perceive female cuticular hydrocarbons just as well as females do? Could there be a cryptic male choice due to the small differences in female cuticular hydrocarbons between genotypes?

3.       Do Coelopa frigida produce any volatile pheromones or other signaling compounds that may be involved in mate choice apart from cuticular hydrocarbons?

4.       How well is the supergene characterized? Do we know participant genes that could shape different aspects of the male traits that females choose? Are there genes involved in growth included in the supergene?

References:

1. Thompson, M. J. & Jiggins, C. D. Supergenes and their role in evolution. Heredity (Edinb). 113, 1–8 (2014).
2. Schwander, T., Libbrecht, R. & Keller, L. Supergenes and complex phenotypes. Curr. Biol. 24, R288–R294 (2014).
3. Joron, M. et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477, 203–206 (2011).
4. Kunte, K. et al. doublesex is a mimicry supergene. Nature 507, 229–232 (2014).
5. Lamichhaney, S. et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat. Genet. 48, 84–88 (2015).
6. Küpper, C. et al. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet. 48, 79–83 (2015).
7. Wang, J. et al. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493, 664–668 (2013).
8. Kunte, K. Female-limited mimetic polymorphism: A review of theories and a critique of sexual selection as balancing selection. Anim. Behav. 78, 1029–1036 (2009).
9. Butlin, R. K., Read, I. L. & Day, T. H. The effects of a chromosomal inversion on adult size and male mating success in the seaweed fly, Coelopa frigida. Heredity (Edinb). 49, 51–62 (1982).
10. Blyth, J. E. & Gilburn, A. S. The effect of an inversion system and the time interval between matings on postcopulatory sexual selection in the seaweed fly, Coelopa frigida. Heredity (Edinb). 95, 174–178 (2005).

Tags: mate choice, sexual conflict, sexual selection

doi: https://doi.org/10.1242/prelights.30248

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