Low mutation load in a supergene underpinning alternative male mating strategies in ruff

Ruffs are shorebirds with an elaborate lekking behavior involving three male morphs with different mating strategies: Independents, Satellites, and Faeders1,2. The latter two are heterozygous for different versions of a supergene maintained by an inversion that were estimated to have occurred about 4 million years ago3. Faeders carry an intact inversion while the Satellite allele is recombinant, both of which are expected to accumulate high mutational load because they are recessive lethals. Here we have constructed a highly contiguous genome assembly of the inversion region for both the Independent and Satellite haplotypes. The recombination event(s) between an inverted and non-inverted chromosome creating the Satellite allele must have occurred recently (within the last 100,000 years) based on the minute sequence divergence between the Satellite and Independent alleles in the recombinant regions. Contrary to expectations4,5, we find no expansion of repeats and only a very modest mutation load on the Satellite allele in the nonrecombinant region despite high sequence divergence (1.46%). The essential centromere protein CENPN gene is disrupted by the inversion, and surprisingly is as well conserved on the inversion haplotypes as on the noninversion haplotype. The results suggest that the inversion may be much younger than previously thought. The lack of mutation load despite recessive lethality can be explained by the introgression of the inversion from a now extinct lineage.