Avian supergene study explores evolutionary paradox behind unusual frill mating strategies

In the colorful world of courtship birds, the ruff (Calidris pugnax) is one of a kind. Breeding in marshes and wet meadows throughout Eurasia, males of this medium-sized sandpiper species are well known for their distinctive mating strategies, which range from flamboyant territorial displays to cunning mimicry.

These behaviors, along with striking differences in plumage, are determined by a single genetic region called a supergene. Supergenes are groups of genes that control complex traits. They are often associated with chromosomal inversion, in which the order of genes is reversed along the chromosome relative to the wild-type allele; this serves to suppress recombination, allowing a set of traits to be co-inherited.

Although there are potential benefits to preserving favorable combinations of genetic variants, this lack of recombination can also lead to the accumulation of deleterious mutations within the supergene over time.

However, a new study published in Molecular biology and evolutionentitled “Low mutation load in a supergene underlying alternative male mating strategies in the ruff (Calidris pugnax)”, revealed a remarkable evolutionary paradox, because the supergene that underlies the mating strategy mating in males in the ruff exhibits a surprisingly low mutation load.

The study results therefore challenge our understanding of the evolution and persistence of supergenes in nature.

Frilled males have long attracted the attention of scientists and birders because of their spectacular courtship displays and strange plumage, resembling the extravagant collars worn in the 16th century that inspired the species’ name. There are actually three distinct types of male ruffs, known as Independents, Satellites and Faeders, which differ in behavior, plumage and size.

“Independents have spectacular ornamental feathers and these males defend their territory on the lek (mating grounds),” explains Leif Andersson, the lead author of the new study.

“Satellites have light-colored ornamental feathers and do not defend the lek’s territory but allow independent males to dominate them. This behavior helps independent males attract females ready to mate; the advantage to satellites is They have access to the mating ground without needing to expend energy defending the lek’s territory. Faeders are non-territorial female mimics without ornamental feathers. They sneak up on the lek and attempt to s mate with females.

Interestingly, the Satellite and Faeder phenotypes are determined by the presence of an inversion that harbors approximately 100 genes. “The Faeder haplotype is an intact inversion while the Satellite haplotype arose from genetic recombination between the Independent and Faeder haplotypes,” continues Andersson.

In addition to carrying one of the inverted haplotypes, all Satellite and Faeder males carry an independent haplotype, because the presence of two copies of the inversion (in the recessive or homozygous state) is lethal.

The frill supergene has long intrigued Andersson and his research team.

“When we first discovered the ruff supergene,” says Andersson, “we were surprised to find that the sequence divergence between the inversion alleles and the wild-type allele was as high as 1.4%. is higher than the sequence divergence between humans and chimpanzees and suggested a split around 4 million years ago, based on the substitution rate estimated for birds.

“Inversion alleles are recessive lethal, probably because the inversion breaks an essential gene. So the question that emerged is, how do you maintain a recessive lethal allele for 4 million years?”

To investigate this mystery, researchers used cutting-edge genomic sequencing techniques to create highly contiguous genome assemblies for independent and satellite haplotypes. They used these assemblies alongside previously published whole-genome data to assess the mutational load of the inverted supergene.

As Andersson noted, “Population genetics theory predicts that supergenes should accumulate genetic load (e.g., deleterious mutations) due to relaxed purifying selection, particularly if the supergene is a recessive lethal as is the ruff supergene.”

Surprisingly, however, the researchers found no substantial accumulation of repetitive elements and only modest mutation load on the Satellite and Faeder haplotypes. This unexpected finding forced the study authors to re-evaluate their hypotheses about the ruff supergene. “I really had to re-evaluate the way I thought about supergenes as we continued to find evidence of recent purifying selection where there shouldn’t have been any,” notes Andersson.

The authors propose two potential scenarios to resolve this paradox. First, the inversion may have only recently acquired its recessive lethality. If an older version of the supergene were more common and was not lethal recessive, recombination could occur in ruffs carrying two copies of the inversion, allowing deleterious mutations to be eliminated by purifying selection.

An alternative hypothesis, favored by the authors, is that the supergene would have been introduced by introgression from another species or subspecies. In this scenario, hybridization between a ruff and another species leads to the introduction of the supergene into the ruff’s genome, and its persistence is then favored by selection because it holds together the alleles contributing to a mating strategy successful male.

Although the study authors were unable to identify the lineage that may have contributed to the inversion, they note that given the estimated timeline, the donor species may now be extinct.

This study highlights the complex forces governing male mating strategies in the ruff and supergenes in general. “Inversions are easy to find with modern genomic tools but difficult to understand,” notes Andersson. “However, it should be very interesting to analyze gene expression in multiple tissues of the different forms and try to understand which of the inversion genes contribute to the dramatic differences between the forms.”

Although their genomic data has so far uncovered two potential candidate genes, one involved in testosterone metabolism and the other likely to influence ornamental feather coloration, additional transcriptomic data are needed to answer to this question. Unfortunately, such data can be difficult to obtain: “The main challenge of this proposed gene expression study,” explains Andersson, “is that it is a wild species and is not easy to assemble the large collection of samples that will be taken. necessary for a complete analysis.

Despite this obstacle, further research into this remarkable model system promises to provide a deeper understanding of the origin, persistence, and evolutionary trajectories of supergenes.