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90-Gene Cluster Key to Divergent Plumage & Spectacular Mating Behavior in Eurasian Shorebird Males; Causative Balanced Polymorphism Has Been Maintained for 4 Million Years; Cluster Contains Genes for Sex Hormone Regulation and Pigmentation

The ruff is a Eurasian shorebird that has a spectacular “lekking” behavior (a typer of mating behavior), in which highly ornamented males compete for females. Now, two independent research groups report that male ruffs with alternative reproductive strategies carry a chromosomal rearrangement that has been maintained as a balanced genetic polymorphism for approximately 4 million years. [Note: “Lekking” is a mating ritual in some species, in which males assemble on the mating ground (the lek), where they spar with each other or put on extravagant visual or aural displays (mating dances or gymnastics, plumage displays, vocal challenges, etc.) so that a female will select them for mating. The two studies, one led by scientists at Uppsala University in Sweden, and the other led by scientists at the UK’s University of Sheffield and at the Univesrsity of Graz in Austria, were published online on November 16, 2015 in Nature Genetics. The Uppsala article is titled “Structural Genomic Changes Underlie Alternative Reproductive Strategies in the Ruff (Philomachus pugnax).” The UK/Austria study is titled “A Supergene Determines Highly Divergent Male Reproductive Morphs in the Ruff.” Three different types of ruff males are seen at the “leks” (mating grouns) of this species (see accompanying video, link below). “Independent” males show colorful ruffs and head tufts and fight vigorously for territories. “Satellite” males are slightly smaller than “Independents,” do not defend territories, and have white ruffs and head tufts. “Faeder” males mimic females by their small size and lack of ornamental feathers, and they do not defend territory. The “Independent” and “Satellite” males show a remarkable interaction in which the “Satellite” males allow “Independent” males to dominate them on the leks. Both “Independents” and “Satellites” benefit from this interaction because it increases their mating success by attracting females that are ready to mate, explains Dr. Fredrik Widemo, who did his Ph.D. work on ruff lekking behavior.

“’Faeder’ males also have a chance to mate with females when other males are occupied with male-male interactions,”continues Dr. Widemo.
Previous studies have indicated that these remarkable differences between male morphs are under strict genetic control and are determined by a single genetic region.

How, however, can such complex differences in behavior, size, and plumage have a simple genetic basis? To shed light on this enigma, the researchers have sequenced the entire genomes of “Independent,” “Satellite,” and “Faeder” male ruffs.

“We discovered that both ‘Satellite’ and ‘Faeder’ males carry a so-called “supergene” that is not a single gene with superpower, but a cluster of approximately 90 genes kept together by a chromosomal inversion, which means that there is no genetic exchange between the three different morphs, says Sangeet Lamichhaney, one of the Ph.D. students involved in the study.

The group reports that the sequence difference between the chromosome variants is as large as 1.4 percent, which is higher than the average sequence difference between human and chimpanzee chromosomes. The scientists estimate that the chromosome inversion occurred approximately 4 million years ago.

“The ‘Satellite’ and ‘Faeder’ male morphs are the result of an evolutionary process over million of years and involve many genetic changes among the 90 genes in this ‘supergene,’” explains Uppsala University’s Leif Andersson, Ph.D., who led the study.

The ruff “supergene” contains five genes that have a role in the metabolism of steroid hormones.

“It is particularly interesting that we see an enrichment of genetic changes in the vicinity of a gene, HSD17B2, that determines an enzyme that converts active testosterone to a more inactive form,” continues Dr. Andersson.

“Independents have a significantly higher level of testosterone than Satellite and Faeder males and we think this is the reason that, in turn, leads to an altered behavior.”

There are many examples of associations between behavior and pigmentation in animals, but the underlying causal relationships have rarely been revealed. The present study now provides insights into why there is such a strong association between altered behavior and white color in Satellite males.

“The simple answer is that the ‘supergene’ contains both, genes like HSD17B2 affecting the metabolism of sex hormones, and the MC1R gene controlling pigmentation,” explains Mr. Lamichhaney.

Why has this fascinating difference in male reproductive strategies evolved in the ruff?

“Fighting over territories and females is both energetically costly and risky. This created an opportunity for the evolution of alternative male mating strategies in which males spend less energy on fighting,” explains Dr. Widemo.

“We think that this evolutionary process started with the occurrence of the inversion about 4 million years ago and that the inversion, in itself, altered the regulation of one or more genes affecting the metabolism of sex hormones and this created a primitive alternative male morph, which has been further improved step by step by the accumulation of many genetic changes,” concludes Dr. Andersson.

Please the following video demonstrating alternative ruff male reproductive strategies at a lek in Karesuando, Sweden (http://www.scilifelab.se/research/scientific-highlights/ruff). This video clip is based on a production from NHK, the Japanese Broadcasting Company.

[Press release] [Nature Genetics article-Uppsala] [Nature Genetics article-UK/Austria] [SciLifeLabs article & video]

[Washington Post article]