Stuck in a Ruff: Having a supergene is not always super

Female Ruffs with a large inversion have lower reproductive success.

Occasionally, a section of DNA might be flipped around. Such inversions can be quite large and hold a collection of genes, giving rise to so-called supergenes. In the Ruff (Calidris pugnax), for example, a genomic chuck of roughly 4.5 million DNA-letters – containing 125 genes – was inverted about 3.8 million years ago. This chromosomal rearrangement resulted in two distinct morphs: the large and territorial Independent morph (with the “normal” section of DNA) and the smaller Faeder morph (with the inversion). The latter morph developed a new mating strategy in which males sneakily try to copulate in the territories of Independents by pretending to be a female. Later on, a third morph arose through the recombination between the ancestral DNA-section and the inversion. The resulting Satellite morphs are semi-cooperative, they display on the territories of Independent males to attract more females, even though they don’t always manage to mate.

This complicated mating system has been extensively studied from the male perspective. However, these three morphs also occur in females. A recent study in the journal Nature Communications provided a female perspective: what are the fitness consequences of this supergene for females?

Following Females

Lina Giraldo-Deck and her colleagues monitored the reproductive success of 186 female Ruffs, covering the three morphs: 118 Independents, 48 Satellites and 20 Faeders. These experiments revealed that “Faeder females laid fewer and smaller eggs with reduced offspring survival compared to Independent and Satellite females.” The exact mechanisms underlying the lower reproductive success of Faeder females remain to be determined. It could be related to the accumulation of deleterious alleles in the supergene due to the lack of recombination (see this study for more details on mutational accumulation in inversions). A detailed genomic analysis is needed to this test idea.

Faeder females have lower reproductive success in terms of hatching probability (left graph). The resulting offspring also showed a lot of variation in the probability of leaving the nest (right graph). From: Giraldo-Dec et al. (2022).

Sexual Conflict

But if female Faeders have such low reproductive success, why doesn’t the supergene disappear from the population? The researchers argue that this female disadvantage is compensated for by the higher reproductive success of male Faeders. This hypothesis was supported by an analytical model, showing that male Faeders need to fertilize 2.4% of the females to keep the supergene at a stable frequency in the population. This mathematical model remains to be confirmed with field observations, but it does seem like a reasonable explanation.

The resulting situation – female disadvantage and male advantage from the supergene – is a beautiful example of intralocus sexual conflict. At a particular genetic locus (the supergene, in this case), males and females have different evolutionary interests. We would not have discovered this extra layer of complexity if we only focused on the role of males in this mating system. A female perspective can be refreshing.

A graphical representation of the conflict between the sexes in Ruffs. The lower reproductive success of Faeder females leads to less offspring of this morph. However, male Faeders have a higher reproductive success, maintaining this morph in the population. From: Giraldo-Deck et al. (2022).

References

Giraldo-Deck, L. M., Loveland, J. L., Goymann, W., Tschirren, B., Burke, T., Kempenaers, B., … & Küpper, C. (2022). Intralocus conflicts associated with a supergene. Nature Communications13(1), 1-8.

Featured image: Ruff (Calidris pugnax) © Åsa Berndtsson | Wikimedia Commons

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