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 Communications, 13(1), 1-8.

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

Chromosomal evolution in sandpipers

Dynamic reshuffling of chromosomes across the Charadriiformes phylogeny.

In general, birds have a very stable number of chromosomes. Most species house 40 pairs of chromosomes – so, 80 in total – in their cells (commonly noted down as 2n = 80). These chromosomes can be divided into a few huge macrochromosomes and several tiny microchromosomes. However, not all species adhere to this “2n = 80 rule” in birds. In biology, there are always some exceptions. Falcons, for example, show chromosomal numbers of only 2n = 40 to 2n = 52. These atypical counts are probably the outcome of fusions between microchromosomes into macrochromosomes (see this blog post for more about the peculiar genomes of falcons). The order Charadriiformes – waders, gulls and allies – exhibit a wide range of karyotypes, ranging from 2n = 42 in the Eurasian Thick-knee (Burhinus oedicnemus) to 2n = 98 in the Common Snipe (Gallinago gallinago). To gain more insights into the patterns of chromosomal evolution in this bird group, researchers took a closer look at the karyotype of the Spotted Sandpiper (Actitis macularius). Their findings appeared in the journal BMC Ecology and Evolution.

Fissions

The Spotted Sandpiper has 92 chromosomes of which 14 pairs are macrochromosomes. To reconstruct the chromosomal evolution of this species, the researchers “painted” the chromosomes of the Spotted Sandpiper onto the karyotype of the Eurasian Thick-knee. This molecular technique revealed how different chromosomes were rearranged in the two species. It turns out that in the Spotted Sandpiper several chromosomes have been split into two or more smaller chromosomes. For instance, the second chromosome pair in the Eurasian Thick-knee (denoted as BOE2) split into four new pairs in the Spotted Sandpaper (namely AMA3, AMA11, AMA12 and AMA13). Similarly, BOE3 was divided into AMA4, AMA14 and AMA15. The figure below provides a nice overview of this karyotypic puzzle.

An overview of the chromosomal rearrangements between the Eurasian Thick-knee (BOE) and the Spotted Sandpiper (AMA). From: Pinheiro et al. (2021).

Phylogeny

By combining the chromosomal information of the Eurasian Thick-knee and the Spotted Sandpiper with karyotypic knowledge of other bird species, the researchers managed to reconstruct the evolutionary history of chromosome numbers in the order Charadriiformes. Most fissions occurred quite early in the evolution of these birds, namely after the gulls (family Laridae) split from the other families. An additional fission probably took place at the base of the sandpiper family Scolopacidae. Interestingly, rearrangements in the opposite direction – fusion of several chromosomes – happened within the Jacanidae family, giving rise to an ancestral-like karyotype of 2n = 82.

Seeing all these chromosomal reshuffling, I cannot help but wonder whether these changes were adaptive. Did the birds benefit from having more or less chromosomes in their cells? Or are these just non-adaptive rearrangements without much impact on individual fitness? Exciting questions that will hopefully be addressed in a future blog post.

Chromosomal changes across the phylogeny of the Charadriiformes. The karyotypes at the bottom depict the putative ancestral karyotype (PAK) of birds and the PAK of Scolopaci (SPAK).

References

Pinheiro, M. L. S., Nagamachi, C. Y., Ribas, T. F. A., Diniz, C. G., Ferguson-Smith, M. A., Yang, F., & Pieczarka, J. C. (2021). Chromosomal painting of the sandpiper (Actitis macularius) detects several fissions for the Scolopacidae family (Charadriiformes). BMC Ecology and Evolution, 21(1), 1-10.

Featured image: Spotted Sandpiper (Actitis macularius) © Mike Baird | Wikimedia Commons