Uncovering The Genomic Secrets Of Color Variants In Female Cuckoo Birds

Why do female common cuckoos have one of two different colors, whilst the males are all the same color?

Sexual dimorphism — the visible differences between males and females of the species — can easily be seen in a wide variety of animals — even in humans. Although plenty of research has focused on understanding the evolutionary foundations underlying these distinct traits, there is another type of dimorphism that has received far less attention: intrasexual polymorphisms — also known as sex-limited polymorphisms — where one sex shows greater variation in a particular trait than the other.

The common cuckoo, Cuculus canorus, is one such species. Common cuckoos are obligate brood parasites that lay their eggs into other species’ nests, thereby forcing the reluctant songbird hosts to care for a cuckoo baby. Interestingly, cuckoo birds show a plumage color polymorphism that is limited to females: Adult males are gray whereas females are either gray or reddish-brown (rufous). They are sparrowhawk mimics: a causal human or avian observer might mistake a common cuckoo for a Eurasian sparrowhawk, Accipiter nisus, a small raptor that commonly preys on the cuckoos’ songbird foster parents. But why would a cuckoo mimic a sparrowhawk?

“With this mimicry, the bird imitates dangerous predators of the host birds, so that they keep their distance instead of attacking,” the study’s senior co-author, evolutionary biologist Jochen Wolf, Professor and Chair of Evolutionary Biology at Munich University, said in a statement.

Why did this polymorphism evolve? Why do only females show this color morph? One proposed explanation is that the rarer (rufous) color morph has an advantage because the rufous adult females are harassed less frequently by adult males because they mimic juvenile cuckoos, which are rufous colored. Another proposes that the rarer rufous female color morph has an advantage because they are mobbed and attacked less frequently by their songbird hosts — until the host birds get wise to the trick. For example, if there are a lot of grey hawk-mimetic cuckoos or a lot of sparrowhawks in a particular area, potential host birds soon learn to distinguish whether the bird they’re looking at is a sparrowhawk or a cuckoo, and respond accordingly. (Potential foster parents occasionally kill adult cuckoos that are near their nests.)

“Then the advantage of the rufous morph comes into play, as it is less common and has not been learned by the hosts,” Professor Wolf stated.

Which color variant the host songbirds learn to fear and to mob depends upon the abundance both of the cuckoos and of the birds of prey. Further, the prevalence of each color morph varies between different populations within the same species as well as between cuckoo species. Because only female cuckoos get close to the hosts’ nests, only female cuckoos show these color morphs, suggesting these color variant genes only occur in the females’ genomes — an example of a sex-limited polymorphism.

“We would therefore expect these color variants — so-called polymorphisms — to be fixed somewhere in the female genome,” Professor Wolf said.

Genes that affect males and females differently often reside on the sex chromosomes. In mammals, males are the heterogametic sex (XY chromosomes), determined by their non-matching sex chromosomes. But birds are the opposite of mammals: In birds, females are the heterogametic sex (ZW chromosomes). This disparity led the researchers to hypothesize that the color variation observed in female cuckoos is probably linked to gene(s) on the female sex chromosome or on the mitochondrial genome, which comes solely from the mother.

For this reason, Professor Wolf and collaborators focused their efforts on identifying and locating the female-limited polymorphism on the W chromosome, which is also female-limited. They also investigated this polymorphism’s genetic basis, and reconstructed its evolutionary history.

“We found that, instead of a single gene or set of genes, nearly all variations in the gray or rufous coloration were associated with the full length of the female-limited W chromosome,” pointed out study co-author, ornithologist Mark Hauber, executive director of the The City University of New York Advanced Science Research Center and a psychology professor at the CUNY Graduate Center.

“That was really unexpected.”

As part of this work, Professor Wolf, Professor Hauber and collaborators found that the common cuckoo’s sister species (its closest living relative), the oriental cuckoo, Cuculus optatus, shared the same melanin-based color morphs and genetic variants. For this reason, they surmised that the genetic polymorphism was an ancient one — originating over 1 million years ago in the shared common ancestor of these birds, predating the two species’ divergence that occurred roughly 140,000 years ago.

“Consequently, the mutations already existed in a common ancestor and are therefore older than the speciation,” Professor Wolf explained.

But which color variant has the greatest advantage for these birds? Considering how long this polymorphism has been maintained in both sister species, it’s safe to conclude that neither variant is “the best”.

“This causes the genetic variation to be maintained for a long time,” Professor Wolf elaborated.

Basically, when there are two competing genetic variants in a population, the more beneficial one “wins” and becomes established. However, when two genetic variants are present for millions of years, as these have been, it indicates that the rarer of the two variants is advantageous, so the population oscillates between the two and eventually settles into a more-or-less consistent balance for each variant.

Are there other traits that may show similar dynamics?

“Our results support the intriguing possibility that numerous other traits that are sex-specific but more difficult to investigate are genetically encoded on the matrilinear genome like the color polymorphism of the female cuckoo,” Professor Wolf replied.

Source:

Justin Merondun, Cristiana I. Marques, Pedro Andrade, Swetlana Meshcheryagina, Ismael Galván, Sandra Afonso, Joel M. Alves, Pedro M. Araújo, Gennadiy Bachurin, Jennifer Balacco, Miklós Bán, Olivier Fedrigo, Giulio Formenti, Frode Fossøy, Attila Fülöp, Mikhail Golovatin, Sofia Granja, Chris Hewson, Marcel Honza, Kerstin Howe, Greger Larson, Attila Marton, Csaba Moskát, Jacquelyn Mountcastle, Petr Procházka, Yaroslav Red’Kin, Ying Sims, Michal Šulc, Alan Tracey, Jonathan M. D. Wood, Erich D. Jarvis, Mark E. Hauber, Miguel Carneiro, and Jochen B. W. Wolf (2024). Evolution and genetic architecture of sex-limited polymorphism in cuckoos, Science Advances 10(17) | doi:10.1126/sciadv.adl525