Evolution and genetic architecture of sex-limited polymorphism in cuckoos

Merondun J, … [13 co-authors] …, Fülöp A, … [6 co-authors] …, Marton A, … [11 co-authors] …, Wolf JBW 2024. Evolution and genetic architecture of sex-limited polymorphism in cuckoos. Science Advances 10; eadl5255. link

Abstract

Sex-limited polymorphism has evolved in many species including our own. Yet, we lack a detailed understanding of the underlying genetic variation and evolutionary processes at work. The brood parasitic common cuckoo (Cuculus canorus) is a prime example of female-limited color polymorphism, where adult males are monochromatic gray and females exhibit either gray or rufous plumage. This polymorphism has been hypothesized to be governed by negative frequency-dependent selection whereby the rarer female morph is protected against harassment by males or from mobbing by parasitized host species. Here, we show that female plumage dichromatism maps to the female-restricted genome. We further demonstrate that, consistent with balancing selection, ancestry of the rufous phenotype is shared with the likewise female dichromatic sister species, the oriental cuckoo (Cuculus optatus). This study shows that sex-specific polymorphism in trait variation can be resolved by genetic variation residing on a sex-limited chromosome and be maintained across species boundaries.

W chromosome–encoded female- limited polymorphism predates speciation of C. canorus and C. optatus. (A) Maximum- likelihood phylogeny of the W chromosome (n= 53,712 biallelic SnPs) rooted along the truncated outgroup branch of the lesser cuckoo (C. poliocephalus), further including two specimens of another outgroup species (C. micropterus). nodes with Sh- like approximate likelihood ratio test (Sh- alRt; > 99%) support are marked with a diamond. (B) Autosomal ancestry coefficients (n= 16,031,301 biallelic SnPs) with individuals (x axis) displayed in the same order as the phylogeny. (C) Jittered sampling distribution with insets for two lo-calities with higher sampling density. (D) First principal component of autosomal (left) and W chromosome (right) genetic variation, with Pc scores scaled from 0.0 to 1.0 (outgroups C. poliocephalus and C. micropterus excluded). Because of deviations from normality, two Wilcoxon rank sum tests were conducted on each axis to evaluate significant differences between species and plumage morphs, denoted below each axis after Bonferroni correction. the eigenvalue proportion of variance explained is indicated adjacent to each Pc label. *P< 0.05; ns, not significant.