Phylogeography of a sex-limited polymorphism: Disentangling phenotypic variation in the Tourmaline Sunangel, Heliangelus exortis

Abstract

While much research has focused on the evolution of ornaments in male animals, females can also exhibit ornamental phenotypes and these have received much less attention. In the hummingbird species H. exortis (Tourmaline Sunangel), females appear to exhibit an intriguing pattern of variation across their geographic range in the tropical Andes, with some populations exhibiting a sex-limited polymorphism where females can have either a drab or variable male-like phenotype depending on the amount of iridescence on their gorgets. We conducted a phenotypic description of female plumage using pattern-based and reflectance spectrophotometry analyses across the distribution of H. exortis. We also performed a phylogeographic analysis to investigate how phenotypic variation relates to evolutionary relationships between populations and to gain insights into the origin and maintenance of the polymorphism. Our findings indicate that, in contrast to previous findings which suggested that geographic variation in the polymorphism was clinal, females in all Colombian populations exhibit a continuous range of polymorphic states, whereas those in Ecuador do not exhibit the polymorphism at all. Molecular analyses further revealed genetic differentiation among populations across the species distribution, highlighting a long history of isolation between populations and the role of inter-Andean valleys as major biogeographic barriers to gene flow. Additionally, our study uncovered a complex evolutionary history within the H. exortis clade, including an apparent loss of the polymorphism in the Ecuadorian population and the origin of a phenotypically distinct species, H. micraster, which is nested within H. exortis and sister to Ecuadorian populations. We propose that the phenotypic variation observed in H. exortis may be the result of genetic drift under geographic isolation or social selection acting differently within populations, leading to the maintenance of the female-limited polymorphism in Colombia and its loss in Ecuador. Our results emphasize the role that females can play in shaping the phenotypic and genetic diversity of species. We suggest that further molecular and socioecological studies are needed to better understand the evolution of the polymorphism and to delimit species boundaries within the genus.