Gene flow throughout the evolutionary history of a polymorphic and generalist clownfish

Even seemingly homogeneous on the surface, the oceans display high environmental heterogeneity across space and time. Indeed, different soft barriers structure the marine environment, which offers an appealing opportunity to study various evolutionary processes such as population differentiation and speciation. Here, we focus on Amphiprion clarkii (Actinopterygii; Perciformes), the most widespread of clownfishes that exhibits the highest colour polymorphism. Clownfishes can only disperse during a short pelagic larval phase before their sessile adult lifestyle, which might limit connectivity among populations, thus facilitating speciation events. Consequently, the taxonomic status of A. clarkii has been under debate. We used whole-genome resequencing data of 67 A. clarkii specimens spread across the Indian and Pacific Oceans to characterise the species population structure, demographic history, and colour polymorphism. We found that A. clarkii spread from the Indo-Pacific Ocean to the Pacific and Indian Oceans following a stepping-stone dispersal and that gene flow was pervasive throughout its demographic history. Moreover, edge populations exhibited more similar colouration patterns compared to central populations. However, we demonstrate that colour polymorphism is not associated with population structure, thus, colour phenotype is unreliable in assessing the taxonomic status of A. clarkii. Our study further highlights the power of whole-genome comparative studies to determine the taxonomy of geographically wide-ranging and phenotypically diverse species, supporting the status of A. clarkii as a single species.