Parapatric speciation with recurrent gene flow of two sexual dichromatic pheasants

Abstract

Understanding speciation has long been a fundamental goal of evolutionary biology. It is widely accepted that speciation requires an interruption of gene flow to generate strong reproductive isolation between species. The mechanism of how speciation in sexually dichromatic species operates in the face of gene flow remains an open question. Two species in the genus Chrysolophus, the Golden Pheasant (C. pictus) and Lady Amherst's Pheasant (C. amherstiae), both of which exhibit significant plumage dichromatism, are currently parapatric in southwestern China with several hybrid recordings in field. In this study, we estimated the pattern of gene flow during the speciation of the two pheasants using the Approximate Bayesian Computation (ABC) method based on data from multiple genes. Using a newly assembled de novo genome of Lady Amherst's Pheasant and resequencing of widely distributed individuals, we reconstructed the demographic history of the two pheasants by the PSMC (pairwise sequentially Markovian coalescent) method. The results provide clear evidence that the gene flow between the two pheasants was consistent with the predictions of the isolation with migration model during divergence, indicating that there was long-term gene flow after the initial divergence (ca. 2.2 million years ago). The data further support the occurrence of secondary contact between the parapatric populations since around 30 kya with recurrent gene flow to the present, a pattern that may have been induced by the population expansion of the Golden Pheasant in the late Pleistocene. The results of the study support the scenario of speciation between the Golden Pheasant and Lady Amherst's Pheasant with cycles of mixing-isolation-mixing, possibly due to the dynamics of geographical context in the late Pleistocene. The two species provide a good research system as an evolutionary model for testing reinforcement selection in speciation.