Secondary contact after allopatric divergence explains avian speciation and high species diversity in the Himalayan-Hengduan Mountains

Abstract

The geographical context of speciation is important for understanding speciation and community assembly. However, the predominant mode of speciation in the Himalayan-Hengduan Mountains (HHMs), a global biodiversity hotspot, remains unknown. Here, we examined the role of geography in speciation using four pairs of sister or closely related avian species that currently co-occur in the HHMs. While multilocus network analyses based on nine to eleven genes revealed deep splits between these species, several allelic networks based on individual loci suggested phylogenetic paraphyly implying a recent history of divergence. Following extensive sampling in the contact zones of these species pairs, the coalescence-based approximate Bayesian computation approach supported no gene flow during their divergence and was consistent with an allopatric speciation model. We further estimated the divergence times of the four species pairs during the middle and late Pleistocene, which were characterized by increased amplitudes of glacial variability. We found a positive relationship between their divergence times and current sympatry levels, supporting a scenario of secondary contact following allopatric speciation. The Pleistocene glacial-interglacial cycles may have led to the initial geographic population isolation; ecological divergence or mate choice might further accelerate their differentiation during secondary contact, facilitating their speciation and species accumulation in the mountainous landscape. Our findings reveal the critical role of geographic isolation in speciation in the HHMs and shed light on how this biodiversity hotspot aggregates numerous species.