Gene flow during glacial habitat shifts facilitates character displacement in a Neotropical flycatcher radiation

Balaji Chattopadhyay, Kritika M. Garg, Chyi Yin Gwee, Scott V. Edwards, Frank E. Rheindt

Pleistocene climatic fluctuations are known to be an engine of biotic diversification at higher latitudes, but their impact on highly diverse tropical areas such as the Andes remains less well-documented. Specifically, while periods of global cooling may have led to fragmentation and differentiation at colder latitudes, they may - at the same time - have led to connectivity among insular patches of montane tropical habitat with unknown consequences on diversification. In the present study we utilized ~5.5 kb of DNA sequence data from eight nuclear loci and one mitochondrial gene alongside diagnostic morphological and bioacoustic markers to test the effects of Pleistocene climatic fluctuations on diversification in a complex of Andean tyrant-flycatchers of the genus Elaenia. Population genetic and phylogenetic approaches coupled with coalescent simulations demonstrated disparate levels of gene flow between the taxon chilensis and two parapatric Elaenia taxa predominantly during the last glacial period but not thereafter, possibly on account of downward shifts of montane forest habitat linking the populations of adjacent ridges. Additionally, morphological and bioacoustic analyses revealed a distinct pattern of character displacement in coloration and vocal traits between the two sympatric taxa albiceps and pallatangae, which were characterized by a lack of gene flow. Our study demonstrates that global periods of cooling are likely to have facilitated gene flow among Andean montane Elaenia flycatchers that are more isolated from one another during warm interglacial periods such as the present era. We also identify a hitherto overlooked case of plumage and vocal character displacement, underpinning the complexities of gene flow patterns caused by Pleistocene climate change across the Andes.