Continental diversification and insular speciation in a widespread passerine (Troglodytes musculus) in southern South America

Abstract

Understanding how the evolutionary dynamics of geographically widespread species play out in space and time is critical for uncovering the processes shaping biodiversity. We integrated mitochondrial DNA and genome-wide SNPs to investigate the history of diversification of the Southern House Wren (Troglodytes musculus) in southern South America and its insular relative, Cobbs Wren (T. cobbi), from the Malvinas/Falkland Islands (MFI). T. musculus is an abundant and widespread species, and by studying its population structure and demographic history we aim to uncover the processes that may have shaped the evolutionary history of this and other co-distributed taxa in southern South America. All analyses indicate a latitudinal divergence, with an initial split between northern populations (Bolivia, Northern and Central Argentina, Uruguay) and southern populations from Patagonia and the MFI. Shortly after this initial divergence, further diversifications occurred, including the colonization of the MFI from Patagonia, where this newly formed insular population became isolated from the continent, and the split between an Andean lineage and a widespread, lowland lineage occurring in lowland Bolivia, Northern and Central Argentina and Uruguay. Both the timing of these splits and the mitochondrial and genomic patterns of variation uncovered in T. musculus are consistent with a major role of glaciations -and particularly the Great Patagonian Glaciation-in the diversification of this species in the southern Neotropics. The negligible gene flow between the MFI and the continent, which derived in the formation of a new species, Cobbs Wren, contrasts with the notorious gene flow in the secondary, post-glacial contact zones between the northern and southern lineages, although with reduced gene flow between the Andean and lowland populations. We also observed cases of mito-nuclear discordance, highlighting the value of multi-locus approaches in revealing complex evolutionary histories. These results underscore how historical divergence, ecological barriers and corridors, and secondary contact after varying degrees of differentiation in allopatry jointly shape population structure and genetic diversity, with implications for understanding the diversification of widely distributed taxa.