Extreme genetic structure and dynamic range evolution in a montane passerine bird: implications for tropical diversification

Aim Employ phylogeographic analyses of a widespread species complex to examine the role of historical and evolutionary processes in the origin and maintenance of high species diversity in the Neotropical montane region. Location Neotropical highlands. Taxon Henicorhina wood-wrens (Aves, Troglodytidae). Methods We collected mtDNA sequence data for 288 individuals thoroughly covering the range of the Henicorhina leucophrys complex from Mexico to Bolivia. Sequences were employed to characterize population structure, infer phylogenetic relationships among populations and their divergence times, examine lineage accumulation through time, and identify presumptive species using coalescent methods. We also explored the origin of elevational and latitudinal replacements involved in spatial changes in species assemblages in the Andes. Results We found remarkable genetic structure within the complex, which consists of numerous lineages reaching >12% sequence divergence; most divergent populations occur in areas separated by topographic barriers but several of them, typically not sister to each other, co-occur with elevational segregation on mountain slopes or replace each other with latitude along the Andes. Some close relatives occur in areas separated by thousands of kilometers, with more distant relatives occupying intervening areas. The complex likely originated in the Mexican highlands and expanded extensively in South America while diverging rapidly at a constant rate into many different lineages which have persisted for millions of years. Coalescent analyses consistently revealed that the complex may comprise more than 30 species; while we do not suggest these presumptive species should be recognized by taxonomists in the absence of additional data, H. leucophrys is a distant outlier among New World birds in terms of high lineage diversity within a single recognized species. Main Conclusions Our study captured wood-wren lineages in the act of building up diversity via divergence and persistence in allopatry, achievement of secondary sympatry, and coexistence at the landscape scale mediated by ecological and evolutionary divergence. Although dispersal by wood-wrens is restricted at present and this likely accounts for strong population structure across topographic barriers, their ranges have been dynamic, managing to disperse over much of the montane Neotropics. Phases of expansion and contraction of ranges and localized extinctions of populations likely account for phylogeographic patterns which are precursors to the origin of new species and the accumulation of diversity in tropical mountains.