Old divergence and restricted gene flow between torrent duck (Merganetta armata) subspecies in the Central and Southern Andes

Aim: To investigate the structure and rate of gene flow among populations of habitat-specialized species to understand the ecological and evolutionary processes underpinning their population dynamics and historical demography, including speciation and extinction. Location: Peruvian and Argentine Andes. Taxon: Two subspecies of torrent duck (Merganetta armata). Methods: We sampled 156 individuals in Peru (M. a. leucogenis; Chillon River, n = 57 and Pachachaca River, n = 49) and Argentina (M. a. armata; Arroyo Grande River, n = 33 and Malargue River, n = 17), and sequenced the mitochondrial DNA (mtDNA) control region to conduct coarse and fine-scale demographic analyses of population structure. Additionally, to test for differences between subspecies, and across genetic markers with distinct inheritance patterns, a subset of individuals (Peru, n = 10 and Argentina, n = 9) was subjected to partial genome resequencing, obtaining 4,027 autosomal and 189 Z-linked double-digest restriction-associated DNA sequences. Results: Haplotype and nucleotide diversities were higher in Peru than Argentina across all markers. Peruvian and Argentine subspecies showed concordant species-level differences (ΦST mtDNA = 0.82; ΦST autosomal = 0.30; ΦST Z chromosome = 0.45), including no shared mtDNA haplotypes. Demographic parameters estimated for mtDNA using IM and IMa2 analyses, and for autosomal markers using ∂a∂i (isolation-with-migration model), supported an old divergence (mtDNA = 600,000 years before present (ybp), 95% HPD range = 1.2 Mya to 200,000 ybp; and autosomal ∂a∂i = 782,490 ybp), between the two subspecies, characteristic of deeply diverged lineages. The populations were well-differentiated in Argentina but moderately differentiated in Peru, with low unidirectional gene flow in each country. Main conclusions: We suggest that the South American Arid Diagonal was preexisting and remains a current phylogeographic barrier between the ranges of the two torrent duck subspecies, and the adult territoriality and breeding site fidelity to the rivers define their population structure.