Genomic and phenotypic divergence-with-gene-flow across an ecological and elevational gradient in a neotropical bird

Abstract

Aim: Some species have populations that vary in ecologically relevant traits along environmental gradients, which is a pattern often generated by secondary contact post divergence in allopatry. However, an alternative explanation for such a pattern would be primary contact, where populations diverge in the presence of gene flow through the action of strong natural selection. We aimed to test the divergence-with-gene-flow model across an environmental gradient in a Chaco-Andes dry forest bird. Location: Central Andes Mountain range and Chaco region of Argentina and Bolivia. Taxon: Phytotoma rutila (Aves, Cotingidae). Methods: We generated ddRADseq loci for 23 individuals and obtained body size variation data for 146 museum specimens. We evaluated population genetic structure and tested the effects of elevation and isolation by geographic distance on genomic divergence. To distinguish divergence in allopatry from divergence-with-gene-flow, we compared the divergence of phenotypic traits (bill, tarsus and wing) with neutral genomic variation (S-test and PST–FST comparisons), conducted coalescent analyses to estimate gene flow and divergence time, and calculated relative (FST) versus absolute (DXY) genomic divergence. Results: We found (a) P. rutila differs genomically and phenotypically following the highland-lowland axis of the study region, with altitudinal variation explaining genomic variation; (b) larger phenotypic than neutral genomic divergence; (c) asymmetric gene flow between Andean and Chacoan populations; and (d) a pattern of relative and absolute genomic differentiation compatible with divergence-with-gene-flow. Main conclusions: The mechanism behind the morphological and genomic diversification along the Chaco-Andes dry forest belt in P. rutila is divergence-with-gene-flow. Diversification in South America implicates gene flow between populations and natural selection following environmental gradients, as well as vicariance. This complex combination contrasts with the traditional idea that speciation in birds occurred primarily in allopatry.