Neutral and functionally important genes shed light on phylogeography and the history of high‐altitude colonization in a widespread New World duck

Abstract

Phylogeographic studies often infer historical demographic processes underlying species distributions based on patterns of neutral genetic variation, but spatial variation in functionally important genes can provide additional insights about biogeographic history allowing for inferences about the potential role of adaptation in geographic range evolution. Integrating data from neutral markers and genes involved in oxygen (O2)‐transport physiology, we test historical hypotheses about colonization and gene flow across low‐ and high‐altitude regions in the Ruddy Duck (Oxyura jamaicensis), a widely distributed species in the New World. Using multilocus analyses that for the first time include populations from the Colombian Andes, we also examined the hypothesis that Ruddy Duck populations from northern South America are of hybrid origin. We found that neutral and functional genes appear to have moved into the Colombian Andes from both North America and southern South America, and that high‐altitude Colombian populations do not exhibit evidence of adaptation to hypoxia in hemoglobin genes. Therefore, the biogeographic history of Ruddy Ducks is likely more complex than previously inferred. Our new data raise questions about the hypothesis that adaptation via natural selection to high‐altitude conditions through amino acid replacements in the hemoglobin protein allowed Ruddy Ducks to disperse south along the high Andes into southern South America. The existence of shared genetic variation with populations from both North America and southern South America as well as private alleles suggests that the Colombian population of Ruddy Ducks may be of old hybrid origin. This study illustrates the breadth of inferences one can make by combining data from nuclear and functionally important loci in phylogeography, and underscores the importance of complete range‐wide sampling to study species history in complex landscapes.

Molecular and morphological differentiation among Torrent Duck (Merganetta armata) populations in the Andes

“…The star‐like shape of the haplotype network (Figure b) revealed a presumably ancestral haplotype present in all populations and at least one private haplotype for each main clade recovered using the mtDNA data. Although geographic variation in haemoglobin genes has been previously documented (Lozano‐Jaramillo et al, ), the presence of private alleles is interesting in a gene often subject to intense natural selection and supports a long history of isolation among lineages. Most of the haemoglobin polymorphisms were located at introns and one non‐synonymous substitution was found, corresponding to the previously described Ala/Thr‐α77 substitution (McCracken, Barger, Bulgarella, Johnson, Sonsthagen, et al, ); this substitution appears to occur only in the Central Andes (Figures c and b) and was not sampled at high elevation or moderately high elevation in the Argentine or Colombian populations, respectively.…”

“…Classic ideas about barriers and climate influencing population divergence have been confirmed by a variety of more recent studies examining patterns of genetic differentiation and evolutionary relationships of birds from Andean cloud forests (Cadena, ; Chaves & Smith, , Parra, Remsen, Alvarez‐Rebolledo, & Mcguire, ; Prieto‐Torres, Cuervo, & Bonaccorso, ; Quintero, Ribas, & Cracraft, ; Rheindt, Cuervo, & Brumfield, ; Ribas, Moyle, Miyaki, Cracraft, ; Sedano & Burns, ; Van Doren et al, ; Weir et al, ; Winger et al, , Winger, ; see additional references in Avendaño, Arbeláez‐Cortés, & Cadena, ). The increasing integration of molecular data sets with data describing geographic variation in plumage, morphometrics, ecology and physiology has further advanced studies of avian speciation in the Andes, enabling a more complete understanding of patterns and processes involved in diversification (Benham & Witt, ; Lozano‐Jaramillo et al, ; Milá, Wayne, Fitze, & Smith, ; Natarajan et al, ; Seeholzer & Brumfield, ; Winger & Bates, ). Nonetheless, to fully understand how historical and evolutionary processes have influenced species histories to result in contemporary patterns of avian diversity in the Andes, one needs studies of differentiation across species with varying habitat preferences and life histories.…”

“…Prior to this study, no phylogeographic analysis had focused on Andean birds sharing latitudinal and elevational distributions with cloud forest birds yet differing in habitat preferences due to their association with riverine/aquatic environments. Although there are several studies on the phylogeography of Neotropical waterfowl species (Bulgarella et al, ; Lozano‐Jaramillo et al, ; McCracken, Bulgarella, et al, ; Muñoz‐Fuentes, Cortázar‐Chinarro, Lozano‐Jaramillo, & McCracken, ; Wilson, Peters, McCracken ), none of them focused on species associated with rivers on forested slopes. Furthermore, ours is the first analysis of Andean waterfowl species considering variation in mitochondrial and nuclear genes across the range of a widespread species in the light of quantitative estimates of morphological differentiation among populations.…”

“…However, we do not interpret patterns of HBA2 variation in the context of adaptive evolution because (a) experimental evidence documenting functional differences in observed substitutions is lacking, and (b) Torrent Ducks sampled at all elevations (low and high) exhibited the same relatively high Hb‐O 2 affinity, comparatively left‐shifted to low‐altitude waterfowl populations (Natarajan et al, ). Thus, our analyses of the biparentally inherited nuclear HBA2 and the maternally inherited control region served to provide complementary insights from neutral and functionally important loci about the biogeographical history of species (Lozano‐Jaramillo, McCracken, & Cadena, ).…”

PRIMEROS REGISTROS DE Oxyura jamaicensis andina EN ECUADOR

“…Se ha propuesto que O. j. andina podría considerarse como una especie y que la variabilidad fenotípica existente en la población no es el resultado de la afluencia reciente de individuos de otras poblaciones (Lozano-Jaramillo et al, 2018). Sin embargo, los individuos registrados en Ecuador reflejan evidente variación, con fenotipos más cercanos a O. j. ferruginea, que tiene cabeza y cuello completamente negros y es la subespecie previamente registrada en Ecuador (Ridgely & Greenfield, 2006;McMullan & Navarrete, 2017).…”