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.
Highlights
The validity of this hypothesis was brought into question; by functional analyses revealing no discernible effects on oxygen affinity of the variation in hemoglobin sequences between lowland and highland Ruddy Ducks (Natarajan et al, 2015). Such analyses did not rule out the possibility that genetic variants contributed to variation in other structural or functional properties of the hemoglobin protein (Natarajan et al, 2015). Our results suggest this possibility is unlikely given that we found that not all Colombian individuals have the “high-elevation” genotype identified by the earlier study: only 20% of the individuals from Colombia were homozygous for the allele previously thought to be restricted to high elevations, 52% were heterozygous, and 28% had the lowland genotype found in North America
Our work echoes recent suggestions that examining patterns of genetic and phenotypic variation with dense sampling in populations from northern South America is critical to gain a comprehensive understanding of the biogeographic history of species with broad distribution ranges in the Americas (Avendaño, Arbeláez-Cortés, & Cadena, 2017; Pérez-Emán et al, 2017)
Relative to previous analysis, our addition of samples from the Colombian Andes to phylogeographic analyses revealed (1) that the direction of colonization of Ruddy Ducks appears more difficult to determine—and may even be opposite—than that which was previously inferred, and (2) that if adjustment to high-elevation conditions played an important role in colonization of new areas by Ruddy Ducks, it likely occurred through different adaptive mechanisms than those previously considered or via phenotypic plasticity in physiological parameters that remain to be studied
Summary
To complete the geographic sampling of Ruddy Ducks employed in previous analyses, which only considered a handful of specimens from the Cordillera Central of the Colombian Andes (McCracken & Sorenson, 2005), we obtained 26 additional samples from the Cordillera Oriental of Colombia. To determine whether different geographic populations (North America, Colombia, Southern Andes) are genetically distinct clusters, we used the multilocus clustering algorithm in the program STRUCTURE v 2.2.3 (Pritchard, Stephens, & Donnelly, 2000) We based this analysis on our seven-locus data set, where each locus was coded as a haplotype, and included all the individuals for which no more than two of the loci were missing (n = 85 individuals). Genetic structure between populations of Ruddy Ducks varied considerably across the seven loci, with Φst values ranging from 0.12 to 0.61 (Table 1) Despite this variation, genetic differentiation was significant for all population comparisons and loci, except between the Southern Andes and Colombia for the FGB intron. For the βA hemoglobin, 28% of the Colombian individuals were homozygous for the North American low-elevation genotype (Thr-69; Muñoz-Fuentes et al, 2013), 20% were homozygous for the high-altitude Andean genotype (Ser- 69), and 52% were heterozygous (Thr/Ser-69)
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