Speciation is a continuous and dynamic process, and studying organisms during the early stages of this process can aid in identifying speciation mechanisms. The mallard (Anas platyrhynchos) and Mexican duck (A. [p.] diazi) are two recently diverged taxa with a history of hybridization and controversial taxonomy. To understand their evolutionary history, we conducted genomic scans to characterize patterns of genetic diversity and divergence across the mitochondrial DNA (mtDNA) control region, 3523 autosomal loci and 172 Z-linked sex chromosome loci. Between the two taxa, Z-linked loci (ΦST = 0.088) were 5.2 times more differentiated than autosomal DNA (ΦST = 0.017) but comparable to mtDNA (ΦST = 0.092). This elevated Z differentiation deviated from neutral expectations inferred from simulated data that incorporated demographic history and differences in effective population sizes between marker types. Furthermore, 3% of Z-linked loci, compared to <0.1% of autosomal loci, were detected as outlier loci under divergent selection with elevated relative (ΦST ) and absolute (dXY ) estimates of divergence. In contrast, the ratio of Z-linked and autosomal differentiation among the seven Mexican duck sampling locations was close to 1:1 (ΦST = 0.018 for both markers). We conclude that between mallards and Mexican ducks, divergence at autosomal markers is largely neutral, whereas greater divergence on the Z chromosome (or some portions thereof) is likely the product of selection that has been important in speciation. Our results contribute to a growing body of literature indicating elevated divergence on the Z chromosome and its likely importance in avian speciation.
Resolving evolutionary relationships and establishing population structure depends on molecular diagnosability that is often limited for closely related taxa. Here, we use 3,200 ddRAD‐seq loci across 290 mallards, American black ducks, and putative hybrids to establish population structure and estimate hybridization rates. We test between traditional assignment probability and accumulated recombination events based analyses to assign hybrids to generational classes. For hybrid identification, we report the distribution of recombination events complements ADMIXTURE simulation by extending resolution past F4 hybrid status; however, caution against hybrid assignment based on accumulated recombination events due to an inability to resolve F1 hybrids. Nevertheless, both analyses suggest that there are relatively few backcrossed stages before a lineage's hybrid ancestry is lost and the offspring are effectively parental again. We conclude that despite high rates of observed interspecific hybridization between mallards and black ducks in the middle part of the 20th century, our results do not support the predicted hybrid swarm. Conversely, we report that mallard samples genetically assigned to western and non‐western clusters. We indicate that these non‐western mallards likely originated from game‐farm stock, suggesting landscape level gene flow between domestic and wild conspecifics.
Along with manipulating habitat, the direct release of domesticated individuals into the wild is a practice used worldwide to augment wildlife populations. We test between possible outcomes of human‐mediated secondary contact using genomic techniques at both historical and contemporary timescales for two iconic duck species. First, we sequence several thousand ddRAD‐seq loci for contemporary mallards (Anas platyrhynchos) throughout North America and two domestic mallard types (i.e., known game‐farm mallards and feral Khaki Campbell's). We show that North American mallards may well be becoming a hybrid swarm due to interbreeding with domesticated game‐farm mallards released for hunting. Next, to attain a historical perspective, we applied a bait‐capture array targeting thousands of loci in century‐old (1842–1915) and contemporary (2009–2010) mallard and American black duck (Anas rubripes) specimens. We conclude that American black ducks and mallards have always been closely related, with a divergence time of ~600,000 years before present, and likely evolved through prolonged isolation followed by limited bouts of gene flow (i.e., secondary contact). They continue to maintain genetic separation, a finding that overturns decades of prior research and speculation suggesting the genetic extinction of the American black duck due to contemporary interbreeding with mallards. Thus, despite having high rates of hybridization, actual gene flow is limited between mallards and American black ducks. Conversely, our historical and contemporary data confirm that the intensive stocking of game‐farm mallards during the last ~100 years has fundamentally changed the genetic integrity of North America's wild mallard population, especially in the east. It thus becomes of great interest to ask whether the iconic North American mallard is declining in the wild due to introgression of maladaptive traits from domesticated forms. Moreover, we hypothesize that differential gene flow from domestic game‐farm mallards into the wild mallard population may explain the overall temporal increase in differentiation between wild black ducks and mallards, as well as the uncoupling of genetic diversity and effective population size estimates across time in our results. Finally, our findings highlight how genomic methods can recover complex population histories by capturing DNA preserved in traditional museum specimens.
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Recently evolved species typically share genetic variation across their genomes due to incomplete lineage sorting and/or ongoing gene flow. Given only subtle allele frequency differences at most loci and the expectation that divergent selection may affect only a tiny fraction of the genome, distinguishing closely related species based on multi‐locus data requires substantial genomic coverage. In this study, we used ddRAD‐seq to sample the genomes of five recently diverged, New World “mallards” (Anas spp.), a group of dabbling duck species characterized by diagnosable phenotypic differences but minimal genetic differentiation. With increased genomic sampling, we aimed to characterize population structure within this group and identify genomic regions that may have experienced divergent selection during speciation. We analyzed 3,017 autosomal ddRAD‐seq loci and 177 loci from the Z‐chromosome. In contrast to previous studies, the ddRAD‐seq data were sufficient to assign individuals to their respective species or subspecies and to generate estimates of gene flow in a phylogenetic framework. We find limited evidence of contemporary gene flow between the dichromatic mallard and several monochromatic taxa, but find evidence for historical gene flow between some monochromatic species pairs. We conclude that the overall genetic similarity of these taxa likely reflects retained ancestral polymorphism rather than recent and extensive gene flow. Thus, despite recurring cases of hybridization in this group, our results challenge the current dogma predicting the genetic extinction of the New World monochromatic dabbling ducks via introgressive hybridization with mallards. Moreover, ddRAD‐seq data were sufficient to identify previously unknown outlier regions across the Z‐chromosome and several autosomal chromosomes that may have been involved in the diversification of species in this recent radiation.
Estimating the frequency of hybridization is important to understand its evolutionary consequences and its effects on conservation efforts. In this study, we examined the extent of hybridization in two sister species of ducks that hybridize. We used mitochondrial control region sequences and 3589 double-digest restriction-associated DNA sequences (ddRADseq) to identify admixture between wild lesser scaup (Aythya affinis) and greater scaup (A. marila). Among 111 individuals, we found one introgressed mitochondrial DNA haplotype in lesser scaup and four in greater scaup. Likewise, based on the site-frequency spectrum from autosomal DNA, gene flow was asymmetrical, with higher rates from lesser into greater scaup. However, using ddRADseq nuclear DNA, all individuals were assigned to their respective species with >0.95 posterior assignment probability. To examine the power for detecting admixture, we simulated a breeding experiment in which empirical data were used to create F1 hybrids and nine generations (F2-F10) of backcrossing. F1 hybrids and F2, F3 and most F4 backcrosses were clearly distinguishable from pure individuals, but evidence of admixed histories was effectively lost after the fourth generation. Thus, we conclude that low interspecific assignment probabilities (0.011-0.043) for two lesser and nineteen greater scaup were consistent with admixed histories beyond the F3 generation. These results indicate that the propensity of these species to hybridize in the wild is low and largely asymmetric. When applied to species-specific cases, our approach offers powerful utility for examining concerns of hybridization in conservation efforts, especially for determining the generational time until admixed histories are effectively lost through backcrossing.
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