Rapid radiation and hybridization contribute to weak differentiation and hinder phylogenetic inferences in the New World Mallard complex (<i>Anas</i>spp.)

Lavretsky, Philip; Hernández‐Baños, Blanca E.; Peters, Jeffrey L.

doi:10.1642/auk-13-164.1

Cited by 30 publications

(75 citation statements)

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“…ybp = 632,305, range = 166,166–2,076,004 ybp) data sets. Our estimated divergence times between black ducks and wild mallards are on average greater than previously suggested (180,000 ybp (95% CI = 100,000–400,000 ybp); Lavretsky, Hernández Baños, et al, ), which may be due to the much smaller set of used loci (17 nuclear introns) and samples (25 per species) analysed previously. Finally, we recovered a relatively low migration rate of approximately two to three migrants per generation whether analysing historical (1.87 migrants per generation, range = 0.04–8.44 migrants per generation) or contemporary (2.82 migrants per generation, range = 0.21–9.72 migrants per generation) data sets.…”

Section: Resultscontrasting

confidence: 75%

“…Trimmomatic (Bolger, Lohse, & Usadel, ) was used to trim or discard poor quality sequences. The Burrows Wheeler Aligner v. 07.15 (bwa; Li & Durbin, ) program was used to index and align per sample sequences to our reference—comprised of initial ddRAD sequences used to build the capture array and a consensus mtDNA sequence of mallards and black ducks (Lavretsky, Hernández Baños, & Peters, ; Lavretsky, McCracken, et al, )—using optimized parameters as described in Schubert et al (; ‐T 25 ‐I 1024). Due to known postmortem degradation effects on DNA, we used MapDamage v 2.0 (Jónsson, Ginolhac, Schubert, Johnson, & Orlando, ) to rescale the base scores of historical samples based on patterns of DNA fragmentation and cytosine deamination.…”

Section: Methodsmentioning

confidence: 99%

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Assessing changes in genomic divergence following a century of human‐mediated secondary contact among wild and captive‐bred ducks

et al. 2020

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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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Section: Methodsmentioning

confidence: 99%

Assessing changes in genomic divergence following a century of human‐mediated secondary contact among wild and captive‐bred ducks

et al. 2020

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“…Next, to visualize patterns of differentiation across the genome, pairwise per locus Φ ST values were calculated in the r package PopGenome (Pfeifer et al, ), and plotted in excel by chromosomal position (i.e., Manhattan plots). BayeScan v. 2.1 (Foll & Gaggiotti, ), which has relatively low rates of false positives (<1%) for populations with low overall differentiation (Pérez‐Figueroa, García‐Pereira, Saura, Rolán‐Alvarez, & Caballero, ), as is observed in the NW “mallard” radiation ( Φ ST estimates range from 0.011 to 0.043; Lavretsky, Hernández Baños, et al, ), was used to test for outlier loci. BayeScan employs a reversible‐jump MCMC method by calculating a posteriori probability models with and without selection across loci.…”

Section: Methodsmentioning

confidence: 99%

“…Among the monochromatic species, black ducks have the highest rates of hybridization and introgression with mallards (Lavretsky, Janzen, & McCracken, ), and previous studies have suggested either that the two forms are conspecific (Ankney et al, ), or that black ducks have suffered a complete breakdown of their genetic distinctiveness (Mank, Carlson, & Brittingham, ). Although the frequency of mixed pairs and hybrid individuals remains uncertain (Heusmann, ; Johnsgard, ; Kirby, Reed, Dupuis, Obrecht, & Quist, ), black ducks and mallards are genetically indistinguishable based on allozymes (Ankney et al, ), microsatellites (Mank et al, ), and sequence data from a limited number of mitochondrial and nuclear genes (Johnson & Sorenson, ; Lavretsky, Hernández Baños, & Peters, ; Lavretsky, McCracken, et al, ; McCracken et al, ). ddRAD‐seq methods, however, have provided sufficient genomic coverage and allele frequency differences to identify population structure, hybrid individuals, founder events, and genomic regions putatively under divergent selection between mallards and Mexican ducks (Lavretsky et al, ), between the two mottled duck subspecies (Peters et al, ), and more recently between mallards and black ducks (Lavretsky et al, ).…”

Section: Introductionmentioning

confidence: 99%

ddRAD‐seq data reveal significant genome‐wide population structure and divergent genomic regions that distinguish the mallard and close relatives in North America

et al. 2019

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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.

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“…Among these lineages, the genus Anas (i.e. the dabbling ducks) seems particularly predisposed for global radiations (Johnson and Sorenson , Proches and Ramdhani , Lavretsky et al ), which is likely attributable to their vagile tendencies. Within the genus Anas , the blue‐winged duck complex, named after their prominent blue wing patch, inhabits all continents except Antarctica and comprises six species, including the northern shoveler A. clypeata , the red shoveler A. platalea , the Cape shoveler A. smithii , the Australasian shoveler A. rhynchotis , the blue‐winged teal A. discors , and the cinnamon teal A. cyanoptera .…”

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Divergence and gene flow in the globally distributed blue‐winged ducks

Nelson

Wilson

McCracken

et al. 2017

Journal of Avian Biology

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The ability to disperse over long distances can result in a high propensity for colonizing new geographic regions, including uninhabited continents, and lead to lineage diversification via allopatric speciation. However, high vagility can also result in gene flow between otherwise allopatric populations, and in some cases, parapatric or divergence‐with‐gene‐flow models might be more applicable to widely distributed lineages. Here, we use five nuclear introns and the mitochondrial control region along with Bayesian models of isolation with migration to examine divergence, gene flow, and phylogenetic relationships within a cosmopolitan lineage comprising six species, the blue‐winged ducks (genus Anas), which inhabit all continents except Antarctica. We found two primary sub‐lineages, the globally‐distributed shoveler group and the New World blue‐winged/cinnamon teal group. The blue‐winged/cinnamon sub‐lineage is composed of sister taxa from North America and South America, and taxa with parapatric distributions are characterized by low to moderate levels of gene flow. In contrast, our data support strict allopatry for most comparisons within the shovelers. However, we found evidence of gene flow from the migratory, Holarctic northern shoveler A. clypeata and the more sedentary, African Cape shoveler A. smithii into the Australasian shoveler A. rhynchotis, although we could not reject strict allopatry. Given the diverse mechanisms of speciation within this complex, the shovelers and blue‐winged/cinnamon teals can serve as an effective model system for examining how the genome diverges under different evolutionary processes and how genetic variation is partitioned among highly dispersive taxa.

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Rapid radiation and hybridization contribute to weak differentiation and hinder phylogenetic inferences in the New World Mallard complex (Anasspp.)

Abstract: BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.

Cited by 30 publications

References 98 publications

Assessing changes in genomic divergence following a century of human‐mediated secondary contact among wild and captive‐bred ducks

Assessing changes in genomic divergence following a century of human‐mediated secondary contact among wild and captive‐bred ducks

ddRAD‐seq data reveal significant genome‐wide population structure and divergent genomic regions that distinguish the mallard and close relatives in North America

Divergence and gene flow in the globally distributed blue‐winged ducks

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