Philip Lavretsky

Phylogenetics of a recent radiation in the mallards and allies (Aves: Anas): Inferences from a genomic transect and the multispecies coalescent

Reconstructing species trees by incorporating information from many independent gene trees reduces the confounding influence of stochastic lineage sorting. Such analyses are particularly important for taxa that share polymorphisms due to incomplete lineage sorting or introgressive hybridization. We investigated phylogenetic relationships among 14 closely related taxa from the mallard (Anas spp.) complex using the multispecies coalescent and 20 nuclear loci sampled from a genomic transect. We also examined how treating recombining loci and hybridizing species influences results by partitioning the data using various protocols. In general, topologies were similar among the various species trees, with major clades consistently composed of the same taxa. However, relationships among these clades and among taxa within clades changed among partitioned data sets. Posterior support generally decreased when filtering for recombination, whereas excluding mallards (Anas platyrhynchos) increased posterior support for taxa known to hybridize with them. Furthermore, branch lengths decreased substantially for recombination-filtered data. Finally, concordance between nuclear and morphometric topologies conflicted with those in the mitochondrial tree, particularly with regard to the placement of the Hawaiian duck (A. wyvilliana), Philippine duck (A. luzonica), and two spot-billed ducks (A. zonorhyncha and A. poecilorhyncha). These results demonstrate the importance of maximizing sequence length and taxon sampling when inferring taxonomic relationships that are confounded by extensive allele sharing.

Speciation genomics and a role for the Z chromosome in the early stages of divergence between Mexican ducks and mallards

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.

Mito-nuclear discord in six congeneric lineages of Holarctic ducks (genus Anas).

Many species have Holarctic distributions that extend across Europe, Asia and North America. Most genetics research on these species has examined only mitochondrial (mt) DNA, which has revealed wide variance in divergence between Old World (OW) and New World (NW) populations, ranging from shallow, unstructured genealogies to deeply divergent lineages. In this study, we sequenced 20 nuclear introns to test for concordant patterns of OW–NW differentiation between mtDNA and nuclear (nu) DNA for six lineages of Holarctic ducks (genus Anas). Genetic differentiation for both marker types varied widely among these lineages (idiosyncratic population histories), but mtDNA and nuDNA divergence within lineages was not significantly correlated. Moreover, compared with the association between mtDNA and nuDNA divergence observed among different species, OW–NW nuDNA differentiation was generally lower than mtDNA divergence, at least for lineages with deeply divergent mtDNA. Furthermore, coalescent estimates indicated significantly higher rates of gene flow for nuDNA than mtDNA for four of the six lineages. Thus, Holarctic ducks show prominent mito‐nuclear discord between OW and NW populations, and we reject differences in sorting rates as the sole cause of the within‐species discord. Male‐mediated intercontinental gene flow is likely a leading contributor to this discord, although selection could also cause increased mtDNA divergence relative to weak nuDNA differentiation. The population genetics of these ducks contribute to growing evidence that mtDNA can be an unreliable indicator of stage of speciation and that more holistic approaches are needed for species delimitation.

Becoming pure: identifying generational classes of admixed individuals within lesser and greater scaup populations

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.

Genetic admixture supports an ancient hybrid origin of the endangered Hawaiian duck

Speciation is regarded primarily as a bifurcation from an ancestral species into two distinct taxonomic units, but gene flow can create complex signals of phylogenetic relationships, especially among different loci. We evaluated several hypotheses that could account for phylogenetic discord between mitochondrial DNA (mtDNA) and nuclear DNA (nuDNA) within Hawaiian duck (Anas wyvilliana), including stochastic lineage sorting, mtDNA capture and widespread genomic introgression. Our results best support the hypothesis that the contemporary Hawaiian duck is descended from an ancient hybridization event between the mallard (Anas platyrhynchos) and Laysan duck (Anas laysanensis). Whereas mtDNA clearly shows a sister relationship between Hawaiian duck and mallard, nuDNA is consistent with a genetic mosaic with nearly equal contributions from Laysan duck and mallard. In addition, coalescent analyses suggest that gene flow from either mallard or Laysan duck, depending on the predefined tree topology, is necessary to explain contemporary genetic diversity in Hawaiian ducks, and these estimates are more consistent with ancient, rather than contemporary, hybridization. Time since divergence estimates suggest that the genetic admixture event occurred around the Pleistocene–Holocene boundary, which is further supported by circumstantial evidence from the Hawaiian subfossil record. Although the extent of reproductive isolation from either putative parental taxon is not currently known, these species are phenotypically, genetically and ecologically different, and they meet primary criteria used in avian taxonomy for species designation. Thus, the available data are consistent with an admixed origin and support the hypothesis that the Hawaiian duck may represent a young hybrid species.

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

ABSTRACT Of the 13 taxa composing the Mallard complex, 4 occur in North America: the sexually monochromatic American Black Duck (A. rubripes), Mexican Duck (A. [platyrhynchos] diazi), and Mottled Duck (A. fulvigula), and the dichromatic Mallard (Anas platyrhynchos). Although morphologically distinct, inferring the evolutionary relationships of this group is confounded by extensive genic sharing due to incomplete lineage sorting and ongoing hybridization. The objective of this study was to examine the underlying cause (i.e. incomplete lineage sorting vs. contemporary gene flow) of phylogenetic uncertainty. Whereas most taxa were fairly structured at mitochondrial DNA, a “starburst” pattern of divergence consistent with a rapid radiation was recovered with 17 nuclear introns. Furthermore, nuclear-based divergence estimates and tests of population structure recovered Florida and West Gulf Coast Mottled Ducks as well-differentiated and genetically diagnosable from each other and the remaining taxa, whereas Mallards, American Black Ducks, and Mexican Ducks were indistinguishable. In general, neither population structure analyses nor coalescent-based gene flow estimates conclusively identified the presence of hybrids or significant gene flow, suggesting that genetic similarity within the group is largely influenced by incomplete lineage sorting. However, we also cannot reject potentially high levels of gene flow. Moreover, inconsistent relationships among species trees indicated that phylogenetic results were sensitive to which individuals were included. Taxa within the New World group are phenotypically distinguishable, yet genetically similar and seemingly lack the apparent reproductive isolation that is consistent with early stages of (incomplete) speciation. Future work should focus on genomic regions under selection to better understand the stage of speciation among the various incipient forms.

Genetic Population Structure across the Range of Endangered Northeastern Bulrush, Scirpus ancistrochaetus

Premise of research. Determining population structure and the spatial distribution of existing genetic variation is important for prioritizing areas for conservation of endangered species. Specifically, identifying clusters of genetically differentiated populations ensures that the genetic diversity of a species is conserved. Scirpus ancistrochaetus, northeastern bulrush, is a federally endangered wetland sedge, found in eight states in the northeastern United States, for which little information on genetic structure is available. Methodology. We collected leaf samples from 96 separate wetlands spanning seven states and representing over half of all known sites (N = 71 sites). We sequenced eight variable loci, which were used to construct distance-based trees and calculate population-assignment probabilities to investigate population structure, and we tested isolation by distance by correlating genetic similarity with geographic distance among populations. Pivotal results. All plants sampled from the same wetland (i.e., a population) were genetically identical with low heterozygosity, and there was little to no variation among clustered wetlands within a site. Scirpus ancistrochaetus was genetically structured across its range. Notably, all populations from New England were genetically identical to each other but differed from all other populations, and a similar pattern was observed for northern Pennsylvania populations. Three genetic clusters were identified, including a primarily New England cluster, a primarily Pennsylvanian cluster, and a southern Appalachian cluster, and overall, genetic distances were consistent with isolation by distance. Although genetic clusters mostly corresponded with geography, some populations did not show this geographic-genetic association, suggesting long-distance dispersal; for example, one population from West Virginia was assigned to the New England cluster. Overall, the highest genetic diversity was found within Pennsylvania and nearby states. Conclusions. Whether similarity between geographically distant locations is due to animal-mediated gene flow or retention of ancestral alleles needs additional study. Additionally, the development of a large number of new markers may help to reveal diversity in areas such as New England with wetlands that did not have any diversity using our markers. Nevertheless, conservation of different genetic clusters at a regional scale is important for maintaining the genetic diversity of S. ancistrochaetus, particularly in its southern range, where the greater amount of genetic diversity suggests that this region is a reservoir of genetic variation.

Developing major histocompatibility markers in a species of concern: the Sacramento perch Archoplites interruptus

Primers targeting two non-neutral major histocompatibility complex (mhc) II β genes were developed and assayed across several disjoint Sacramento perch Archoplites interruptus sampling locations. Variability at the two mhc loci among sampling stocks strongly correlated to previous estimates with neutral markers, suggesting that the effect of genetic drift was not limited to neutrally evolving regions of the genome. The novel mhc primers will help develop admixture schemes in A. interruptus captive breeding programmes and will increase the success of future reintroductions of this species of concern.