Coast to coast: High genomic connectivity in North American scoters

Abstract

Dispersal shapes demographic processes and therefore is fundamental to understanding biological, ecological, and evolutionary processes acting within populations. However, assessing population connectivity in scoters (Melanitta sp.) is challenging as these species have large spatial distributions that span remote landscapes, have varying nesting distributions (disjunct vs. continuous), exhibit unknown levels of dispersal, and vary in the timing of the formation of pair bonds (winter vs. fall/spring migration) that may influence the distribution of genetic diversity. Here, we used double‐digest restriction‐associated DNA sequence (ddRAD) and microsatellite genotype data to assess population structure within the three North American species of scoter (black scoter, M. americana; white‐winged scoter, M. deglandi; surf scoter, M. perspicillata), and between their European congeners (common scoter, M. nigra; velvet scoter, M. fusca). We uncovered no or weak genomic structure (ddRAD ΦST < 0.019; microsatellite FST < 0.004) within North America but high levels of structure among European congeners (ddRAD ΦST > 0.155, microsatellite FST > 0.086). The pattern of limited genomic structure within North America is shared with other sea duck species and is often attributed to male‐biased dispersal. Further, migratory tendencies (east vs. west) of female surf and white‐winged scoters in central Canada are known to vary across years, providing additional opportunities for intracontinental dispersal and a mechanism for the maintenance of genomic connectivity across North America. In contrast, the black scoter had relatively elevated levels of divergence between Alaska and Atlantic sites and a second genetic cluster found in Alaska at ddRAD loci was concordant with its disjunct breeding distribution suggestive of a dispersal barrier (behavioral or physical). Although scoter populations appear to be connected through a dispersal network, a small percentage (<4%) of ddRAD loci had elevated divergence which may be useful in linking areas (nesting, molting, staging, and wintering) throughout the annual cycle.

High site fidelity does not equate to population genetic structure for common goldeneye and Barrow's goldeneye in North America

“…2) is consistent with the genomes of these two species being under similar evolutionary constrains. This ratio indicates an evolutionary scenario in which the genomes of Barrow's goldeneye and common goldeneye have largely diverged neutrally and in allopatry (where we expect a Z-chromosome to autosomal Φ ST ratio of ≤ 1.33; Caballero 1995, Whitlock and McCauley 1999, Dean et al 2015, as is also the case between other sister taxa of scaup (Lavretsky et al 2016) and scoters (Sonsthagen et al 2019). Thus, here we provide evidence that the divergence of the two goldeneye species is likely the result of a relatively deep evolutionary split, and that these two species have likely been evolving under neutral conditions and largely independent from one another throughout their evolutionary histories.…”

“…Once again this finding is in contrast to all other Holarctic sea duck species for which range‐wide genomic structure has been assessed (e.g. common eider nuclear introns Φ ST = 0.000–0.208, Sonsthagen et al 2011; common merganser nuclear introns Φ ST = 0.254–0.274, Peters et al 2012; black scoter Melanitta americana ddRAD Φ ST = 0.196–0.200, white‐winged scoter M. deglandi ddRAD Φ ST = 0.155–0.160, Sonsthagen et al 2019). The finding that common goldeneye appears unstructured across the Atlantic Ocean suggests that dispersal between Eurasia and North America is potentially more common than previously thought.…”

“…Specifically, we aim to test whether patterns of regional (Alaska, Yukon, Ontario) genetic differentiation within both species at autosomal and sex‐linked (Z‐chromosome) loci correspond to population structure identified by previous analyses of band recovery and maternally‐inherited mtDNA data (Pearce et al 2014). Given high wintering site fidelity (where pair formation likely occurs), high mtDNA differentiation ( F ST = 0.58; Pearce et al 2014) and strong intra‐specific nuclear genetic structure detected in other sea duck species (common eider, Somateria mollissima ; Sonsthagen et al 2011, but see Pearce et al 2004, 2005, Wilson et al 2016, Sonsthagen et al 2019, 2020b), we expect to find some level of structure in the nuclear genome. Despite high breeding site fidelity, a lack of genetic structure in Barrow's goldeneye along the Pacific Coast or common goldeneye between sampling regions would suggest that wintering areas are likely used by individuals hatched from multiple nesting regions, or that an initial dispersal event of juveniles acts to homogenize genetic diversity.…”

“…Delineating population boundaries is critical for understanding demography, migratory connectivity and population dynamics, which are all important factors in effective management and conservation (Lande 1988, Supple and Shapiro 2018, Sonsthagen et al 2019). However, directly documenting regional population structure and individual dispersal events can be challenging, especially for species that reside in remote landscapes and occupy large distributions across their annual cycle (Lavretsky et al 2016, Sonsthagen et al 2019).…”

“…High site fidelity does not equate to population genetic structure for common goldeneye and Barrow's goldeneye in North America Introduction Delineating population boundaries is critical for understanding demography, migratory connectivity and population dynamics, which are all important factors in effective management and conservation (Lande 1988, Supple and Shapiro 2018, Sonsthagen et al 2019. However, directly documenting regional population structure and individual dispersal events can be challenging, especially for species that reside in remote landscapes and occupy large distributions across their annual cycle (Lavretsky et al 2016, Sonsthagen et al 2019. Quantifying genetic structure and rates and directionality of gene flow within a species can provide valuable information on these various stochastic and demographic factors.…”