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Genetic structure and biogeographic history of the Bicknell’s Thrush/ Gray-cheeked Thrush species complex

Citation

FitzGerald, Alyssa et al. (2020), Genetic structure and biogeographic history of the Bicknell’s Thrush/ Gray-cheeked Thrush species complex, Dryad, Dataset, https://doi.org/10.5061/dryad.vt4b8gtn1

Abstract

Abstract We examined species limits, admixture, and genetic structure among populations in the Bicknell’s Thrush (Catharus bicknelli)–Gray-cheeked Thrush (C. minimus) species complex to establish the geographic and temporal context of speciation in this group, which is a model system in ecology and a high conservation priority. We obtained mitochondrial ND2 sequences from 186 Bicknell’s Thrushes, 77 Gray-cheeked Thrushes, and 55 individuals of their closest relative, the Veery (C. fuscescens), and genotyped a subset of individuals (n = 72) at 5,633 anonymous single nucleotide polymorphic (SNP) loci. Between-species sequence divergence was an order of magnitude greater than divergence within each species, divergence was dated to the late Pleistocene (420 kbp) based on Bayesian coalescence estimation, and a coalescent model (IMa) revealed almost no gene flow between species based on ND2. SNP data were consistent with mitochondrial results and revealed low levels of admixture among species (3 of 37 Bicknell’s Thrushes, no Gray-cheeked Thrushes, and no Veeries were >2% admixed). Species distribution models projected to the Last Glacial Maximum suggest that Bicknell’s Thrush and Gray-cheeked Thrush resided in primarily allopatric refugia in the late Pleistocene, consistent with the genetic data that support reproductive isolation over an extended period of time. Our genetic data suggest that both species underwent demographic expansions, possibly as they expanded out of Pleistocene refugia into their current ranges. We conclude that Bicknell’s Thrush and Gray-cheeked Thrush are 2 distinct species-level lineages despite low levels of Gray-cheeked Thrush introgression in Bicknell’s Thrushes, and divergence has been maintained by a long history of allopatry in subtly different habitats. Their unique phylogeography among boreal forest birds indicates that either cryptic species breaks in eastern North America are still undiscovered, or another factor, such as divergent natural selection, high migratory connectivity, or interspecific competition, played a role in their divergence.

Methods

DNA extracts were sent to the Institute of Genomic Diversity at Cornell University for genotyping-by-sequencing. High quality DNA extracts (>20 ng/μL) were digested with the restriction enzyme PstI and a unique barcode/adapter combination was ligated to each sample prior to pooling and amplification by PCR. Fragments were pooled with amplicons from other bird species to create three sequencing libraries, with 95 barcoded individuals per library, and sequenced on multiple lanes of a Hi-Seq 2000 Illumina sequencer (Illumina, San Digeo, CA). Each library resulted in ~200 Gbp of raw data. The 100 base pair reads were filtered using the Universal Network Enabled Analysis Kit (UNEAK) pipeline implemented in TASSEL 3.0. Adapter dimers and sequences with an ambiguous base were removed and all reads were trimmed to 64 bp. Identical reads were merged into “tags” within each barcoded individual. Using a pairwise alignment, tags with 1 bp mismatch were retained as candidate SNPs. Candidate SNP loci that were present in fewer than 75% of individuals were removed, and then individuals possessing fewer than 50% of candidate SNPs were removed. To construct genotypes based on sequencing coverage, a maximum-likelihood method with an updated version of the script from White et al. (2013) was implemented; this method retained SNPs with an AIC ≥ 4 units lower than the next best reconstructed genotype. To remove paralogs (duplicated regions within the genome), SNPs with observed heterozygosities ≥ 0.75 were removed. Finally, SNPs present in fewer than 25% of individuals and individuals with fewer than 70% of SNPs were excluded. Following filtering, we retained a dataset of 5633 SNPs from 72 birds, including 37 Bicknell’s Thrushes from locations spanning the species’ entire breeding range, 23 Gray-cheeked Thrushes representing both subspecies and including individuals from Siberia, Alaska, and eastern Canada, a probable late migrating Gray-cheeked Thrush, and a small sample of eastern and western Veeries (n = 11).

Usage Notes

The first column lists the sample identification number; all samples are museum accession numbers; date of collection, location of collection, and species type are listed in FitzGerald et al. (2019) The Auk. Each individual has two rows. The first row is the SNP name. A '0' indicates an uncalled allele.

Funding

Natural Sciences and Engineering Research Council of Canada, Award: RGPIN-2016-06538

Natural Sciences and Engineering Research Council of Canada, Award: 492890

American Museum of Natural History Frank Chapman

Centre for Forest Science and Innovation

University at Albany Benevolent Association