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(Sylvilagus Transitionalis) and Cross‑Amplifcation in the Eastern Cottontail (S

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(Sylvilagus Transitionalis) and Cross‑Amplifcation in the Eastern Cottontail (S King et al. BMC Res Notes (2017) 10:741 https://doi.org/10.1186/s13104-017-3062-2 BMC Research Notes RESEARCH NOTE Open Access Microsatellite marker development from next‑generation sequencing in the New England cottontail (Sylvilagus transitionalis) and cross‑amplifcation in the eastern cottontail (S. foridanus) Timothy L. King1, Michael Eackles1, Aaron Aunins2*, Thomas J. McGreevy Jr.3, Thomas P. Husband3, Anthony Tur4 and Adrienne I. Kovach5 Abstract Objective: The New England cottontail (Sylvilagus transitionalis) is a species of high conservation priority in the Northeastern United States, and was a candidate for federal listing under the Endangered Species Act until a recent decision determined that conservation actions were sufcient to preclude listing. The aim of this study was to develop a suite of microsatellite loci to guide future research eforts such as the analysis of population genetic struc- ture, genetic variation, dispersal, and genetic mark-recapture population estimation. Results: Thirty-fve microsatellite markers containing tri- and tetranucleotide sequences were developed from shotgun genomic sequencing of tissue from S. transitionalis, S. obscurus, and S. foridanus. These loci were screened in n 33 wild S. transitionalis sampled from a population in eastern Massachusetts, USA. Thirty-two of the 35 loci were polymorphic= with 2–6 alleles, and observed heterozygosities of 0.06–0.82. All loci conformed to Hardy–Weinberg Equilibrium proportions and there was no evidence of linkage disequilibrium or null alleles. Primers for 33 of the 35 loci amplifed DNA extracted from n 6 eastern cottontail (S. foridanus) samples, of which nine revealed putative species-diagnostic alleles. These loci =will provide a useful tool for conservation genetics investigations of S. transitiona- lis and a potential diagnostic species assay for diferentiating sympatric eastern and New England cottontails. Keywords: Microsatellites, Cross-amplifcation, Sylvilagus transitionalis, Sylvilagus foridanus, Sylvilagus obscurus, Next- generation sequencing Introduction [5]. Remnant New England cottontail populations are Te New England cottontail (Sylvilagus transitionalis) is found today in < 14% of the species’ historical range a narrow niche specialist that relies on the dense under- and occur in fve geographically and genetically distinct story vegetation of early successional or shrubland habi- populations located in southern Maine and southeast- tats [1]. Tese ephemeral habitats have declined steeply ern New Hampshire, central New Hampshire, eastern in recent decades in the Northeastern United States Massachusetts on Cape Cod, eastern Connecticut and [2–4]. As a result, many shrubland species, including the Rhode Island, and western Connecticut and New York New England cottontail, face severe population declines [5]. Within these areas, cottontails face the consequences of population isolation and loss of genetic diversity [6, 7]. *Correspondence: [email protected] As a result of uncertainty in long-term species’ viability, 2 Natural Systems Analysts, Leetown Science Center, 11649 Leetown the New England cottontail is a high priority for conser- Road, Kearneysville, WV 25430, USA Full list of author information is available at the end of the article vation in the Northeastern United States. To help recover © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. King et al. BMC Res Notes (2017) 10:741 Page 2 of 7 the species, state and Federal natural resource managers A universal M13 sequence was added to the 5′ end of collaborated with academicians and other stakehold- either the forward or reverse primer of each primer pair ers to develop and implement a conservation strategy to enabling an M13 FAM labeled fuorescent dye comple- improve the outlook for the species [8]. As a result, the mentary to the universal tail to be incorporated into the United States Fish and Wildlife Service determined list- polymerase chain reaction (PCR) product [13]. Polymer- ing of the species under the Endangered Species Act was ase chain reactions were performed in 25 μl volumes, no longer warranted [9]. Despite this decision, much consisting of 10 ng of DNA, 1 X PCR Bufer (Promega, uncertainty remains about the species’ viability and pop- Madison, WI), 0.25 μM of labeled forward primer, ulation status [7, 10]. To evaluate the efectiveness of the 0.5 μM of unlabeled reverse primer, 0.1 μM of labeled conservation strategy and inform adaptive modifcations M13, 2.0 mM MgCl 2, 0.2 mM of each dNTP, 0.25 units/μl to improve outcomes, extensive population monitoring Bovine Serum Albumin (New England Biolabs, Ipswich, and research into population structure and genetic diver- MA), and 0.06 units/μl of Taq polymerase (Promega), sity are needed [8]. To this end, our goal was to develop a using the following cycling conditions: 94 °C for 15 min, suite of microsatellite markers to aid future conservation 29 cycles of 94 °C for 1 min, 58 °C for 45 s, and 72 °C for genetics research on the New England cottontail as well 45 s, 5 cycles of 94 °C for 1 min, 52 °C for 45 s, and 72 °C as other Sylvilagus species. for 45 s, all followed by 72 °C for 10 min. PCR products for each locus were electrophoresed separately on an ABI Main text 3130 Genetic Analyzer (TermoFisher Scientifc) auto- Methods mated DNA sequencer. Alleles were called using Gen- For microsatellite marker development, total genomic eMapper (ver. 4) (TermoFisher Scientifc) following the DNA was extracted from tissue samples obtained from protocols described in [14]. 13 New England cottontail, one eastern cottontail (S. Loci that amplifed consistently and were easily score- foridanus), and two Appalachian cottontail (S. obscurus) able on the sample of n = 8 wild New England cottontails using the DNEasy Blood and Tissue kit (Qiagen, Ger- were then tested on DNA extracted from an additional mantown, MD). We chose to sequence multiple species sample of n = 33 New England cottontails from a wild to maximize the number of microsatellites available for population in eastern Massachusetts, on Cape Cod. In screening in the target species S. transitionalis. Sequenc- addition, DNA extracted from a sample of n = 6 sympa- ing libraries were created from these genomic DNA sam- tric eastern cottontails, also collected from eastern Mas- ples for sequencing on the Ion Torrent PGM and Ion sachusetts were tested for cross-species amplifcation. Proton (TermoFisher Scientifc, Frederick, MD). For each sequencing library, the extracted DNA was quanti- Data analyses fed with a Nanodrop spectrophotometer (TermoFisher Genotype data from the Cape Cod New England cot- Scientifc), and 100 ng of DNA from each individual was tontail collection (n = 33) were analyzed for null alleles, used for construction of multiple 200 base pair libraries large allele dropout, and scoring errors using MICRO- following the manufacturer’s protocol. For libraries with CHECKER (ver 2.2.3) [15]. Genetic diversity and het- multiple individuals in one run, equimolar proportions of erozygosity were quantifed using GenAlEx 6.5 [16, 17]. each library were pooled prior to chip loading. Exact tests in GENEPOP [18] were used to determine Sequence reads from each completed run were if genotypes at each locus conformed to Hardy–Wein- imported into Qiagen CLC Genomics Workbench (ver. berg equilibrium (HWE). Multi-locus tests of conform- 7) for processing. Reads were length trimmed to a mini- ance to HWE were completed using Fisher’s method in mum size of 30 bp, and the quality trimming threshold GENEPOP. Linkage disequilibrium (LD) was tested for was set to 0.01 corresponding to a Phred score of 20. all pairs of loci using contingency tables in GENEPOP. Sequence reads from each of the 5 separate runs were All tests of HWE and LD tests in GENEPOP used the then screened individually for all possible di-, tri-, tetra, default Markov chain parameters. Signifcance levels for penta-, and hexanucleotide microsatellite repeat motifs HWE and LD tests were adjusted using the sequential with a minimum repeat length of fve with the program Bonferroni correction [19]. QDD (ver. 3) [11]. Primers were designed for each puta- To evaluate the utility of these loci for population tive microsatellite locus within QDD using the integrated genetic studies, multiple analyses were performed with PRIMER 3 code [12]. Seventy-fve tri- and tetra nucleo- the n = 33 New England cottontail collection. All multi- tide loci identifed by QDD with predicted amplifed locus genotypes were subjected to analysis via GENECAP lengths between 100 and 250 bp were selected for screen- [20] to identify matching samples, calculate match prob- ing within a collection of n = 8 wild-caught New Eng- abilities, and estimate the sibling probability of identity land cottontails sampled from across the species range. (PIsibs) [21]. To assess the randomness of the collection King et al. BMC Res Notes (2017) 10:741 Page 3 of 7 (e.g., to ensure the collection did not consist of a small and
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