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Hierarchical population structure of a rare lagomorph indicates recent fragmentation has disrupted metapopulation function

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Abstract

An understanding of genetic diversity and population structure is important to the conservation of declining species within fragmented habitats. These issues become critical for small, isolated populations, in which stochasticity is a main driver of genetic change and possibly of population extinction. In eastern New York and New England the endemic New England cottontail has declined due to habitat loss and fragmentation. As a species that exhibits metapopulation dynamics, habitat fragmentation can have profound implications for its persistence. We examined genetic diversity, population structure, and effective population size (Ne) of New England cottontails in New York, a purported remnant stronghold for the species. We amplified ten microsatellite loci from tissues collected from live-captures and from fecal pellets. We investigated potential hierarchical population structuring using programs STRUCTURE and BAPS. STRUCTURE identified four hierarchical tiers consisting of nine clusters, and BAPS clustering was highly consistent with that given by STRUCTURE. Most populations displayed significant genetic differentiation (FST = 0.04–0.34) and little to no evidence of ongoing connectivity. Low genetic diversity was observed based on allelic richness (2.2–3.0), and all populations had critically low effective population sizes (Ne; 2.7–57.1). Observed trends in population subdivision, genetic diversity, and Ne were consistent with reported trends in the state-endangered Maine-New Hampshire populations, and not indicative of a genetic stronghold within New York. Instead, the small and isolated populations observed here imply a breakdown in metapopulation functionality indicative of conditions faced by the species range-wide and an immediate need for human intervention to restore connectivity and rebuild populations.

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References

  • Amaral KE, Palace M, O’Brien KM, Fenderson LE, Kovach AI (2016) Anthropogenic habitats facilitate dispersal of an early successional obligate: implications for restoration of an endangered ecosystem. PLoS ONE 11:e0148842

    PubMed  PubMed Central  Google Scholar 

  • Balkenhol N, Waits LP (2009) Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Mol Ecol 18:4151–4164

    PubMed  Google Scholar 

  • Batson WG, Gordon IJ, Fletcher DB, Manning AD (2015) Translocation tactics: a framework to support the IUCN Guidelines for wildlife translocations and improve the quality of applied methods. J Appl Ecol 52:1598–1607

    Google Scholar 

  • Bauer ML (2018) Assessing the effects of habitat restoration on shrubland specialists: case study on the New England cottontail and shrubland birds. Thesis, University of New Hampshire, Durham, NH

  • Benjamini Y, Hochberg Y (2000) On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Educ Behav Stat 25:60–83

    Google Scholar 

  • Brichieri-Colombi TA, Moehrenschlager A (2016) Alignment of threat, effort, and perceived success in North American conservation translocations. Conserv Biol 30:1159–1172

    PubMed  Google Scholar 

  • Broquet T, Petit E (2004) Quantifying genotyping errors in noninvasive population genetics. Mol Ecol 13:3601–3608

    CAS  PubMed  Google Scholar 

  • Brubaker DR, Kovach AI, Ducey MJ, Jakubas WJ, O’Brien KM (2014) Factors influencing detection in occupancy surveys of a threatened lagomorph. Wildl Soc Bull 38:513–523. https://doi.org/10.1002/wsb.416

    Article  Google Scholar 

  • Cheeseman AE (2017) Factors limiting recovery of the New England cottontail in New York. Dissertation, State University of New York College of Environmental Science and Forestry, Syracuse, NY

  • Cheeseman AE, Ryan SJ, Whipps CM, Cohen JB (2018) Competition alters seasonal resource selection and promotes use of invasive shrubs by an imperiled native cottontail. Ecol Evol 8:11122–11133

    PubMed  PubMed Central  Google Scholar 

  • Cheeseman AE, Cohen JB, Ryan SJ, Whipps CM (2019) Determinants of home range size of imperiled New England and introduced eastern cottontails. Can J Zool 97:516–523

    Google Scholar 

  • Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package-I-one-table methods. R News 4:5–10

    Google Scholar 

  • Corander J, Sirén J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129

    Google Scholar 

  • DeMay SM, Becker PA, Rachlow JL, Waits LP (2017) Genetic monitoring of an endangered species recovery: demographic and genetic trends for reintroduced pygmy rabbits (Brachylagus idahoensis). J Mammal 98:350–364

    Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth G, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    CAS  PubMed  Google Scholar 

  • Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Google Scholar 

  • Estes-Zumpf WA, Rachlow JL, Waits LP, Warheit KI (2010) Dispersal, gene flow, and population genetic structure in the pygmy rabbit (Brachylagus idahoensis). J Mammal 91:208–219. https://doi.org/10.1644/09-Mamm-a-032r.1

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Google Scholar 

  • Fenderson LE (2010) Landscape genetics of the New England cottontail: effects of habitat fragmentation on population genetic structure and dispersal. Thesis, University of New Hampshire, Durham, NH

  • Fenderson LE, Kovach AI, Litvaitis JA, Litvaitis MK (2011) Population genetic structure and history of fragmented remnant populations of the New England cottontail (Sylvilagus transitionalis). Conserv Genet 12:943–958

    Google Scholar 

  • Fenderson LE, Kovach AI, Litvaitis JA, O’Brien KM, Boland KM, Jakubas WJ (2014) A multiscale analysis of gene flow for the New England cottontail, an imperiled habitat specialist in a fragmented landscape. Ecol Evol 4:1853–1875. https://doi.org/10.1002/ece3.1068

    Article  PubMed  PubMed Central  Google Scholar 

  • Forys E, Humphrey SR (1999) The importance of patch attributes and context to the management and recovery of an endangered lagomorph. Landsc Ecol 14:177–185. https://doi.org/10.1023/a:1008013831843

    Article  Google Scholar 

  • François O, Durand E (2010) Spatially explicit Bayesian clustering models in population genetics. Mol Ecol Resour 10:773–784

    PubMed  Google Scholar 

  • Frankham R, Ballou JD, Eldridge MD, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475

    PubMed  Google Scholar 

  • Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63. https://doi.org/10.1016/j.biocon.2013.12.036

    Article  Google Scholar 

  • Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618

    PubMed  Google Scholar 

  • Frantz A, Pope L, Carpenter P, Roper T, Wilson G, Delahay R, Burke T (2003) Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Mol Ecol 12:1649–1661

    CAS  PubMed  Google Scholar 

  • Fuller S, Tur A (2012) Conservation strategy for the New England cottontail (Sylvilagus transitionalis). https://newenglandcottontail.org/sites/default/files/conservation_strategy_final_12-3-12.pdf. Accessed 10 July 2018

  • Galpern P, Manseau M, Hettinga P, Smith K, Wilson P (2012) Allelematch: an R package for identifying unique multilocus genotypes where genotyping error and missing data may be present. Mol Ecol Resour 12:771–778

    PubMed  Google Scholar 

  • Gilbert KJ, Whitlock MC (2015) Evaluating methods for estimating local effective population size with and without migration. Evolution 69:2154–2166

    PubMed  Google Scholar 

  • Griffith B, Scott JM, Carpenter JW, Reed C (1989) Translocation as a species conservation tool: status and strategy. Science 245:477–480

    CAS  PubMed  Google Scholar 

  • Guinand B, Scribner KT, Page KS, Filcek K, Main L, Burnham-Curtis MK (2006) Effects of coancestry on accuracy of individual assignments to population of origin: examples using Great Lakes lake trout (Salvelinus namaycush). Genetica 127:329–340

    PubMed  Google Scholar 

  • Haddad NM et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052

    PubMed  PubMed Central  Google Scholar 

  • Hanski I (2011) Habitat loss, the dynamics of biodiversity, and a perspective on conservation. Ambio 40:248–255

    PubMed  PubMed Central  Google Scholar 

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479

    CAS  PubMed  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    PubMed  PubMed Central  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    CAS  PubMed  Google Scholar 

  • Jamieson IG, Allendorf FW (2012) How does the 50/500 rule apply to MVPs? Trends Ecol Evol 27:578–584

    PubMed  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    PubMed  Google Scholar 

  • Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281

    PubMed  PubMed Central  Google Scholar 

  • Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788

    Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Google Scholar 

  • King JL, Duncan CL, Garcelon DK (2014) Status of the Santa Catalina Island fox thirteen years after its decline. Monogr West N Am Nat 7:382–396

    Google Scholar 

  • King TL, Eackles M, Aunins A, McGreevy TJ, Husband TP, Tur A, Kovach AI (2017) Microsatellite marker development from next-generation sequencing in the New England cottontail (Sylvilagus transitionalis) and cross-amplification in the eastern cottontail (S. floridanus). BMC Res Notes 10:741

    PubMed  PubMed Central  Google Scholar 

  • Kovach AI, Litvaitis MK, Litvaitis JA (2003) Evaluation of fecal mtDNA analysis as a method to determine the geographic distribution of a rare lagomorph. Wildl Soc Bull 31:1061–1065

    Google Scholar 

  • Kristensen TV, Kovach AI (2018) Spatially explicit abundance estimation of a rare habitat specialist: implications for SECR study design. Ecosphere 9:e02217

    Google Scholar 

  • Litvaitis MK, Litvaitis JA (1996) Using mitochondrial DNA to inventory the distribution of remnant populations of New England cottontails. Wildl Soc Bull 24:725–730

    Google Scholar 

  • Litvaitis JA, Villafuerte R (1996) Factors affecting the persistence of New England cottontail metapopulations: the role of habitat management. Wildl Soc Bull 24:686–693

    Google Scholar 

  • Litvaitis MK, Litvaitis JA, Lee WJ, Kocher TD (1997) Variation in the mitochondrial DNA of the Sylvilagus complex occupying the northeastern United States. Can J Zool 75:595–605. https://doi.org/10.1139/Z97-074

    Article  CAS  Google Scholar 

  • Moro D (2003) Translocation of captive-bred dibblers Parantechinus apicalis (Marsupialia: Dasyuridae) to Escape Island, Western Australia. Biol Conserv 111:305–315. https://doi.org/10.1016/S0006-3207(02)00296-3

    Article  Google Scholar 

  • Newmark WD (1995) Extinction of mammal populations in western North American national parks. Conserv Biol 9:512–526

    Google Scholar 

  • Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474

    PubMed  PubMed Central  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    CAS  PubMed  Google Scholar 

  • Papanastassiou K (2015) A landscape genetics approach for comparing connectivity across the range of the New England cottontail. Thesis, University of New Hampshire, Durham, NH

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    CAS  PubMed  Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859

    CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627

    PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Google Scholar 

  • Robson KM, Lamb CT, Russello MA (2016) Low genetic diversity, restricted dispersal, and elevation-specific patterns of population decline in American pikas in an atypical environment. J Mammal 97:464–472

    Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Resour 4:137–138

    Google Scholar 

  • Ryan SJ, Gavard EJ, Cheeseman AE, Cohen JB, Whipps CM (2016) Reference and baseline hematocrit measures for the threatened New England cottontail (Sylvilagus transitionalis) and comparison with sympatic eastern cottontail (Sylvilagus floridanus) rabbits. J Zoo Wildl Med 47:659–662

    CAS  PubMed  Google Scholar 

  • Singer FJ, Papouchis CM, Symonds KK (2000) Translocations as a tool for restoring populations of bighorn sheep. Restor Ecol 8:6–13. https://doi.org/10.1046/j.1526-100x.2000.80061.x

    Article  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    CAS  PubMed  Google Scholar 

  • Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504. https://doi.org/10.1093/bioinformatics/btn478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • U.S. Fish and Wildlife Service [USFWS] (2006) Endangered and Threatened wildlife and plants; review of native species that are candidates or proposed for listing as Endangered or Threatened; annual notice of findings on resubmitted petitions; annual description of progress on listing actions. Fed Reg 71:53755–53835

    Google Scholar 

  • U.S. Fish and Wildlife Service [USFWS] (2015) Endangered and Threatened wildlife and plants; 12-month finding on a petition to list the new england cottontail as an Endangered or Threatened Species. Fed Reg 80:55286–55304

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Google Scholar 

  • Verhoeven KJ, Simonsen KL, McIntyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647

    Google Scholar 

  • Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    CAS  PubMed  Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756

    PubMed  Google Scholar 

  • Warren AR (2017) An evaluation of New England cottontail habitat restoration. Thesis, University of New Hampshire, Durham, NH

  • Weckworth BV, Musiani M, DeCesare NJ, McDevitt AD, Hebblewhite M, Mariani S (2013) Preferred habitat and effective population size drive landscape genetic patterns in an endangered species. Proc R Soc B 280:1–9. https://doi.org/10.1098/rspb.2013.1756

    Article  Google Scholar 

  • Whipps C, Gavard EJ, Cohen JB, Ryan SJ (2019) Gastrointestinal parasites of the New England cottontail (Sylvilagus transitionalis) and eastern cottontail (Sylvilagus floridanus) in the Hudson Valley, New York. Parasitol Res, in press

  • Whiteley AR, Coombs JA, Hudy M, Robinson Z, Colton AR, Nislow KH, Letcher BH (2013) Fragmentation and patch size shape genetic structure of brook trout populations. Can J Fish Aquat Sci 70:678–688. https://doi.org/10.1139/cjfas-2012-0493

    Article  Google Scholar 

  • Whitlock MC (2000) Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution 54:1855–1861

    CAS  PubMed  Google Scholar 

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Acknowledgements

The New York State Department of Environmental Conservation (NYSDEC) (Grant No. 66287) and G Douglas provided funding, field support and property access. The USDA McIntire-Stennis Program of SUNY-ESF and the Edna Bailey Sussman Foundation provided additional funding. D Rosenblatt, P Novak, J Jaycox, L Masi, and E Burns provided field assistance and technical support. T Goodie and H Kilpatrick provided training. The United States Fish and Wildlife Service and Maine Department of Inland Fisheries and Wildlife provided additional radio collars. The New York State Department of Parks, Recreation, and Historic Preservation, National Park Service, and Clean Air Fund provided additional land access. KE Alger, KAW Lindsay, S Benedict, and C Michaud provided laboratory support. S Silver, M Hall, J Bittner, C Conte, J DeCotis, S Dermody, K Deweese, J Droke, I Dudley, D Eline, E Gavard, T Hillman, R Kelble, E Kohler, E McKean, S Mello, M Ratchford, E Reuber, S Sultaire, J Wojcik and the NYSDEC and Queen’s Zoo assisted with fieldwork.

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Correspondence to Amanda E. Cheeseman.

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Cheeseman, A.E., Cohen, J.B., Whipps, C.M. et al. Hierarchical population structure of a rare lagomorph indicates recent fragmentation has disrupted metapopulation function. Conserv Genet 20, 1237–1249 (2019). https://doi.org/10.1007/s10592-019-01206-z

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