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Genome-wide SNPs redefines species boundaries and conservation units in the freshwater mussel genus Cyprogenia of North America

  • 1.

    Frankham, R. Challenges and opportunities of genetic approaches to biological conservation. Biol. Conserv. 143, 1919–1927 (2010).

    Article 

    Google Scholar 

  • 2.

    Goldstein, P. Z., Desalle, R., Amato, G. & Vogler, A. P. Conservation genetics at the species boundary. Conserv. Biol. 14, 120–131 (2000).

    Article 

    Google Scholar 

  • 3.

    Isaac, N. J. B., Mallet, J. & Mace, G. M. Taxonomic inflation: Its influence on macroecology and conservation. Trends Ecol. Evol. 19, 464–469 (2004).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 4.

    Lydeard, C. et al. The global decline of nonmarine mollusks. Bioscience 54, 321–330 (2004).

    Article 

    Google Scholar 

  • 5.

    Haag, W. R. & Williams, J. D. Biodiversity on the brink: An assessment of conservation strategies for North American freshwater mussels. Hydrobiologia 735, 45–60 (2014).

    Article 

    Google Scholar 

  • 6.

    Ricciardi, A. & Rasmussen, J. Extinction rates of North American freshwater fauna. Conserv. Biol. 13, 1220–1222 (1999).

  • 7.

    Spooner, D. E. & Vaughn, C. C. Context-dependent effects of freshwater mussels on stream benthic communities. Freshw. Biol. 51, 1016–1024 (2006).

    CAS 
    Article 

    Google Scholar 

  • 8.

    Vaughn, C. C., Spooner, D. E. & Galbraith, H. S. Contex-dependent species identity effects within a functional group of filter-feeding bivalves. Ecology 88, 1654–1662 (2007).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 9.

    Vaughn, C. C., Nichols, S. J. & Spooner, D. E. Community and foodweb ecology of freshwater mussels. J. N. Am. Benthol. Soc. 27, 409–423 (2008).

    Article 

    Google Scholar 

  • 10.

    McMahon, R. F. Ecology and Classification of North American Freshwater Invertebrates (Academic Press, 1991).

    Google Scholar 

  • 11.

    Watters, G. T. Unionids, fishes, and the species-area curve. J. Biogeogr. 19, 481–490 (1992).

    Article 

    Google Scholar 

  • 12.

    Haag, W. R. & Warren, M. L. Host fishes and reproductive biology of 6 freshwater mussel species from the Mobile Basin, USA. J. N. Am. Benthol. Soc. 16, 576–585 (1997).

    Article 

    Google Scholar 

  • 13.

    Eckert, N. L. Reproductive biology and host requirement differences among isolated populations of Cyprogenia aberti (Conrad, 1850). MS Thesis, Southwest Missouri State University, Springfield (2003).

  • 14.

    Barnhart, M. C., Haag, W. R. & Roston, W. N. Adaptations to host infection and larval parasitism in Unionoida. J. N. Am. Benthol. Soc. 27, 370–394 (2008).

    Article 

    Google Scholar 

  • 15.

    Rogers, S. O., Watson, B. T. & Neves, R. J. Life history and population biology of the endangered tan riffleshell (Epioblasma florentina walkeri) (Bivalvia: Unionidae). J. N. Am. Benthol. Soc. 20, 582–594 (2001).

    Article 

    Google Scholar 

  • 16.

    Burr, B. M. & Mayden, R. L. Phylogenetics and North American freshwater fishes. In: Systematics, Historical Ecology, and North American Freshwater Fishes. (Stanford University Press, 1992).

  • 17.

    Oesch, R. D. Missouri Naiades: A Guide to the Mussels of Missouri (Missouri Department of Conservation, 1995).

    Google Scholar 

  • 18.

    Harris, J. L. et al. Unionoida (Mollusca: Margaritiferidae, Unionidae) in Arkansas, third status review. J. Ark. Acad. Sci. 63, 50–86 (2009).

    Google Scholar 

  • 19.

    Obermeyer, B. K. Recovery plan for four freshwater mussels in southeast Kansas: Neosho mucket (Lampsilis rafinesqueana), Ouachita kidneyshell (Ptychobranchus occidentalis), rabbitsfoot (Quadrula cylindrica cylindrica), and western fanshell (Cyprogenia aberti). Kansas Department of Parks and Wildlife (2000).

  • 20.

    Serb, J. M. Discovery of genetically distinct sympatric lineages in the freshwater mussel Cyprogenia aberti (Bivalvia: Unionidae). J. Molluscan Stud. 72, 425–434 (2006).

    Article 

    Google Scholar 

  • 21.

    Grobler, J. P., Jones, J. W., Johnson, N. A., Neves, R. J. & Hallerman, E. M. Homogeneity at nuclear microsatellite loci masks mitochondrial haplotype diversity in the endangered fanshell pearlymussel (Cyprogenia stegaria). J. Hered. 102, 196–206 (2011).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 22.

    Serb, J. M. & Barnhart, M. C. Congruence and conflict between molecular and reproductive characters when assessing biological diversity in the Western Fanshell Cyprogenia aberti (Bivalvia, Unionidae)1. Ann. Missouri Bot. Gard. 95, 248–261 (2008).

    Article 

    Google Scholar 

  • 23.

    Chong, J. P., Harris, J. L. & Roe, K. J. Incongruence between mtDNA and nuclear data in the freshwater mussel genus Cyprogenia (Bivalvia: Unionidae) and its impact on species delineation. Ecol. Evol. 6, 2439–2452 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 24.

    Hohenlohe, P. A. et al. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6, e1000862 (2010).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 25.

    Leaché, A. D., Fujita, M. K., Minin, V. N. & Bouckaert, R. R. Species delimitation using genome-wide SNP Data. Syst. Biol. 63, 534–542 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 26.

    Bruneaux, M. et al. Molecular evolutionary and population genomic analysis of the nine-spined stickleback using a modified restriction-site-associated DNA tag approach. Mol. Ecol. 22, 565–582 (2013).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 27.

    Wagner, C. et al. Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Mol. Ecol. 22, 787–798 (2013).

  • 28.

    Larson, W. A. et al. Genotyping by sequencing resolves shallow population structure to inform conservation of Chinook salmon (Oncorhynchus tshawytscha). Evol. Appl. 7, 355–369 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 29.

    Lee, S.-R., Jo, Y.-S., Park, C.-H., Friedman, J. M. & Olson, M. S. Population genomic analysis suggests strong influence of river network on spatial distribution of genetic variation in invasive saltcedar across the southwestern United States. Mol. Ecol. 27, 636–646 (2017).

    Article 
    CAS 

    Google Scholar 

  • 30.

    Massatti, R., Reznicek, A. A. & Knowles, L. L. Utilizing RADseq data for phylogenetic analysis of challenging taxonomic groups: A case study in carex sect. Racemosae. Am. J. Bot. 103, 337–347 (2016).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 31.

    Razkin, O. et al. Species limits, interspecific hybridization and phylogeny in the cryptic land snail complex Pyramidula: The power of RADseq data. Mol. Phylogenet. Evol. https://doi.org/10.1016/j.ympev.2016.05.002 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 32.

    Rubin, B. E. R., Ree, R. H. & Moreau, C. S. Inferring phylogenies from RAD sequence data. PLoS ONE 7, e33394 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 33.

    Takahashi, T., Nagata, N. & Sota, T. Application of RAD-based phylogenetics to complex relationships among variously related taxa in a species flock. Mol. Phylogenet. Evol. https://doi.org/10.1016/j.ympev.2014.07.016 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 34.

    Boucher, F. C., Casazza, G., Szövényi, P. & Conti, E. Sequence capture using RAD probes clarifies phylogenetic relationships and species boundaries in Primula sect. Auricula. Mol. Phylogenet. Evol. https://doi.org/10.1016/j.ympev.2016.08.003 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 35.

    Combosch, D. J., Lemer, S., Ward, P. D., Landman, N. H. & Giribet, G. Genomic signatures of evolution in Nautilus—An endangered living fossil. Mol. Ecol. 26, 5923–5938 (2017).

    PubMed 
    Article 

    Google Scholar 

  • 36.

    Cruaud, A. et al. Empirical assessment of RAD sequencing for interspecific phylogeny. Mol. Biol. Evol. 31, 1272–1274 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 37.

    Eaton, D. A. R. & Ree, R. H. Inferring phylogeny and introgression using RADseq data: An example from flowering plants (Pedicularis: Orobanchaceae). Syst. Biol. 62, 689–706 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 38.

    Emerson, K. J. et al. Resolving postglacial phylogeography using high-throughput sequencing. Proc. Natl. Acad. Sci. USA 107, 16196–16200 (2010).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 39.

    Herrera, S. & Shank, T. M. RAD sequencing enables unprecedented phylogenetic resolution and objective species delimitation in recalcitrant divergent taxa. Mol. Phylogenet. Evol. 100, 70–79 (2016).

    PubMed 
    Article 

    Google Scholar 

  • 40.

    Hipp, A. L. et al. A framework phylogeny of the American Oak Clade based on sequenced RAD data. PLoS ONE 9, e93975 (2014).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 41.

    Jones, J. C., Fan, S., Franchini, P., Schartl, M. & Meyer, A. The evolutionary history of Xiphophorus fish and their sexually selected sword: A genome-wide approach using restriction site-associated DNA sequencing. Mol. Ecol. 22, 2986–3001 (2013).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    Funk, W. C. et al. Adaptive divergence despite strong genetic drift: Genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis). Mol. Ecol. 25, 2176–2194 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 43.

    Taberlet, P. & Luikart, G. Non-invasive genetic sampling and individual identification. Biol. J. Linn. Soc. 68, 41–55 (1999).

    Article 

    Google Scholar 

  • 44.

    Palsbøll, P. J., Bérubé, M. & Allendorf, F. W. Identification of management units using population genetic data. Trends Ecol. Evol. 22, 11–16 (2007).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 45.

    Gibbs, J., Jr. Hunter, M. & Sterling, E. Population genetics: Diversity within versus diversity among populations. In: Problem-Solving in Conservation Biology and Wildlife Management: Exercises for Class, Field, and Laboratory 29–35 (Blackwell Publishing Ltd., 2008). https://doi.org/10.1002/9781444319576.ch4.

  • 46.

    Berendzen, P. B., Simons, A. M., Wood, R. M., Dowling, T. E. & Secor, C. L. Recovering cryptic diversity and ancient drainage patterns in eastern North America: Historical biogeography of the Notropis rubellus species group (Teleostei: Cypriniformes). Mol. Phylogenet. Evol. 46, 721–737 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 47.

    Ray, J. M., Wood, R. M. & Simons, A. M. Phylogeography and post-glacial colonization patterns of the rainbow darter, Etheostoma caeruleum (Teleostei: Percidae). J. Biogeogr. 33, 1550–1558 (2006).

    Article 

    Google Scholar 

  • 48.

    Strange, R. M. & Burr, B. M. Intraspecific phylogeography of North American highland fishes: A test of the pleistocene vicariance hypothesis. Evolution (N. Y.) 51, 885–897 (1997).

    Google Scholar 

  • 49.

    Pflieger, W. L. A distributional study of missouri fishes. Univ. Kans. Publ. Mus. Nat. Hist. 20 (1971).

  • 50.

    Thornbury, W. D. Regional geomorphology of the United States. J. Geol. 73, 815–816 (1965).

    Article 

    Google Scholar 

  • 51.

    Mayden, R. Vicariance biogeography, parsimony, and evolution in North American freshwater fishes. Syst. Zool. 37, 329–355 (1988).

  • 52.

    Echelle, A. A., Echelle, A. F., Smith, M. H. & Hill, L. G. Analysis of genic continuity in a headwater fish, Etheostoma radiosum (Percidae). Copeia 1975, 197–204 (1975).

    Article 

    Google Scholar 

  • 53.

    Haponski, A. E., Bollin, T. L., Jedlicka, M. A. & Stepien, C. A. Landscape genetic patterns of the rainbow darter Etheostoma caeruleum: A catchment analysis of mitochondrial DNA sequences and nuclear microsatellites. J. Fish Biol. 75, 2244–2268 (2010).

    Article 
    CAS 

    Google Scholar 

  • 54.

    Turner, T. F. & Trexler, J. C. Ecological and historical associations of gene flow in darters (Teleostei: Percidae). Evolution (N. Y.) 52, 1781–1801 (1998).

    Google Scholar 

  • 55.

    Turner, T. F., Trexler, J. C., Kuhn, D. N. & Robison, H. W. Life-history variation and comparative phylogeography of darters (Pisces: Percidae) From the North American Central Highlands. Evolution (N. Y.) 50, 2023–2036 (1996).

    Google Scholar 

  • 56.

    Cross, F., Mayden, R. & Stewart, J. Fishes in the Western Mississippi Drainage. The Zoogeography of North American Freshwater Fishes (Wiley, 1986).

    Google Scholar 

  • 57.

    Barnhart, M. C. Reproduction and Fish Host of the Western Fanshell, Cyprogenia aberti (Conrad 1850) (Kansas Department of Wildlife and Parks, 1997).

    Google Scholar 

  • 58.

    Inoue, K., Monroe, E. M., Elderkin, C. L. & Berg, D. J. Phylogeographic and population genetic analyses reveal Pleistocene isolation followed by high gene flow in a wide ranging, but endangered, freshwater mussel. Heredity (Edinb). 112, 282–290 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 59.

    Catchen, J. M., Amores, A., Hohenlohe, P. A., Cresko, W. A. & Postlethwait, J. H. Stacks: Building and genotyping Loci de novo from short-read sequences. G3 Genes Genomes Genet. 1, 171–182 (2011).

    CAS 

    Google Scholar 

  • 60.

    Catchen, J. M., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 61.

    Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S. & Hoekstra, H. E. Double digest RADseq: An inexpensive method for De Novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7, e37135 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 62.

    Mastretta-Yanes, A. et al. Restriction site-associated DNA sequencing, genotyping error estimation and de novo assembly optimization for population genetic inference. Mol. Ecol. Resour. 15, 28–41 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 63.

    Meirmans, P. G. & Van Tienderen, P. H. Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4, 792–794 (2004).

    Article 

    Google Scholar 

  • 64.

    Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution (N. Y.) 38, 1358–1370 (1984).

    CAS 

    Google Scholar 

  • 65.

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

    Article 

    Google Scholar 

  • 66.

    Excoffier, L., Smouse, P. E. & Quattro, J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131, 479–491 (1992).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 67.

    Jombart, T. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 68.

    R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. Available online at https://www.R-project.org/ (2018).

  • 69.

    Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 94 (2010).

  • 70.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 71.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 72.

    Earl, D. A. & Vonholdt, B. M. Structure Harvester: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361 (2012).

    Article 

    Google Scholar 

  • 73.

    Rosenberg, N. A. distruct: A program for the graphical display of population structure. Mol. Ecol. Notes 4, 137–138 (2004).

    Article 

    Google Scholar 

  • 74.

    Minh, B., Nguyen, M.-A. & von Haeseler, A. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 30, 1188–1195 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 75.

    Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).

    CAS 
    Article 

    Google Scholar 

  • 76.

    Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 77.

    Bryant, D., Bouckaert, R., Felsenstein, J., Rosenberg, N. A. & Roychoudhury, A. Inferring species trees directly from biallelic genetic markers: Bypassing gene trees in a full coalescent analysis. Mol. Biol. Evol. 29, 1917–1932 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 78.

    Bouckaert, R. et al. BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, 1–6 (2014).

    Article 
    CAS 

    Google Scholar 

  • 79.

    Kass, R. E. & Raftery, A. E. kass1995BayesFactors. J. Am. Stat. Assoc. 90, 773–795 (1995).

    Article 

    Google Scholar 

  • 80.

    Cornuet, J.-M. et al. DIYABC v2.0: A software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30, 1187–1189 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 81.

    Cabrera, A. A. & Palsbøll, P. J. Inferring past demographic changes from contemporary genetic data: A simulation-based evaluation of the ABC methods implemented in diyabc. Mol. Ecol. Resour. 17, e94–e110 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 82.

    Jones, J. W. & Neves, R. J. Life history and propagation of the endangered fanshell pearlymussel, Cyprogenia stegaria Rafinesque (Bivalvia: Unionidae) The University of Chicago Press on behalf of the Society for F. J. N. Am. Benthol. Soc. 21, 76–88 (2002).

    Article 

    Google Scholar 


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