Genomic and phenotypic divergence informs translocation strategies for an endangered freshwater fish.
Etheostoma akatulo
Caney Fork River system
Endangered Species Act
darter
ddRAD
microendemism
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
28
03
2021
received:
08
12
2020
accepted:
19
04
2021
pubmed:
8
5
2021
medline:
29
7
2021
entrez:
7
5
2021
Statut:
ppublish
Résumé
Translocation, the movement of organisms for conservation purposes, can result in unintended introgression if genetic material flows between populations in new ways. The Bluemask Darter Etheostoma akatulo is a federally endangered species of freshwater fish inhabiting the Caney Fork River system and three of its tributaries (Collins River, Rocky River, and Cane Creek) in Tennessee. The current conservation strategy for Bluemask Darters involves translocating the progeny of broodstock from the Collins River (in the west) to the Calfkiller River (in the east) where the species had been extirpated. In this study, we use ddRAD sequence data from across the extant range to assess this translocation strategy in light of population structure, phylogeny, and demography. We also include museum specimen data to assess morphological variation among extant and extirpated populations. Our analyses reveal substantial genetic and phenotypic disparities between a western population in the Collins River and an eastern population encompassing the Rocky River, Cane Creek, and upper Caney Fork, the two of which shared common ancestry more than 100,000 years ago. Furthermore, morphological analyses classify 12 of 13 Calfkiller River specimens with phenotypes consistent with the eastern population. These results suggest that current translocations perturb the evolutionary boundaries between two delimited populations. Instead, we suggest that repopulating the Calfkiller River using juveniles from the Rocky River could balance conflicting signatures of demography, diversity, and divergence. Beyond conservation, the microgeographic structure of Bluemask Darter populations adds another puzzle to the phylogeography of the hyperdiverse freshwater fishes in eastern North America.
Substances chimiques
DNA, Mitochondrial
0
Banques de données
Dryad
['10.5061/dryad.3bk3j9khp']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
3394-3407Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Alexander, M. L., & Phillips, C. T. (2012). Habitats used by the endangered Fountain Darter (Etheostoma fonticola) in the San Marcos River, Hays County. Texas. the Southwestern Naturalist, 57(4), 449-452. https://doi.org/10.1894/0038-4909-57.4.449
Allendorf, F. W., Hohenlohe, P. A., & Luikart, G. (2010). Genomics and the future of conservation genetics. Nature Reviews Genetics, 11(10), 697-709. https://doi.org/10.1038/nrg2844
Andreasen, L., & Springer, C. (2001). Hatcheries promote fish recovery. Endangered Species Update, 18(3), S32-S33.
Argentina, J. E., Angermeier, P. L., Hallerman, E. M., & Welsh, S. A. (2018). Spatial extent of analysis influences observed patterns of population genetic structure in a widespread darter species (Percidae). Freshwater Biology, 63(10), 1185-1198. https://doi.org/10.1111/fwb.13106
Beneteau, C. L., Mandrak, N. E., & Heath, D. D. (2009). The effects of river barriers and range expansion of the population genetic structure and stability in Greenside Darter (Etheostoma blennioides) populations. Conservation Genetics, 10(2), 477-487. https://doi.org/10.1007/s10592-008-9627-9
Blanton, R. E., Cashner, M. F., Thomas, M. R., Brandt, S. L., & Floyd, M. A. (2019). Increased habitat fragmentation leads to isolation among and low genetic diversity within populations of the imperiled Kentucky Arrow Darter (Etheostoma sagitta spilotum). Conservation Genetics, 20(5), 1009-1022. https://doi.org/10.1007/s10592-019-01188-y
Bouckaert, R., Vaughan, T. G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F. K., Müller, N. F., Ogilvie, H. A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., … Drummond, A. J. (2019). BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLOS Computational Biology, 15(4), e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Bouzat, J. L., Johnson, J. A., Toepfer, J. E., Simpson, S. A., Esker, T. L., & Westemeier, R. L. (2009). Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conservation Genetics, 10(1), 191-201. https://doi.org/10.1007/s10592-008-9547-8
Bryant, D., Bouckaert, R., Felsenstein, J., Rosenberg, N. A., & RoyChoudhury, A. (2012). Inferring species trees directly from biallelic genetic markers: Bypassing gene trees in a full coalescent analysis. Molecular Biology and Evolution, 29(8), 1917-1932. https://doi.org/10.1093/molbev/mss086
Camak, D. T., & Piller, K. R. (2018). Going with the flow: Testing the role of habitat isolation among three ecologically divergent darter species. Copeia, 106(2), 375-387. https://doi.org/10.1643/CG-17-623
Chang, C. C., Chow, C. C., Tellier, L. C., Vattikuti, S., Purcell, S. M., & Lee, J. J. (2015). Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience, 4(1), 7. https://doi.org/10.1186/s13742-015-0047-8
Conant, S. (1988). Saving endangered species by translocation: Are we tinkering with evolution? BioScience, 38(4), 254-257. https://doi.org/10.2307/1310848
Coyne, J. A., & Orr, H. A. (2004). Speciation. Oxford University Press.
Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M., & Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution, 15(7), 290-295. https://doi.org/10.1016/S0169-5347(00)01876-0
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., & Durbin, R. (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156-2158. https://doi.org/10.1093/bioinformatics/btr330
Doll, J. C., Etchison, L., & Owensby, D. (2020). Population estimate of the state and federally threatened Spotfin Chub using underwater observations. North American Journal of Fisheries Management, 40(2), 342-353. https://doi.org/10.1002/nafm.10414
Dray, S., & Dufour, A.-B. (2007). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22(4), 1-20.
Eaton, D. A. R., & Overcast, I. (2020). ipyrad: Interactive assembly and analysis of RADseq datasets. Bioinformatics, 36(8), 2592-2594. https://doi.org/10.1093/bioinformatics/btz966
Eaton, D. A. R., Spriggs, E. L., Park, B., & Donoghue, M. J. (2017). Misconceptions on missing data in RAD-seq phylogenetics with a deep-scale example from flowering plants. Systematic Biology, 66(3), 399-412. https://doi.org/10.1093/sysbio/syw092
Euclide, P., & Marsden, J. E. (2018). Role of drainage and barriers in the genetic structuring of a tessellated darter population. Conservation Genetics, 19(6), 1379-1392. https://doi.org/10.1007/s10592-018-1107-2
Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C., & Foll, M. (2013). Robust demographic inference from genomic and SNP data. PLoS Genetics, 9(10), e1003905. https://doi.org/10.1371/journal.pgen.1003905
Faith, D. P. (1992). Conservation evaluation and phylogenetic diversity. Biological Conservation, 61(1), 1-10. https://doi.org/10.1016/0006-3207(92)91201-3
Fluker, B., Jones, K., & Kuhajda, B. (2019). Genetic structure and diversity of the Blueface Darter Etheostoma cyanoprosopum, a microendemic freshwater fish in the southeastern USA. Endangered Species Research, 40, 133-147. https://doi.org/10.3354/esr00986
George, A. L., Kuhajda, B. R., Williams, J. D., Cantrell, M. A., Rakes, P. L., & Shute, J. R. (2009). Guidelines for propagation and translocation for freshwater fish conservation. Fisheries, 34(11), 529-545. https://doi.org/10.1577/1548-8446-34.11.529
Goudet, J. (2005). Hierfstat, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes, 5(1), 184-186. https://doi.org/10.1111/j.1471-8286.2004.00828.x
Graham, C. F., Boreham, D. R., Manzon, R. G., Stott, W., Wilson, J. Y., & Somers, C. M. (2020). How “simple” methodological decisions affect interpretation of population structure based on reduced representation library DNA sequencing: A case study using the lake whitefish. PLoS One, 15(1), e0226608. https://doi.org/10.1371/journal.pone.0226608
Haponski, A. E., Marth, T. A., & Stepien, C. A. (2007). Genetic divergence across a low-head dam: A preliminary analysis using logperch and greenside darters. Journal of Great Lakes Research, 33, 117-126.
Hollingsworth, P. R., & Near, T. J. (2009). Temporal patterns of diversification and microendemism in Eastern Highland endemic Barcheek Darters (Percidae: Etheostomatinae). Evolution: International Journal of Organic Evolution, 63(1), 228-243. https://doi.org/10.1111/j.1558-5646.2008.00531.x
IUCN/SSC (2013). Guidelines for reintroductions and other conservation translocations. Version 1.0. IUCN/SSC.
Jamieson, I. G. (2011). Founder effects, inbreeding, and loss of genetic diversity in four avian reintroduction programs. Conservation Biology, 25(1), 115-123. https://doi.org/10.1111/j.1523-1739.2010.01574.x
Jelks, H. L., Walsh, S. J., Burkhead, N. M., Contreras-Balderas, S., Diaz-Pardo, E., Hendrickson, D. A., Lyons, J., Mandrak, N. E., McCormick, F., Nelson, J. S., Platania, S. P., Porter, B. A., Renaud, C. B., Schmitter-Soto, J. J., Taylor, E. B., & Warren, M. L. (2008). Conservation status of imperiled North American freshwater and diadromous fishes. Fisheries, 33(8), 372-407. https://doi.org/10.1577/1548-8446-33.8.372
Johnson, M. S. (2000). Measuring and interpreting genetic structure to minimize the genetic risks of translocations. Aquaculture Research, 31(1), 133-143. https://doi.org/10.1046/j.1365-2109.2000.00396.x
Jombart, T. (2008). adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403-1405. https://doi.org/10.1093/bioinformatics/btn129
Kamvar, Z. N., Tabima, J. F., & Grünwald, N. J. (2014). Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281. https://doi.org/10.7717/peerj.281
Keck, B. P., & Near, T. J. (2010). Geographic and temporal aspects of mitochondrial replacement in Nothonotus darters (Teleostei: Percidae: Etheostomatinae). Evolution, 64(5), 1410-1428. https://doi.org/10.1111/j.1558-5646.2009.00901.x
Knaus, B. J., & Grünwald, N. J. (2017). vcfr: A package to manipulate and visualize variant call format data in R. Molecular Ecology Resources, 17(1), 44-53. https://doi.org/10.1111/1755-0998.12549
Laikre, L., Schwartz, M. K., Waples, R. S., & Ryman, N. (2010). Compromising genetic diversity in the wild: Unmonitored large-scale release of plants and animals. Trends in Ecology & Evolution, 25(9), 520-529. https://doi.org/10.1016/j.tree.2010.06.013
Lawson, D. J., Hellenthal, G., Myers, S., & Falush, D. (2012). Inference of population structure using dense haplotype data. PLOS Genetics, 8(1), e1002453. https://doi.org/10.1371/journal.pgen.1002453
Layman, S. R., & Mayden, R. L. (2009). A new species of the darter subgenus Doration (Percidae: Etheostoma) from the Caney Fork River system. Tennessee. Copeia, 2009(1), 157-170. https://doi.org/10.1643/CI-07-129
Layman, S. R., Simons, A. W., & Wood, R. M. (1993). Status of the Dirty Darter, <em>Etheostoma olivaceum</em>, and Bluemask Darter, <em>Etheostoma</em> (<em>Doration</em>) sp., with notes on fishes of the Caney Fork River system, Tennessee. Journal of the Tennessee Academy of Science, 68(2), 65-70.
Lemopoulos, A., Prokkola, J. M., Uusi-Heikkilä, S., Vasemägi, A., Huusko, A., Hyvärinen, P., Koljonen, M.-L., Koskiniemi, J., & Vainikka, A. (2019). Comparing RADseq and microsatellites for estimating genetic diversity and relatedness-Implications for brown trout conservation. Ecology and Evolution, 9(4), 2106-2120. https://doi.org/10.1002/ece3.4905
Lenormand, T. (2002). Gene flow and the limits to natural selection. Trends in Ecology & Evolution, 17(4), 183-189. https://doi.org/10.1016/S0169-5347(02)02497-7
Linck, E., & Battey, C. J. (2019). Minor allele frequency thresholds strongly affect population structure inference with genomic data sets. Molecular Ecology Resources, 19(3), 639-647. https://doi.org/10.1111/1755-0998.12995
Lundberg, J. G., Kottelat, M., Smith, G. R., Stiassny, M. L. J., & Gill, A. C. (2000). So many fishes, so little time: An overview of recent ichthyological discovery in continental waters. Annals of the Missouri Botanical Garden, 87(1), 26-62. https://doi.org/10.2307/2666207
Malinsky, M., Trucchi, E., Lawson, D. J., & Falush, D. (2018). RADpainter and fineRADstructure: Population inference from RADseq data. Molecular Biology and Evolution, 35(5), 1284-1290. https://doi.org/10.1093/molbev/msy023
Mayden, R. L. (1988). Vicariance biogeography, parsimony, and evolution in North American freshwater fishes. Systematic Biology, 37(4), 329-355. https://doi.org/10.1093/sysbio/37.4.329
McFerrin, L. (2013). HDMD: Statistical analysis tools for high dimension molecular data (HDMD) (Version 1.2) [R]. Retrieved from https://CRAN.R-project.org/package=HDMD
Minh, B. Q., Nguyen, M. A. T., & von Haeseler, A. (2013). Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30(5), 1188-1195. https://doi.org/10.1093/molbev/mst024
Moritz, C. (1995). Uses of molecular phylogenies for conservation. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 349(1327), 113-118. https://doi.org/10.1098/rstb.1995.0097
Moritz, C. (1999). Conservation units and translocations: Strategies for conserving evolutionary processes. Hereditas, 130(3), 217-228. https://doi.org/10.1111/j.1601-5223.1999.00217.x
Morrissey, M. B., & de Kerckhove, D. T. (2009). The maintenance of genetic variation due to asymmetric gene flow in dendritic metapopulations. The American Naturalist, 174(6), 875-889. https://doi.org/10.1086/648311
Near, T. J., Bossu, C. M., Bradburd, G. S., Carlson, R. L., Harrington, R. C., Hollingsworth, P. R., Keck, B. P., & Etnier, D. A. (2011). Phylogeny and temporal diversification of darters (Percidae: Etheostomatinae). Systematic Biology, 60(5), 565-595. https://doi.org/10.1093/sysbio/syr052
Near, T. J., & Keck, B. P. (2005). Dispersal, vicariance, and timing of diversification in Nothonotus darters. Molecular Ecology, 14(11), 3485-3496. https://doi.org/10.1111/j.1365-294X.2005.02671.x
Near, T. J., & Keck, B. P. (2013). Free from mitochondrial DNA: Nuclear genes and the inference of species trees among closely related darter lineages (Teleostei: Percidae: Etheostomatinae). Molecular Phylogenetics and Evolution, 66(3), 868-876. https://doi.org/10.1016/j.ympev.2012.11.009Get
Nguyen, L.-T., Schmidt, H. A., Von Haeseler, A., & Minh, B. Q. (2015). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32(1), 268-274. https://doi.org/10.1093/molbev/msu300
Nosil, P. (2008). Speciation with gene flow could be common. Molecular Ecology, 17(9), 2103-2106. https://doi.org/10.1111/j.1365-294X.2008.03715.x
Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. (2012). Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One, 7(5), e37135. https://doi.org/10.1371/journal.pone.0037135
Petty, M. A., Simmons, J. W., Ruble, C., Shute, J. R., & Rakes, P. L. (2020). Propagation and Reintroduction of Bluemask Darter, Etheostoma akatulo, in the Calfkiller River, White and Putnam Counties, Tennessee. Progress Report for 2019-May 2020. Submitted to the U.S. Fish and Wildlife Service, Cookeville, Tennessee Field Office, Conservation Fisheries, Inc., and Tennessee Valley Authority.
Poland, J. A., Brown, P. J., Sorrells, M. E., & Jannink, J.-L. (2012). Development of high-density genetic maps for Barley and Wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One, 7(2), e32253. https://doi.org/10.1371/journal.pone.0032253
Prevosti, A., Ocana, J., & Alonso, G. (1975). Distances between populations of Drosophila subobscura, based on chromosome arrangement frequencies. Theoretical and Applied Genetics, 45(6), 231-241.
R Core Team (2020). R: A language and environment for statistical computing (Version 3.6.3). R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
Raj, A., Stephens, M., & Pritchard, J. K. (2014). fastSTRUCTURE: Variational inference of population structure in large SNP Data Sets. Genetics, 197(2), 573-589. https://doi.org/10.1534/genetics.114.164350
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Systematic Biology, 67(5), 901-904. https://doi.org/10.1093/sysbio/syy032
Robinson, J. D., Simmons, J. W., Williams, A. S., & Moyer, G. R. (2013). Population structure and genetic diversity in the endangered Bluemask Darter (Etheostoma akatulo). Conservation Genetics, 14(1), 79-92. https://doi.org/10.1007/s10592-012-0427-x
Seddon, P. J. (2010). From reintroduction to assisted colonization: Moving along the conservation translocation spectrum. Restoration Ecology, 18(6), 796-802. https://doi.org/10.1111/j.1526-100X.2010.00724.x
Shute, J. R., Rakes, P. L., & Shute, P. W. (2005). Reintroduction of four imperiled fishes in Abrams Creek. Tennessee. Southeastern Naturalist, 4(1), 93-110.
Simmons, J. W. (2004). Selected life history aspects of the endangered Bluemask Darter Etheostoma (Doration) sp. (MS Thesis). Tennessee Technological University, Cookeville.
Simmons, J. W., Layzer, J. B., & Smith, D. D. (2008). Age-class structure and variability of two populations of the Bluemask Darter Etheostoma (Doration) sp. The American Midland Naturalist, 160(2), 300-309.
Soltis, D. E., Morris, A. B., McLachlan, J. S., Manos, P. S., & Soltis, P. S. (2006). Comparative phylogeography of unglaciated eastern North America. Molecular Ecology, 15(14), 4261-4293. https://doi.org/10.1111/j.1365-294X.2006.03061.x
Stange, M., Sánchez-Villagra, M. R., Salzburger, W., & Matschiner, M. (2018). Bayesian divergence-time estimation with genome-wide single-nucleotide polymorphism data of sea catfishes (Ariidae) supports miocene closure of the Panamanian Isthmus. Systematic Biology, 67(4), 681-699. https://doi.org/10.1093/sysbio/syy006
Sterling, K. A., Reed, D. H., Noonan, B. P., & Warren, M. L. (2012). Genetic effects of habitat fragmentation and population isolation on Etheostoma raneyi (Percidae). Conservation Genetics, 13(3), 859-872. https://doi.org/10.1007/s10592-012-0335-0
Storfer, A. (1999). Gene flow and endangered species translocations: A topic revisited. Biological Conservation, 87(2), 173-180. https://doi.org/10.1016/S0006-3207(98)00066-4
Sunde, J., Yıldırım, Y., Tibblin, P., & Forsman, A. (2020). Comparing the performance of microsatellites and RADseq in population genetic studies: Analysis of data for Pike (Esox lucius) and a synthesis of previous studies. Frontiers in Genetics, 11, 218. https://doi.org/10.3389/fgene.2020.00218
Tallmon, D. A., Luikart, G., & Waples, R. S. (2004). The alluring simplicity and complex reality of genetic rescue. Trends in Ecology & Evolution, 19(9), 489-496. https://doi.org/10.1016/j.tree.2004.07.003
U. S. Fish and Wildlife Service (1993). Final decision on relict and bluemask darters. Federal Register, 58, 68480-68486.
Venables, W. N., & Ripley, B. D. (2013). Modern applied statistics with S-PLUS. Springer Science & Business Media.
Washburn, B. A., Cashner, M. F., & Blanton, R. E. (2020). Small fish, large river: Surprisingly minimal genetic structure in a dispersal-limited, habitat specialist fish. Ecology and Evolution, 10(4), 2253-2268. https://doi.org/10.1002/ece3.6064
Weeks, A. R., Sgro, C. M., Young, A. G., Frankham, R., Mitchell, N. J., Miller, K. A., Byrne, M., Coates, D. J., Eldridge, M. D. B., Sunnucks, P., Breed, M. F., James, E. A., & Hoffmann, A. A. (2011). Assessing the benefits and risks of translocations in changing environments: A genetic perspective. Evolutionary Applications, 4(6), 709-725. https://doi.org/10.1111/j.1752-4571.2011.00192.x
Weir, B. S., & Cockerham, C. C. (1984). Estimating F-Statistics for the analysis of population structure. Evolution, 38(6), 1358-1370. https://doi.org/10.1111/j.1558-5646.1984.tb05657.x
Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L., François, R., Grolemund, G., Hayes, A., Henry, L., Hester, J., Kuhn, M., Pedersen, T., Miller, E., Bache, S., Müller, K., Ooms, J., Robinson, D., Seidel, D., Spinu, V., … Yutani, H. (2019). Welcome to the Tidyverse. Journal of Open Source Software, 4(43), 1686. https://doi.org/10.21105/joss.01686
Williams, T. H., & Mendelson, T. C. (2011). Female preference for male coloration may explain behavioural isolation in sympatric darters. Animal Behaviour, 82(4), 683-689. https://doi.org/10.1016/j.anbehav.2011.06.023
Wright, B. R., Grueber, C. E., Lott, M. J., Belov, K., Johnson, R. N., & Hogg, C. J. (2019). Impact of reduced-representation sequencing protocols on detecting population structure in a threatened marsupial. Molecular Biology Reports, 46(5), 5575-5580. https://doi.org/10.1007/s11033-019-04966-6
Yamamoto, S., Morita, K., Koizumi, I., & Maekawa, K. (2004). Genetic differentiation of White-Spotted Charr (Salvelinus leucomaenis) populations after habitat fragmentation: Spatial-temporal changes in gene frequencies. Conservation Genetics, 5(4), 529-538. https://doi.org/10.1023/B:COGE.0000041029.38961.a0
Yeaman, S. (2015). Local adaptation by alleles of small effect. The American Naturalist, 186(Suppl 1), S74-89. https://doi.org/10.1086/682405
Yu, G., Smith, D. K., Zhu, H., Guan, Y., & Lam, T.-T.-Y. (2017). ggtree: An R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution, 8(1), 28-36. https://doi.org/10.1111/2041-210X.12628
Zieritz, A., Hoffman, J. I., Amos, W., & Aldridge, D. C. (2010). Phenotypic plasticity and genetic isolation-by-distance in the freshwater mussel Unio pictorum (Mollusca: Unionoida). Evolutionary Ecology, 24(4), 923-938. https://doi.org/10.1007/s10682-009-9350-0