Genotyping-by-sequencing reveals the effects of riverscape, climate and interspecific introgression on the genetic diversity and local adaptation of the endangered Mexican golden trout (Oncorhynchus chrysogaster)
Tóm tắt
Từ khóa
Tài liệu tham khảo
Abadía-Cardoso A, Garza JC, Mayden RL, García-De León FJ (2015) Genetic structure of pacific trout at the extreme southern end of their native range. PLoS ONE 10:e0141775. https://doi.org/10.1371/journal.pone.0141775
Ahrens CW, Rymer PD, Stow A et al (2018) The search for loci under selection: trends, biases and progress. Mol Ecol 27:1342–1356. https://doi.org/10.1111/mec.14549
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622
Amish SJ, Ali O, Peacock M et al (2019) Assessing thermal adaptation using family-based association and FST-outlier tests in a threatened trout. Mol Ecol. https://doi.org/10.1111/mec.15100
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data
Baguette M, Blanchet S, Legrand D et al (2013) Individual dispersal, landscape connectivity and ecological networks. Biol Rev 88:310–326. https://doi.org/10.1111/brv.12000
Bahls P (1992) The status of fish populations and management of high mountain lakes in the western United States. Northwest Sci 66:183–193. https://doi.org/10.1016/0006-3207(94)90036-1
Banks SC, Cary GJ, Smith AL et al (2013) How does ecological disturbance influence genetic diversity? Trends Ecol Evol 28:670–679
Behnke RL, Tomelleri JR, McGuane T (2002) Trout and Salmon of North America. Free Press, Chicago
Berthelot C, Brunet F, Chalopin D et al (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5:3657. https://doi.org/10.1038/ncomms4657
Binder TR, Thompson HT, Muir AM et al (2015) New insight into the spawning behavior of lake trout, Salvelinus namaycush, from a recovering population in the Laurentian Great Lakes. Environ Biol Fishes 98:173–181. https://doi.org/10.1007/s10641-014-0247-6
Bourret V, Dionne M, Kent MP et al (2013) Landscape genomics in Atlantic salmon (Salmo salar): searching for gene-environment interactions driving local adaptation. Evolution 67:3469–3487. https://doi.org/10.1111/evo.12139
Brauer CJ, Hammer MP, Beheregaray LB (2016) Riverscape genomics of a threatened fish across a hydroclimatically heterogeneous river basin. Mol Ecol 25:5093–5113. https://doi.org/10.1111/mec.13830
Brauer CJ, Unmack PJ, Smith S et al (2018) On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system. Mol Ecol 27:3484–3497. https://doi.org/10.1111/mec.14808
Buchinger TJ, Marsden JE, Binder TR et al (2017) Temporal constraints on the potential role of fry odors as cues of past reproductive success for spawning lake trout. Ecol Evol 7:10196–10206. https://doi.org/10.1002/ece3.3546
Camarena-Rosales F, Ruiz-Campos G, De La Rosa-Vélez J et al (2008) Mitochondrial haplotype variation in wild trout populations (Teleostei: Salmonidae) from northwestern Mexico. Rev Fish Biol Fish 18:33–45. https://doi.org/10.1007/s11160-007-9060-z
Carim KJ, Eby LA, Barfoot CA, Boyer MC (2016) Consistent loss of genetic diversity in isolated cutthroat trout populations independent of habitat size and quality. Conserv Genet 17:1363–1376. https://doi.org/10.1007/s10592-016-0867-9
Catchen JM (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140. https://doi.org/10.1111/mec.12354.Stacks
Catchen JM, Amores A, Hohenlohe P et al (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3: Genes Genomes Genet 1:171–182. https://doi.org/10.1534/g3.111.000240
Channell R, Lomolino MV (2000) Dynamic biogeography and conservation of endangered species. Nature 403:84–86. https://doi.org/10.1038/47487
Chaput-Bardy A, Lemaire C, Picard D, Secondi J (2008) In-stream and overland dispersal across a river network influences gene flow in a freshwater insect, Calopteryx splendens. Mol Ecol 17:3496–3505. https://doi.org/10.1111/j.1365-294X.2008.03856.x
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295. https://doi.org/10.1016/S0169-5347(00)01876-0
Crockett EL (1998) Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperature. Am Zool 38:291–304. https://doi.org/10.1093/icb/38.2.291
Crozier LG, Hutchings JA (2014) Plastic and evolutionary responses to climate change in fish. Evol Appl 7:68–87. https://doi.org/10.1111/eva.12135
Cushman SA, Landguth EL (2010) Spurious correlations and inference in landscape genetics. Mol Ecol 19:3592–3602. https://doi.org/10.1111/j.1365-294X.2010.04656.x
Dalongeville A, Benestan L, Mouillot D et al (2018) Combining six genome scan methods to detect candidate genes to salinity in the Mediterranean striped red mullet (Mullus surmuletus). BMC Genomics 19:217. https://doi.org/10.1186/s12864-018-4579-z
Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Davis CD, Epps CW, Flitcroft RL, Banks MA (2018) Refining and defining riverscape genetics: how rivers influence population genetic structure. Wiley Interdiscip Rev Water 5:e1269. https://doi.org/10.1002/wat2.1269
de Lafontaine G, Napier JD, Petit RJ, Hu FS (2018) Invoking adaptation to decipher the genetic legacy of past climate change. Ecology 99:1530–1546. https://doi.org/10.1002/ecy.2382
Do C, Waples RS, Peel D et al (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. https://doi.org/10.1111/1755-0998.12157
Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188. https://doi.org/10.1111/j.1365-294X.2007.03659.x
Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:1–10. https://doi.org/10.1371/journal.pone.0019379
Escalante MA, García-De-León FJ, Dillman CB et al (2014) Genetic introgression of cultured rainbow trout in the Mexican native trout complex. Conserv Genet 15:1063–1071. https://doi.org/10.1007/s10592-014-0599-7
Escalante MA, García-De León FJ, Dillman CB et al (2016) Introgresión genética de la trucha arcoíris exótica en poblaciones de trucha dorada mexicana. In: Ruiz-Luna A, García-De León FJ (eds) La Trucha Dorada Mexicana. CIAD-CIBNOR, Mexico, pp 125–136
Escalante MA, García-De León FJ, Ruiz-Luna A et al (2018) The interplay of riverscape features and exotic introgression on the genetic structure of the Mexican golden trout ( Oncorhynchus chrysogaster ), a simulation approach. J Biogeogr 45:1500–1514. https://doi.org/10.1111/jbi.13246
Fan H, Hu Y, Wu Q et al (2018) Conservation genetics and genomics of threatened vertebrates in China. J Genet Genomics 45:593–601. https://doi.org/10.1016/J.JGG.2018.09.005
Faulks LK, Kerezsy A, Unmack PJ et al (2017) Going, going, gone? Loss of genetic diversity in two critically endangered Australian freshwater fishes, Scaturiginichthys vermeilipinnis and Chlamydogobius squamigenus, from Great Artesian Basin springs at Edgbaston, Queensland, Australia. Aquat Conserv Mar Freshw Ecosyst 27:39–50. https://doi.org/10.1002/aqc.2684
Fausch KD (2007) Introduction, establishment and effects of non-native salmonids: considering the risk of rainbow trout invasion in the United Kingdom. J Fish Biol 71:1–32. https://doi.org/10.1111/j.1095-8649.2007.01682.x
Flanagan SP, Forester BR, Latch EK et al (2018) Guidelines for planning genomic assessment and monitoring of locally adaptive variation to inform species conservation. Evol Appl 11:1035–1052. https://doi.org/10.1111/eva.12569
Frichot E, François O (2015) LEA: An R package for landscape and ecological association studies. Methods Ecol Evol 6:925–929. https://doi.org/10.1111/2041-210X.12382
Frichot E, Schoville SD, Bouchard G, François O (2013) Testing for associations between loci and environmental gradients using latent factor mixed models. Mol Biol Evol 30:1687–1699. https://doi.org/10.1093/molbev/mst063
García-De León FJ, Dillman CB, De Los Santos Camarillo AB et al (2020) First steps towards the identification of evolutionarily significant units in Mexican native trout: an assessment of microsatellite variation. Environ Biol Fishes. https://doi.org/10.1007/s10641-020-00979-4
García-De León FJ, Getino-Mamet LN, Rodríguez-Jaramillo C et al (2016) Dimorfismo sexual y periodo reproductivo de la trucha dorada mexicana, Oncorhynchus chrysogaster en los ríos Fuerte, Sinaloa y Culiacán. In: Ruíz-Luna A, García-De León FJ (eds) La Trucha Dorada Mexicana. CIAD-CIBNOR, Mexico, pp 53–72
Grummer JA, Beheregaray LB, Bernatchez L et al (2019) Aquatic landscape genomics and environmental effects on genetic variation. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2019.02.013
Gunnell K, Tada MK, Hawthorne FA et al (2008) Geographic patterns of introgressive hybridization between native Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and introduced rainbow trout (O. mykiss) in the South Fork of the Snake River watershed. Idaho Conserv Genet 9:49–64. https://doi.org/10.1007/s10592-007-9302-6
Günther T, Coop G (2013) Robust identification of local adaptation from allele frequencies. Genetics 195:205–220. https://doi.org/10.1534/genetics.113.152462
Hale MC, Xu P, Scardina J et al (2011) Differential gene expression in male and female rainbow trout embryos prior to the onset of gross morphological differentiation of the gonads. BMC Genomics 12:404. https://doi.org/10.1186/1471-2164-12-404
Hand BK, Muhlfeld CC, Wade AA et al (2016) Climate variables explain neutral and adaptive variation within salmonid metapopulations: the importance of replication in landscape genetics. Mol Ecol 25:689–705. https://doi.org/10.1111/mec.13517
Hecht BC, Matala AP, Hess JE, Narum SR (2015) Environmental adaptation in Chinook salmon (Oncorhynchus tshawytscha) throughout their North American range. Mol Ecol 24:5573–5595. https://doi.org/10.1111/mec.13409
Heggberget TG, Johnsen BO, Hindar K et al (1993) Interactions between wild and cultured Atlantic salmon: a review of the Norwegian experience. Fish Res 18:123–146. https://doi.org/10.1016/0165-7836(93)90044-8
Hendricks S, Anderson EC, Antao T et al (2018) Recent advances in conservation and population genomics data analysis. Evol Appl 11:1197–1211. https://doi.org/10.1111/eva.12659
Hendrickson DA, Neely DA, Mayden RL, et al (2006) Conservation of Mexican native trout and the discovery, status. Protection and recovery of the Conchos trout, the first native. Stud North Am desert fishes Honor EP Pist Conserv Univ Autónoma Nuevo León, Monterrey 162–201
Hendrickson DA, Pérez HE, Findley LT et al (2002) Mexican native trouts: a review of their history and current systematic and conservation status. Rev Fish Biol Fish 12:273–316. https://doi.org/10.1023/A:1025062415188
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. https://doi.org/10.1038/35016000
Hoban S, Kelley JL, Lotterhos KE et al (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat 188:379–397. https://doi.org/10.1086/688018
Hogstrand C, Wilson RW, Polgar D, Wood CM (1994) Effects of zinc on the kinetics of branchial calcium uptake in freshwater rainbow trout during adaptation to waterborne zinc. J Exp Biol 186:55–73
Hunter ME, Hoban SM, Bruford MW et al (2018) Next-generation conservation genetics and biodiversity monitoring. Evol Appl 11:1029–1034. https://doi.org/10.1111/eva.12661
Johnson NS, Higgs D, Binder TR et al (2018) Evidence of sound production by spawning lake trout (Salvelinus namaycush) in lakes Huron and Champlain. Can J Fish Aquat Sci 75:429–438. https://doi.org/10.1139/cjfas-2016-0511
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
Kanno Y, Vokoun JC, Letcher BH (2011) Fine-scale population structure and riverscape genetics of brook trout (Salvelinus fontinalis) distributed continuously along headwater channel networks. Mol Ecol 20:3711–3729. https://doi.org/10.1111/j.1365-294X.2011.05210.x
Kleinman-Ruiz D, Martínez-Cruz B, Soriano L et al (2017) Novel efficient genome-wide SNP panels for the conservation of the highly endangered Iberian lynx. BMC Genomics 18:556. https://doi.org/10.1186/s12864-017-3946-5
Kokko H, Chaturvedi A, Croll D et al (2017) Can Evolution supply what ecology demands? Trends Ecol Evol 32:187–197. https://doi.org/10.1016/j.tree.2016.12.005
Koskinen MT, Haugen TO, Primmer CR (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830. https://doi.org/10.1038/nature01029
Landguth EL, Bearlin A, Day CC, Dunham J (2016) CDMetaPOP: an individual-based, eco-evolutionary model for spatially explicit simulation of landscape demogenetics. Methods Ecol Evol 8:4–11. https://doi.org/10.1111/2041-210X.12608
Landguth EL, Fedy BC, Oyler-Mccance SJ et al (2012) Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern. Mol Ecol Resour 12:276–284. https://doi.org/10.1111/j.1755-0998.2011.03077.x
Lawler JJ, Tear TH, Pyke C et al (2010) Resource management in a changing and uncertain climate. Front Ecol Environ 8:35–43. https://doi.org/10.1890/070146
Le Pichon CLE, Gorges G, Boët P et al (2006) A spatially explicit resource-based approach for managing stream fishes in riverscapes. Environ Manage 37:322–335. https://doi.org/10.1007/s00267-005-0027-3
Leitwein M, Garza JC, Pearse DE (2017) Ancestry and adaptive evolution of anadromous, resident, and adfluvial rainbow trout (Oncorhynchus mykiss) in the San Francisco bay area: application of adaptive genomic variation to conservation in a highly impacted landscape. Evol Appl 10:56–67. https://doi.org/10.1111/eva.12416
Linløkken AN, Haugen TO, Mathew PK et al (2016) Comparing estimates of number of breeders Nb based on microsatellites and single nucleotide polymorphism of three groups of brown trout (Salmo trutta L.). Fish Manage Ecol 23:152–160. https://doi.org/10.1111/fme.12169
Luu K, Bazin E, Blum MGB (2016) pcadapt : an R package to perform genome scans for selection based on principal component analysis. Mol Ecol Resour. https://doi.org/10.1111/1755-0998.12592
Manel S, Holderegger R (2013) Ten years of landscape genetics. Trends Ecol Evol 28:614–621. https://doi.org/10.1016/j.tree.2013.05.012
Marie AD, Bernatchez L, Garant D, Taylor E (2012) Environmental factors correlate with hybridization in stocked brook charr (Salvelinus fontinalis). Can J Fish Aquat Sci 69:884–893. https://doi.org/10.1139/f2012-027
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
Milanesi P, Holderegger R, Caniglia R et al (2017) Expert-based versus habitat-suitability models to develop resistance surfaces in landscape genetics. Oecologia 183:67–79. https://doi.org/10.1007/s00442-016-3751-x
Milano I, Babbucci M, Cariani A et al (2014) Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Mol Ecol 23:118–135. https://doi.org/10.1111/mec.12568
Milián-García Y, Ramos-Targarona R, Pérez-Fleitas E et al (2015) Genetic evidence of hybridization between the critically endangered Cuban crocodile and the American crocodile: implications for population history and in situ/ex situ conservation. Heredity (Edinb) 114:272–280. https://doi.org/10.1038/hdy.2014.96
Miller RR, Williams JD, Williams JE (1989) Extinctions of North American fishes during the past century. Fisheries 14:22–38. https://doi.org/10.2307/1104578
Morita K, Yamamoto S (2002) Effects of habitat fragmentation by damming on the persistence of a stream—dwelling charr. Conserv Biol 16:1318–1323. https://doi.org/10.1046/j.1523-1739.2002.01476.x
Muhlfeld CC, Kalinowski ST, McMahon TE et al (2009) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett. https://doi.org/10.1098/rsbl.2009.0033
Muhlfeld CC, Kovach RP, Al-Chokhachy R et al (2017) Legacy introductions and climatic variation explain spatiotemporal patterns of invasive hybridization in a native trout. Glob Chang Biol 23:4663–4674. https://doi.org/10.1111/gcb.13681
Narum SR, Zendt JS, Graves D, Sharp WR (2008) Influence of landscape on resident and anadromous life history types of Oncorhynchus mykiss. Can J Fish Aquat Sci 65:1013–1023. https://doi.org/10.1139/F08-025
Needham PR, Gard R (1964) A New Trout from Central Mexico: Salmo chrysogaster, the Mexican Golden Trout. Copeia 1964:169. https://doi.org/10.2307/1440847
Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474. https://doi.org/10.1111/j.1752-4571.2008.00015.x
Olsen MT, Islas V, Graves JA et al (2017) Genetic population structure of harbour seals in the United Kingdom and neighbouring waters. Genet Syst. https://doi.org/10.1002/aqc.2760
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Pearse DE (2016) Saving the spandrels? Adaptive genomic variation in conservation and fisheries management. J Fish Biol 89:2697–2716. https://doi.org/10.1111/jfb.13168
Pearse DE, Campbell MA (2018) Ancestry and adaptation of rainbow trout in yosemite national park. Fisheries 43:472–484. https://doi.org/10.1002/fsh.10136
Penaluna BE, Abadía-Cardoso A, Dunham JB et al (2016) Conservation of native pacific trout diversity in Western North America. Fisheries 41:286–300. https://doi.org/10.1080/03632415.2016.1175888
Perreault-Payette A, Muir AM, Goetz F et al (2017) Investigating the extent of parallelism in morphological and genomic divergence among lake trout ecotypes in Lake Superior. Mol Ecol 26:1477–1497. https://doi.org/10.1111/mec.14018
Perrier C, Ferchaud A-L, Sirois P et al (2017) Do genetic drift and accumulation of deleterious mutations preclude adaptation? Empirical investigation using RADseq in a northern lacustrine fish. Mol Ecol 26:6317–6335. https://doi.org/10.1111/mec.14361
Perrier C, Guyomard R, Bagliniere J-L et al (2013) Changes in the genetic structure of Atlantic salmon populations over four decades reveal substantial impacts of stocking and potential resiliency. Ecol Evol 3:2334–2349. https://doi.org/10.1002/ece3.629
Perrier C, Guyomard R, Bagliniere JL, Evanno G (2011) Determinants of hierarchical genetic structure in Atlantic salmon populations: environmental factors vs anthropogenic influences. Mol Ecol 20:4231–4245. https://doi.org/10.1111/j.1365-294X.2011.05266.x
Rahel FJ, Bierwagen B, Taniguchi Y (2008) Managing aquatic species of conservation concern in the face of climate change and invasive species. Conserv Biol 22:551–561. https://doi.org/10.1111/j.1523-1739.2008.00953.x
Raj A, Stephens M, Pritchard JK (2014) FastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197:573–589. https://doi.org/10.1534/genetics.114.164350
Razgour O, Forester B, Taggart JB et al (2019) Considering adaptive genetic variation in climate change vulnerability assessment reduces species range loss projections. Proc Natl Acad Sci 116:10418–10423. https://doi.org/10.1073/pnas.1820663116
Richardson JL, Brady SP, Wang IJ, Spear SF (2016) Navigating the pitfalls and promise of landscape genetics. Mol Ecol 25:849–863. https://doi.org/10.1111/mec.13527
Rieman BE, Allendorf FW (2001) Effective population size and genetic conservation criteria for bull trout. North Am J Fish Manage 21:756–764. https://doi.org/10.1577/1548-8675(2001)021<0756:EPSAGC>2.0.CO;2
Riginos C, Liggins L (2013) seascape genetics: populations, individuals, and genes marooned and adrift. Geogr Compass 7:197–216. https://doi.org/10.1111/gec3.12032
Rosenberg MS, Anderson CD (2011) PASSaGE: pattern analysis, spatial statistics and geographic exegesis: Version 2. Methods Ecol Evol 2:229–232. https://doi.org/10.1111/j.2041-210X.2010.00081.x
Ruiz-Luna A, Hernández-Guzmán R, García-De León FJ, Ramírez-Huerta AL (2017) Potential distribution of endangered Mexican golden trout (Oncorhynchus chrysogaster) in the Rio Sinaloa and Rio Culiacan basins (Sierra Madre Occidental) based on landscape characterization and species distribution models. Environ Biol Fishes. https://doi.org/10.1007/s10641-017-0624-z
Ruzzante DE, McCracken GR, Parmelee S et al (2016) Effective number of breeders, effective population size and their relationship with census size in an iteroparous species. Salvelinus fontinalis Proc R Soc B. https://doi.org/10.1098/rspb.2015.2601
Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evo 4:406–425
Salem M, Kenney PB, Rexroad CE, Yao J (2010) Proteomic signature of muscle atrophy in rainbow trout. J Proteomics 73:778–789. https://doi.org/10.1016/j.jprot.2009.10.014
Sato T, Harada Y (2008) Loss of genetic variation and effective population size of Kirikuchi charr: implications for the management of small, isolated salmonid populations. Animal Conserv 11(2):153–159
Schmidt DJ, Espinoza T, Connell M, Hughes JM (2017) Conservation genetics of the Mary River turtle (Elusor macrurus) in natural and captive populations. Aquat Conserv Mar Freshw Ecosyst. https://doi.org/10.1002/aqc.2851
Splendiani A, Ruggeri P, Giovannotti M, Caputo Barucchi V (2013) Role of environmental factors in the spread of domestic trout in Mediterranean streams. Freshw Biol 58:2089–2101. https://doi.org/10.1111/fwb.12193
Taggart JB, Bron JE, Martin SAM et al (2008) A description of the origins, design and performance of the TRAITS-SGP Atlantic salmon Salmo salar L cDNA microarray. J Fish Biol 72:2071–2094. https://doi.org/10.1111/j.1095-8649.2008.01876.x
Taiyun Wei M (2017) Title visualization of a correlation matrix. Statistician 56:316–324
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/molbev/msl149
Team R Core (2018) R: A language and environment for statistical computing. p 201. https://doi.org/10.1108/eb003648
Tikochinski Y, Bradshaw P, Mastrogiacomo A et al (2018) Mitochondrial DNA short tandem repeats unveil hidden population structuring and migration routes of an endangered marine turtle. Aquat Conserv Mar Freshw Ecosyst. https://doi.org/10.1002/aqc.2908
Torres-Florez JP, Johnson WE, Nery MF et al (2017) The coming of age of conservation genetics in Latin America: what has been achieved and what needs to be done. Conserv Genet 19:1–15. https://doi.org/10.1007/s10592-017-1006-y
Torterotot J-B, Perrier C, Bergeron NE, Bernatchez L (2014) Influence of forest road culverts and waterfalls on the fine-scale distribution of brook trout genetic diversity in a boreal watershed. Trans Am Fish Soc 143:1577–1591. https://doi.org/10.1080/00028487.2014.952449
van Etten J (2012) gdistance: Distances and routes on geographical grids. R package version 1.1-4. Available a t CRAN R-project org/package=gdistance
Vera M, Martinez P, Bouza C (2017) Stocking impact, population structure and conservation of wild brown trout populations in inner Galicia (NW Spain), an unstable hydrologic region. Aquat Conserv Mar Freshw Ecosyst. https://doi.org/10.1002/aqc.2856
Weigel DE, Peterson JT, Spruell P (2003) Introgressive Hybridization between Native Cutthroat Trout and Introduced Rainbow Trout. Ecol Appl 13:38–50
Wenne R, Bernaś R, Poćwierz-Kotus A et al (2016) Recent genetic changes in enhanced populations of sea trout (Salmo trutta m trutta) in the southern Baltic rivers revealed with SNP analysis. Aquat Living Resour 103:29. https://doi.org/10.1051/alr/2016012