Abstract
In brown trout, instances of genetic homogenization after introducing hatchery-reared allochthonous Atlantic strains are well documented. Therefore, mitigation-driven translocation with autochthonous lineages is gaining support. However, when the origin of local donor populations is not clear they should be genetically characterized prior to translocation. Here we present a case study from the Vlasina Plateau in Southeast Serbia, where two drainages, Danube and Aegean, are adjoining. The status of Danubian and Aegean brown trout populations was investigated with respect to inter-relationship and genetic admixture using mtDNA and microsatellite loci. Results revealed a complex genetic structure and demonstrated different levels of introgressive hybridization from the Aegean populations (which belong to the Adriatic evolutionary lineage) into the Danubian populations as a direct consequence of human mediated translocations. While most introgressed Danubian locations showed low to intermediate proportions of allochtonous genes this was not the case with the upper Jerma location, where all individuals were characterized as pure Adriatic lineage of brown trout. Contrarily, Aegean locations from the Plateau are inhabited by pure Adriatic brown trout. Finally, our analysis clearly demonstrates that the biological invasion followed a stepping-stone scenario via the upper Jerma, which served as a local donor population for supplementing other Danubian populations, and excludes the possibility of brown trout invading through physical connections between the two drainages that were established because of Vlasina hydroelectric power plants. Furthermore, evidence of increased stocking in the wider region is additionally supported by the detection of low level introgression with the domesticated Atlantic brown trout.
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References
Aktas C (2020) haplotypes: Manipulating DNA Sequences and Estimating Unambiguous Haplotype Network with Statistical Parsimony. R package version 1.1.2. Accessed 15 July 2021. http://cran.r-project.org/web/packages/haplotypes/
Bardakci F, Degerli N, Ozdemir O, Basibuyuk HH (2006) Phylogeography of the Turkish brown trout Salmo trutta L.: mitochondrial DNA PCR-RFLP variation. J Fish Biol 68:36–55. https://doi.org/10.1111/j.0022-1112.2006.00948.x
Baric S, Riedl A, Meraner A, Medgyesy N, Lackner R, Pelster B, Via JD (2010) Alpine headwater streams as reservoirs of remnant populations of the Danubian clade of brown trout. Freshw Biol 55:866–880. https://doi.org/10.1111/j.1365-2427.2009.02318.x
Belkhir K, Borsa P, Chikhi, L, Raufaste N, Bonhomme F (1996–2004) GENETIX v. 4.04, Logiciel sous WindowsTM pour la Génétique des Populations. Université Montpellier 2, Laboratoire Génome et Population, Montpellier. https://kimura.univ-montp2.fr/genetix/
Benzécri JP (1973) L’analyse des données. Tome 1: La taxinomie.—Tome 2: L’analyse des correspondances. Dunod, Paris
Berger-Tal O, Blumstein DT, Swaisgood RR (2019) Conservation translocations: a review of common difficulties and promising directions. Anim Conserv 23:121–131. https://doi.org/10.1111/acv.12534
Bernatchez L (2001) The evolutionary history of brown trout (Salmo trutta L.) interred from phylogenetic, nested clade, and mismatch analyses of mitochondrial DNA variation. Evolution 55:351–379. https://doi.org/10.1111/j.0014-3820.2001.tb01300.x
Bernatchez L, Guyomard R, Bonhomme F (1992) DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Salmo trutta populations. Mol Ecol 1:161–173. https://doi.org/10.1111/j.1365-294x.1992.tb00172.x
Berrebi P, Caputo Barucchi V, Splendiani A, Muracciole S, Sabatini A, Palmas F, Tougard C, Arculeo M, Marić S (2019) Brown trout (Salmo trutta L.) high genetic diversity around the Tyrrhenian Sea as revealed by nuclear and mitochondrial markers. Hydrobiologia 826:209–231. https://doi.org/10.1007/s10750-018-3734-5
Bohling J, Haffray P, Berrebi P (2016) Genetic diversity and population structure of domestic brown trout (Salmo trutta) in France. Aquaculture 462:1–9. https://doi.org/10.1016/j.aquaculture.2016.04.013
Budy P, Thiede GP, Lobón-Cerviá J, Gonzalez Fernandez G, McHugh P, McIntosh A, Vøllestad LA, Becares E, Jellyman P (2013) Limitation and facilitation of one of the world’s most invasive fish: an intercontinental comparison. Ecology 94:356–367. https://doi.org/10.1890/12-0628.1
Catarino D, Knutsen H, Veríssimo A, Olsen EM, Jorde PE, Menezes G, Sannæs H, Stanković D, Company JB, Neat F, Danovaro R, Dell’Anno A, Rochowski B, Stefanni S (2015) The Pillars of Hercules as a bathymetric barrier to gene flow promoting isolation in a global deep-sea shark (Centroscymnus coelolepis). Mol Ecol 24:6061–6079. https://doi.org/10.1111/mec.13453
Clement M, Posada D, Crandall K (2000) TCS: A computer program to estimate gene genealogies. Mol Ecol 9:1657–1660. https://doi.org/10.1046/j.1365-294x.2000.01020.x
Cortey M, Vera M, Pla C, García-Marín J-L (2009) Northern and Southern expansions of Atlantic brown trout (Salmo trutta) populations during the Pleistocene. Biol J Linn Soc 97:904–917. https://doi.org/10.1111/j.1095-8312.2009.01220.x
Dragišić V (1997) Geološko-hidrogeološke karakteristike sliva Vlasinskog jezera [Geological-hydrogeological characteristics of Vlasinsko Jezero reservoir drainage area]. In: Blaženčić J (ed) Vlasinsko jezero—hidrobiološka studija [Vlasina Lake—hydrobiological study]. Biološki fakultet Univerziteta u Beogradu, Beograd, pp 25–35 ([In Serbian])
Duftner N, Weiss S, Medgyesy N, Sturmbauer C (2003) Enhanced phylogeographic information about Austrian brown trout populations derived from complete mitochondrial control region secuences. J Fish Biol 62:427–435. https://doi.org/10.1046/j.1095-8649.2003.00038.x
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.)] Skeels endemic to Morocco. Theor Appl Genet 92:832–839. https://doi.org/10.1007/BF00221895
Eschbach E, Nolte AW, Kohlmann K, Kersten P, Kail J, Arlinghaus R (2014) Population differentiation of zander (Sander lucioperca) across native and newly colonized ranges suggests increasing admixture in the course of an invasion. Evol Appl 7:555–568. https://doi.org/10.1111/eva.12155
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491. https://doi.org/10.1093/genetics/131.2.479
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486. https://doi.org/10.1093/oxfordjournals.jhered.a111627
Grubić G, Panić A (2008) Reka na granici vremena, u džepu Balkana [River on the border of a time, in the pocket of the Balkans]. Mušičar 1:28–31 ([In Serbian])
Hansen MM, Loeschcke V (1994) Effects of releasing hatchery-reared brown trout to wild trout populations. In: Loeschcke V, Tomiuk J, Jain SK (eds) Conservation Genetics, EXS, vol 68. Birkhäuser Verlag, Basel, pp 273–289. https://doi.org/10.1007/978-3-0348-8510-2_22
Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297. https://doi.org/10.1126/science.131.3409.1292
Jadan M, Čož-Rakovac R, Topić Popović N, Strunjak Perović I (2007) Presence of unsexpected phylogenetic lineages of brown trout Salmo trutta L. in Gacka River. Croatia Aquac Res 38:1682–1685. https://doi.org/10.1111/j.1365-2109.2007.01832x
Janković D, Raspopović M (1960) Ohridska pastrmka (Salmo letnica typicus K.) pod promenjenim uslovima u Vlasinskom baražnom jezeru [Lake Ohrid trout (Salmo letnica typicus K.) under the altered conditions in the Vlasina reservoir]. Arh Biol Nauka 12:117–122 ([In Serbian])
Jensen LF, Hansen MM, Pertoldi C, Holdensgaard G, Mensberg KL, Loeschcke V (2008) Local adaptation in brown trout early life-history traits: implications for climate change adaptability. Proc R Soc B 275:2859–2868. https://doi.org/10.1098/rspb.2008.0870
Jonsson B, Jonsson N (2011) Habitat as a template for life histories. In: Ecology of Atlantic salmon and brown trout Fish & Fisheries Series, vol 33. Springer, Dordrecht, pp 1–21. https://doi.org/10.1007/978-94-007-1189-1_1
Kaspersson R, Sundström F, Bohlin T, Johnsson JI (2013) Modes of competition: adding and removing brown trout in the wild to understand the mechanisms of density-dependence. PLoS ONE 8:e62517. https://doi.org/10.1371/journal.pone.0062517
Kohout J, Jašková I, Papoušek I, Šedivá A, Šlechta V (2012) Effects of stocking on the genetic structure of brown trout, Salmo trutta, in Central Europe inferred from mitochondrial and nuclear DNA markers. Fish Manag Ecol 19:252–263. https://doi.org/10.1111/j.1365-2400.2011.00828.x
Kohout J, Šedivá A, Apostolou A, Stefanov T, Marić S, Gaffarŏglu M, Šlechta V (2013) Genetic diversity and phylogenetic origin of brown trout Salmo trutta populations in eastern Balkans. Biologia 68:1229–1237. https://doi.org/10.2478/s11756-013-0271-6
Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Publications Kottelat Cornol and Freyhof, Berlin
Laikre L, Antunes A, Apostolidis A, Berrebi P, Duguid A, Ferguson A, Garcia—Marin JL, Guyomard R, Hansen MM, Hindar K, Koljonen ML, Largiader C, Martinez P, Nielsen EE, Palm S, Ruzzante DE, Ryman N, Trianthaphyllidis C (1999) Conservation genetic management of brown trout (Salmo trutta) in Europe. Report by the concerted action on identification, management and exploitation of genetic resources in the brown trout (Salmo trutta), "TROUTCONCERT"; EU FAIR CT97-3882. Danmarks fiskeriundersrgelser, Silkeborg
Langridge J, Sordello R, Reyjol Y (2020) Outcomes of wildlife translocations in protected areas: what is the type and extent of existing evidence? A systematic map protocol. Environ Evid 9:16. https://doi.org/10.1186/s13750-020-00199-4
Lerceteau-Köhler E, Weiss S (2006) Development of multiplex PCR microsatellite assay in brown trout Salmo trutta, and its potential application for the genus. Aquaculture 258:641–645. https://doi.org/10.1016/j.aquaculture.2006.04.028
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lobón-Cerviá J, Esteve M, Berrebi P, Duchi A, Lorenzoni M, Young KA (2019) Trout and char of central and southern Europe and northern Africa. In: Kersher JL, Williams JE, Gresswell RE, Lobón-Cerviá J (eds) Trout and char of the world. American Fisheries Society, Besheda, pp 379–410
Madeira MJ, Gómez-moliner BJ, Barbé AM (2005) Genetic introgression on freshwater fish populations caused by restocking programmes. Biol Invasions 7:117–125. https://doi.org/10.1007/s10530-004-9641-x
Marić S, Hegediš A, Nikolić V, Simonović P (2004) Conservation status of two Eastern Balkan endemic fish species in Serbia and a proposal for their protection. Acta Zool Bulg 56:213–222
Marić S, Sušnik S, Simonović P, Snoj A (2006) Phylogeographic study of brown trout from Serbia, based on mitochondrial DNA control region analysis. Genet Sel Evol 38:411–430. https://doi.org/10.1051/gse:2006012
Marić S, Kalamujić B, Snoj A, Razpet A, Lukić-Bilela L, Pojskić N, Sušnik Bajec S (2012) Genetic variation of European grayling (Thymallus thymallus) populations in the Western Balkans. Hydrobiologia 691:225–237. https://doi.org/10.1007/s10750-012-1076-2
Marić S, Sušnik Bajec S, Schöffmann J, Kostov V, Snoj A (2017a) Phylogeography of stream-dwelling trout in the Republic of Macedonia and a molecular genetic basis for revision of the taxonomy proposed by S. Karaman. Hydrobiologia 785:249–260. https://doi.org/10.1007/s10750-016-2930-4
Marić S, Stanković S, Wanzenböck J, Šanda R, Erős T, Takács P, Specziár A, Sekulić N, Bănăduc D, Ćaleta M, Trombitsky I, Galambos L, Sipos S, Snoj A (2017b) Phylogeography and population genetics of the European mudminnow (Umbra krameri) with a time-calibrated phylogeny for the family Umbridae. Hydrobiologia 792:151–168. https://doi.org/10.1007/s10750-016-3051-9
Meffe GK (1986) Conservation genetics and the management of endangered fishes. Fisheries 11:14–23. https://doi.org/10.1577/1548-8446(1986)011%3c0014:CGATMO%3e2.0.CO;2
Meldgaard T, Crivelli AJ, Jesenšek D, Poizat D, Rubin J-F, Berrebi P (2007) Hybridization mechanisms between the endangered marble trout (Salmo marmoratus) and the brown trout (Salmo trutta) as revealed by in-stream experiments. Biol Conserv 136:602–611. https://doi.org/10.1016/j.biocon.2007.01.004
Meraner A, Baric S, Pelster B, Dalla Via J (2007) Trout (Salmo trutta) mitochondrial DNA polymorphism in the centre of the marble trout distribution area. Hydrobiologia 579:337–349. https://doi.org/10.1007/s10750-006-0479-3
Meraner A, Gratton P, Baraldi P, Gandolf A (2013) Nothing but a trace left? Autochthony and conservation status of Northern Adriatic Salmo trutta i nferred from PCR multiplexing, mtDNA control region sequencing and microsatellite analysis. Hydrobiol 702:201–213. https://doi.org/10.1007/s10750-012-1321-8
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE), New Orleans, pp 1–8
Nei M, Chesser RK (1983) Estimation of fixation indices and gene diversities. Ann Hum Genet 47:253–259. https://doi.org/10.1111/j.1469-1809.1983.tb00993.x
Olden JD, Leroy Poff N, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24. https://doi.org/10.1016/j.tree.2003.09.010
Peeler EJ, Oidtmann BC, Midtlyng PJ, Miossec L, Gozlan RE (2011) Non-native aquatic animals introductions have driven disease emergence in Europe. Biol Invasions 13:1291–1303. https://doi.org/10.1007/s10530-010-9890-9
Popa GO, Curtean-Bănăduc A, Bănăduc D, Florescu IE, Burcea A, Dudu A, Georgescu SE, Costache M (2016) Molecular markers reveal reduced genetic diversity in Romanian populations of Brown Trout, Salmo trutta L., 1758 (Salmonidae). Acta Zool Bulg 68:399–406
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Povž M, Jesenšek D, Berrebi P, Crivelli AJ (1996) The Marble trout, Salmo trutta marmoratus, Cuvier 1817, in the Soča River basin. Tour du Valat Publication, Arles, Slovenia, p 65
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 13 July 2021. https://www.R-project.org/
Razpet A, Sušnik S, Jug T, Snoj A (2007) Genetic variation among trout in the River Neretva basin, Bosnia and Herzegovina. J Fish Biol 70:94–110. https://doi.org/10.1111/j.1095-8649.2007.01392.x
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573
Robinson ZL, Coombs JA, Hudy M, Nislow KH, Letcher BH, Whiteley AR (2017) Experimental test of genetic rescue in isolated populations of brook trout. Mol Ecol 26:4418–4433. https://doi.org/10.1111/mec.14225
Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Ryman N (1991) Conservation genetics considerations in fishery management. J Fish Biol 39:211–224. https://doi.org/10.1111/j.1095-8649.1991.tb05085.x
Sanz N (2017) Phylogeographic History of Brown Trout: A Review. In: Lobón-Cerviá J, Sanz N (eds) Brown Trout: Biology, Ecology and Management. Wiley, Hoboken, pp 17–63
Salisbury SJ, McCracken GR, Keefe D, Perry R, Ruzzante DE (2019) Extensive secondary contact among three glacial lineages of Arctic Char (Salvelinus alpinus) in Labrador and Newfoundland. Ecol Evol 9:2031–2045. https://doi.org/10.1002/ece3.4893
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York
Sandlund OT, Berntsen HH, Fiske P, Kuusela J, Muladal R, Niemelä E, Uglem I, Forseth T, Mo TA, Thorstad EB, Veselov AE, Vollset KW, Zubchenko AV (2019) Pink salmon in Norway: the reluctant invader. Biol Invasions 21:1033–1054. https://doi.org/10.1007/s10530-018-1904-z
Seddon PJ, Armstrong DP, Maloney RF (2007) Developing the science of reintroduction biology. Conserv Biol 21:303–312. https://doi.org/10.1111/j.1523-1739.2006.00627.x
Seiler SM, Keeley ER (2009) Competition between native and introduced salmonid fishes: Cutthroat trout have lower growth rate in the presence of cutthroat-rainbow trout hybrids. Can J Fish Aquat Sci 66:133–141. https://doi.org/10.1139/F08-194
Sethuraman A, Hey J (2016) IMa2p—parallel MCMC and inference of ancient demography under the Isolation with migration (IM) model. Mol Ecol Resour 16:206–215. https://doi.org/10.1111/1755-0998.12437
Schöffmann J, Marić S, Snoj A (2019) Trouts of southeast Europe, western and central Asia. In: Kersher JL, Williams JE, Gresswell RE, Lobón-Cerviá J (eds) Trout and char of the world. American Fisheries Society, Besheda, pp 411–456
Simonović P (2001) Ribe Srbije [Fishes of Serbia]. NNK International, Zavod za zaštitu prirode Srbije i Biološki fakultet, Beograd [In Serbian]
Simonović P, Nikolić V (1997) Ihtiofauna Vlasinskog jezera—stanje i perspektiva [Ichthyofauna of the Lake Vlasina—status and prospect]. In: Blaženčić J (ed) Vlasinsko jezero—hidrobiološka studija [Vlasina Lake—hydrobiological study]. Biološki fakultet, Beograd, pp 179–198
Simonović P, Vidović Z, Tošić A, Škraba D, Čanak-Atlagić J, Nikolić V (2015) Risks to stocks of native trout of the genus Salmo (Actinopterygii: Salmoniformes: Salmonidae) of Serbia and management for their recovery. Acta Ichthyol Piscat 45:161–173. https://doi.org/10.3750/AIP2015.45.2.06
Simonović P, Marić S, Tošić A, Škraba Jurlina D, Nikolić V (2018) Morphological and molecular differentiation between rheophilic barbels Barbus spp. (Cyprinidae) from headwaters at the divide between drainage areas of the Danube, Vardar and Struma rivers, Central Balkans. Acta Zool Bulg 70:153–164
Snoj A, Glamuzina B, Razpet A, Zablocki J, Bogut I, Lerceteau-Köhler E, Pojskić N, Sušnik S (2010) Resolving taxonomic uncertainties using molecular systematics: Salmo dentex and the Balkan trout community. Hydrobiologia 651:199–212. https://doi.org/10.1007/s10750-010-0297-5
Snoj A, Marić S, Sušnik Bajec S, Berrebi P, Janjani S, Schöffmann J (2011) Phylogeographic structure and demographic patterns of brown trout in North-West Africa. Mol Phylogenet Evol 61:203–211. https://doi.org/10.1016/j.ympev.2011.05.011
Sotiropoulos K, Eleftherakos K, Džukić G, Kalezić ML, Legakis A, Polymeni RM (2007) Phylogeny and biogeography of the alpine newt Mesotriton alpestris (Salamandridae, Caudata), inferred from mtDNA sequences. Mol Phylogenet Evol 45:211–226. https://doi.org/10.1016/j.ympev.2007.03.012
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
Splendiani A, Ruggeri P, Giovannotti M, Pesaresi S, Occhipinti G, Fioravanti T, Lorenzoni M, Nisi Cerioni P, Caputo Barucchi V (2016) Alien brown trout invasion of the Italian peninsula: the role of geological, climate and anthropogenic factors. Biol Invasions 18:2029–2044. https://doi.org/10.1007/s10530-016-1149-7
Stanković D, Crivelli AJ, Snoj A (2015) Rainbow trout in Europe: introduction, naturalization, and impacts. Rev Fish Sci Aquac 23:39–71. https://doi.org/10.1080/23308249.2015.1024825
Stapp P, Hayward GD (2002) Effects of an introduced piscivore on native trout: insights from a demographic model. Biol Invasions 4:299–316. https://doi.org/10.1023/A:1020985331815
Stevanović V, Jovanović S, Lakušić D, Niketić D (1995) Biodiverzitet Jugoslavije sa pregledom vrsta od međunarodnog značaja [Diversity of vascular flora of Yugoslavia with the survey of international valuable species]. Ecolibri, Biološki fakultet, Beograd [In Serbian]
Suárez J, Bautista JM, Almodóvar A, Machordom A (2001) Evolution of mitochondrial control region in Palaeartic brown trout (Salmo trutta) populations: the biogeographical role of the Iberian Peninsula. Heredity 87:198–206. https://doi.org/10.1046/j.1365-2540.2001.00905.x
Sušnik S, Snoj A, Wilson IF, Mrdak D, Weiss S (2007) Historical demography of brown trout (Salmo trutta) in the Adriatic drainage including the putative S. letnica endemic to Lake Ohrid. Mol Phylogenet Evol 44:63–76. https://doi.org/10.1016/j.ympev.2006.08.021
Sušnik BS, Pustovrh G, Jesenšek D, Snoj A (2015) Population genetic SNP analysis of marble and brown trout in a hybridization zone of the Adriatic watershed in Slovenia. Biol Conserv 184:239–250. https://doi.org/10.1016/j.biocon.2015.01.033
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Taniguchi Y, Fausch KD, Nakano S (2002) Size-structured Interactions between Native and Introduced Species: can intraguild predation facilitate invasion by stream salmonids? Biol Invasions 4:223–233. https://doi.org/10.1023/A:1020915416559
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X windows interface: flexibile strategies for multiple sequence aligment aided by quality analysis tools. Nucleic Acid Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Tot I, Slacki A, Đurić M, Popović M (2015) Butterflies of the Vlasina region in Southeast Serbia (Lepidoptera: Papilionoidea). Acta Entomol Serb 20:117–135. https://doi.org/10.5281/zenodo.45393
Uiblein F, Jagsch A, Honsig-Erlenburg W, Weiss S (2001) Status, habitat use, and vulnerability of the European grayling in Austrian waters. J Fish Biol 59:223–247. https://doi.org/10.1111/j.1095-8649.2001.tb01388.x
Utter FM (1981) Biological criteria for definition of species and distinct intraspecific populations and salmonids under the U. S. Endangered Species Act of 1973. Can J Fish Aquat Sci 38:1626–1635. https://doi.org/10.1139/f81-212
Vähä JP, Erkinaro J, Niemelä E, Primmer CR (2007) Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Mol Ecol 16:2638–2654. https://doi.org/10.1111/j.1365-294X.2007.03329.x
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Vera M, Cortey M, Sanz N, García-Marín J-L (2010) Maintenance of an endemic lineage of brown trout (Salmo trutta) inside the Duero river basin. J Zool Syst Evol Res 48:181–187. https://doi.org/10.1111/j.1439-0469.2009.00547.x
Vera M, García-Marín JL, Martínez P, Araguas RM, Bouza C (2013) Identification and conservation of remnant genetic resources of brown trout in relict populations from Western Mediterranean streams. Hydrobiologia 707:29–45. https://doi.org/10.1007/s10750-012-1402-8
Waters JM (2011) Competitive exclusion: phylogeography’s ‘elephant in the room’? Mol Ecol 20:4388–4394. https://doi.org/10.1111/j.1365-294X.2011.05286.x
Waters JM, Fraser CI, Hewitt GM (2013) Founder takes all: density-dependent processes structure biodiversity. Tree 28:P78-85. https://doi.org/10.1016/j.tree.2012.08.024
Waters JM, Burridge CP, Craw D (2020) River capture and freshwater biological evolution: a review of Galaxiid Fish Vicariance. Diversity 12:216. https://doi.org/10.3390/d12060216
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol 38:1358–1370. https://doi.org/10.1111/j.1558-5646.1984.tb05657.x
Weiss S, Schlötterer C, Waidbacher H, Jungwirth M (2001) Haplotype (mtDNA) diversity of brown trout Salmo trutta in tributaries of the Austrian Danube: massive introgression of Atlantic basin fish–by man or nature? Mol Ecol 10:1241–1246. https://doi.org/10.1046/j.1365-294x.2001.01261.x
Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49. https://doi.org/10.1016/j.tree.2014.10.009
Acknowledgements
The authors wish to express their gratitude to Živojin Stojilković and Ninoslav Kostić from the Association “Veternica—Vlasina” DOO Leskovac, and Nenad Lazarević from the Faculty of Biology, University of Belgrade, for their irrepressible support during realisation of this study. We also thank Anna Nikolić for her comprehensive linguistic help.
Funding
The authors acknowledge the financial support of the Slovenian Research Agency (SSB and AS, research core funding no. P4–0220 and project J4–8218; DS, research core funding No. P1-0255 and P1-0237 and project J1-3015). SM was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. 451–03-9/2021–14/20017), RŠ by the Ministry of Culture of the Czech Republic (DKRVO 2019–2023/6.V.c National Museum, 00023272), JV by institutional resources of the Ministry of Education, Youth and Sports of the Czech Republic. DS was additionally supported by the Slovenian Ministry of Education, Science and Sport and the European Regional Development Fund: Operational Programme for the Implementation of the EU Cohesion Policy in the period 2014–2020 (5442–15/2016/18, C3330-17–529025), and by RI-SI-2 LifeWatch (Operational Programme for the Implementation of the EU Cohesion Policy in the period 2014–2020, Development of Research infrastructure for international competition of Slovene Development of Research infrastructure area).
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SM, RŠ and JV performed the laboratory work. SM and DS wrote the manuscript with assistance from SSB and AS. SM, DS and SSB conducted the data analyses. SM organized the logistic for the fieldwork with assistance from DN and TS. DN and TS participated in the collection of data and helped to draft the manuscript. AS coordinated and supervised the study. All authors read and approved the final manuscript.
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Marić, S., Stanković, D., Sušnik Bajec, S. et al. Perils of brown trout (Salmo spp.) mitigation-driven translocations: a case study from the Vlasina Plateau, Southeast Serbia. Biol Invasions 24, 999–1016 (2022). https://doi.org/10.1007/s10530-021-02688-0
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DOI: https://doi.org/10.1007/s10530-021-02688-0