Abstract
Mediterranean brown trout is subject to several serious threats such as pollution, water abstraction, habitat alteration and especially genetic introgression with domestic strains used for stocking activities. Despite this latter issue has largely been debated by scientists, local managers and stakeholders for decades, official stocking practices with domestic trout still persists in several countries (Italy included), even if there are laws explicitly prohibiting introduction of organisms of non-local origin. Probably, the last opportunity to conserve native brown trout populations is represented by protected areas. Therefore, in the present study, we aimed to verify the role of the Nature 2000 network and a national park as valid tools to guarantee the survival of native brown trout in the Apennines. Partial mitochondrial DNA control region sequence analysis and genotyping of the locus LDH-C1* and 11 microsatellites were used to investigate the genetic diversity of three rivers from central Italy. For all rivers investigated a temporal analysis of introgression was also carried out. The genetic diversity of three domestic stocks was included in the sampling design for comparison. The main results of this study indicated that: (i) the genetic diversity of brown trout in central Italy is very complex and (ii) its conservation is seriously threatened by genetic introgression phenomena still ongoing. The only samples showing no introgression or a decrease in genetic introgression were those isolated by the presence of natural and/or artificial barriers to fish movements rather than protected by inhabiting rivers within the Natura 2000 network. This observation prompts an important reflection on issues concerning fluvial continuity restoration and suggests that barrier removal should be undertaken with caution in order to avoid the concrete risk of domestic trout spreading that could promote additional loss of native brown trout biodiversity.
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References
Araki H, Berejikian BA, Ford MJ, Blouin MS (2008) SYNTHESIS: fitness of hatchery-reared salmonids in the wild. Evol Appl 1:342–355. https://doi.org/10.1111/j.1752-4571.2008.00026.x
Aurelle D, Aurelle D, Berrebi P, Berrebi P (2001) Genetic structure of brown trout (Salmo trutta, L.) populations from south-western France: data from mitochondrial control region variability. Mol Ecol 10:1551–1561. https://doi.org/10.1046/j.1365-294X.2001.01293.x
Bernatchez L (2001) The evolutionary history of brown trout (Salmo trutta L.) inferred from phylogeographic, nested clade, and mismatch analyses of mitochondrial DNA variation. Evolution 55:351–379. https://doi.org/10.2307/2640757
Berrebi P, Caputo Barucchi V, Splendiani A, Muracciole S, Sabatini A, Palmas F, Tougard C, Arculeo M, Maric 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
Bettles CM, Docker MF, Dufour B, Heath DD (2005) Hybridization dynamics between sympatric species of trout: loss of reproductive isolation. J Evol Biol 18:1220–1233. https://doi.org/10.1111/j.1420-9101.2005.00935.x
Bianco PG (1995) Mediterranean endemic freshwater fishes of Italy. Biol Conserv 72:159–170. https://doi.org/10.1016/0006-3207(94)00078-5
Bianco PG (2014) An update on the status of native and exotic freshwater fishes of Italy. J Appl Ichthyol 30:62–77. https://doi.org/10.1111/jai.12291
Caputo V (2003) Ricerche sulla biodiversità della trota fario (Salmo trutta L., 1758) nella Provincia di Pesaro e Urbino e nelle Marche. Quaderni dell’Ambiente, n° 15. Provincia di Pesaro e Urbino, Gestione e tutela delle acque interne, Pesaro
Caputo V, Giovannotti M, Nisi Cerioni P, Caniglia ML, Splendiani A (2004) Genetic diversity of brown trout in central Italy. J Fish Biol 65:403–418. https://doi.org/10.1111/j.1095-8649.2004.00458.x
Caputo V, Giovannotti M, Splendiani A (2010) Pattern of gonad maturation in a highly stocked population of brown trout (Salmo trutta L., 1758) from Central Italy. Ital J Zool 77:14–22. https://doi.org/10.1080/11250000802589576
Champigneulle A, Largiader C, Caudron A (2003) Reproduction De La Truite (Salmo Trutta L.) Dans Le Torrent De Chevenne, Haute Savoie. Un Fonctionnement Original? Bull Fr Pêche Piscic 369:41–70
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. https://doi.org/10.1093/molbev/msl191
Cortey M, Pla C, García-Marín JL (2004) Historical biogeography of Mediterranean trout. Mol Phylogenet Evol 33:831–844. https://doi.org/10.1016/j.ympev.2004.08.012
Coyne JA; Orr HA Speciation
Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B Methodol 39:1–38. https://doi.org/10.2307/2984875
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fabiani A, Gratton P, Zappes IA, Seminara M, D’Orsi A, Sbordoni V, Allegrucci G (2018) Investigating the genetic structure of trout from the Garden of Ninfa (central Italy): suggestions for conservation and management. Fish Manag Ecol 25:1–11. https://doi.org/10.1111/fme.12259
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Gandolfi G, Torricelli P, Zerunian S, Marconato A (1991) I pesci delle acque interne italiane. Unione Zoologica Italiana, Istituto Poligrafico e Zecca dello Stato, Rome
García-Marín JL, Sanz N, Pla C (2008) Proportions of native and introduced brown trout in adjacent fished and unfished Spanish rivers. Conserv Biol 12:313–319. https://doi.org/10.1111/j.1523-1739.1998.96133.x
Gortázar J, García De Jalón D, Alonso-González C et al (2007) Spawning period of a southern brown trout population in a highly unpredictable stream. Ecol Freshw Fish 16:515–527. https://doi.org/10.1111/j.1600-0633.2007.00246.x
Goudet J (1994) FSTAT (Version 1. 2): a computer program to Computer Note Computer Program to. 2-4
Gratton P, Allegrucci G, Gandolfi A, Sbordoni V (2013) Genetic differentiation and hybridization in two naturally occurring sympatric trout Salmo spp. forms from a small karstic lake. J Fish Biol 82:637–657. https://doi.org/10.1111/jfb.12022
Gratton P, Allegrucci G, Sbordoni V, Gandolfi A (2014) The evolutionary jigsaw puzzle of the surviving trout (salmo trutta L. complex) diversity in the italian region. a multilocus bayesian approach. Mol Phylogenet Evol 79:292–304. https://doi.org/10.1016/j.ympev.2014.06.022
Hansen MM, Mensberg K-LD (2009) Admixture analysis of stocked brown trout populations using mapped microsatellite DNA markers: indigenous trout persist in introgressed populations. Biol Lett 5:656–659. https://doi.org/10.1098/rsbl.2009.0214
Hansen MM, Bekkevold D, JensenLF et al (2006) Genetic restoration of a stocked brown trout Salmo trutta population using microsatellite DNA analysis of historical and contemporary samples. J Appl Ecol 43:669–679. https://doi.org/10.1111/j.1365-2664.2006.01185.x
Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916. https://doi.org/10.1111/j.1365-294X.2005.02480.x
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
Klemetsen A, P-a A, Jb D, Jonsson B (2003) Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus L.: a review of aspects of their life histories. 1–59
Kottelat M, Freyhof J (2007) Handbook of european fresh-water fishes. Publications Kottelat, Cornol
Lorenzoni M, Mearelli M, Ghetti L (2006) Native and exotic fish species fish in the tiber River watershed (Umbria–Italy) and their relationship to the longitudinal gradient. Bull Fr Pêche Piscic 382:19–44
Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237. https://doi.org/10.1016/j.tree.2005.02.010
McMeel OM, Hoey EM, Ferguson A (2001) Partial nucleotide sequences, and routine typing by polymerase chain reaction-restriction fragment length polymorphism, of the brown trout (Salmo trutta) lactate dehydrogenase, LDH-C1*90 and *100 alleles. Mol Ecol 10:29–34. https://doi.org/10.1046/j.1365-294X.2001.01166.x
Montgomery ME, Woodworth LM, Nurthen RK et al (2000) Relationships between population size and loss of genetic diversity: comparisons of experimental results with theoretical predictions. Conserv Genet 1:33–43. https://doi.org/10.1023/A:1010173401557
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1111/j.1471-8286.2007.01758.x
Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: Subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627. https://doi.org/10.1111/1755-0998.12512
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
Ryman N (2006) CHIFISH: a computer program testing for genetic heterogeneity at multiple loci using chi-square and Fisher’s exact test. Mol Ecol Notes 6:285–287. https://doi.org/10.1111/j.1471-8286.2005.01146.x
Schenekar T, Weiss S (2017) Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (Salmo trutta) populations. Conserv Genet 18:1011–1022. https://doi.org/10.1007/s10592-017-0949-3
Shields BA, Stubbing DN, Summers DW, Giles N (2005) Temporal and spatial segregation of spawning by wild and farm-reared brown trout, Salmo trutta L. Fish Manag Ecol 12:77–79. https://doi.org/10.1111/j.1365-2400.2004.00429.x
Splendiani A, Giovannotti M, Cerioni PN, Caniglia ML, Caputo V (2006) Phylogeographic inferences on the native brown trout mtDNA variation in central Italy. Ital J Zool 73:179–189. https://doi.org/10.1080/11250000600679751
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(7):2029–2044
Suárez J, Bautista JM, Almodóvar A, Machordom A (2001) Evolution of the mitochondrial control region in Palaearctic 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
Taylor EB (2003) Evolution in mixed company - Evolutionary inferences from studies of natural hybridization in Salmonidae. Evol Illum Salmon Their Relat Salmon Their Relat 1:232–263
Tougard C, Justy F, Guinand B, Douzery EJP, Berrebi P (2018) Salmo macrostigma (Teleostei, Salmonidae): Nothing more than a brown trout (S. trutta) lineage? J Fish Biol 93:302–310. https://doi.org/10.1111/jfb.13751
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 JL (2010) Maintenance of an endemic lineage of brown trout (Salmo trutta) within the Duero river basin. J Zool Syst Evol Res 48:181–187. https://doi.org/10.1111/j.1439-0469.2009.00547.x
Acknowledgements
The authors are grateful to Gary A. Winans (Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, Seattle, Washington, USA) and an anonymous reviewer for the their constructive comments on the earlier version of this manuscript. The authors are grateful to Andrea Gandolfi (Istituto Agrario di San Michele all’Adige, Fondazione Edmund Mach, San Michele All’Adige, Italy) for his useful suggestions about the statistical treatment of the data. Funding was provided by European Commission (LIFE 12 NAT/IT/000940) and Università Politecnica delle Marche.
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10592_2018_1135_MOESM1_ESM.pptx
A) Plot of mean LnP(K) values for 8 wild brown trout samples and 3 hatchery samples from central Italy and B) Plot of MedMeaK and MaxMeaK indices.. Supplementary material 1 (PPTX 104 KB)
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Splendiani, A., Giovannotti, M., Righi, T. et al. Introgression despite protection: the case of native brown trout in Natura 2000 network in Italy. Conserv Genet 20, 343–356 (2019). https://doi.org/10.1007/s10592-018-1135-y
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DOI: https://doi.org/10.1007/s10592-018-1135-y