Abstract
Pacu (Piaractus mesopotamicus) is one of the most important Neotropical freshwater fish species produced by aquaculture in South America. This study is the first attempt to inquire about aquaculture stocks in Argentina regarding genetic diversity and structure. Neither genetic characterization nor pedigree records are available for pacu stocks in farms in Argentina. The presence of hybrids in both natural environment (Lower Paraná River) and farms has not been evaluated yet at the southern region of pacu distribution. Genetic characterization of pacu broodstocks, corresponding to 8 farms, and wild individuals from four areas at Lower Paraná River was performed. Pacu hybrids were not detected neither in wild nor in farm stocks analyzed. In general, similar levels of genetic diversity were observed between cultured and wild fish populations. Global genetic differentiation (Fst = 0.055) indicated a low level of structure and AMOVA showed that genetic variation was mostly within populations. Reduced contemporary effective population size (Ne) was observed, and probably reflects the bottleneck by founder effect in farmed fish populations. Moreover, kinship analysis showed that in fish farms, on average, 43.00% of the individuals were genetically related, whereas in wild population it was 36.40%. We recommend that broodstock management practices, such as using large Ne, single pair mating, precise records, and tagging of brood fish, should be implemented to avoid unintentional mismanagement.
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References
Agostinho AA, Gomes LC, Suzuki HI, Júlio HF Jr (2003) Migratory fish of upper Paraná River basin, Brazil. In: Carolsfeld J, Harvey B, Baer A, Ross C (eds) Migratory fishes of South America: biology, fisheries, and conservation status. World Fisheries Trust, Victoria, pp 19–99
Alarcón JA, Magoulas A, Georgakopoulos T, Zouros E, Alvarez MC (2004) Genetic comparison of wild and cultivated European populations of the gilthead sea bream (Sparus aurata). Aquaculture 230:65–80. https://doi.org/10.1016/s0044-8486(03)00434-4
Allendorf FW, Luikart G (2009) Conservation and the genetics of populations. John Wiley Sons
Beaumont AR, Hoare K (2003) Genetic considerations in the hatchery. In: Beaumont AR, Hoare K (eds) Biotechnology and genetics in fisheries and aquaculture. Blackwell Science, Oxford, pp 73–90. https://doi.org/10.1002/9780470995198.ch4
Bradbeer SJ, Harrington J, Watson H, Warraich A, Shechonge A, Smith A, Tamatamah R, Ngatunga BP, Turner GF, Genner MJ (2019) Limited hybridization between introduced and Critically Endangered indigenous tilapia fishes in northern Tanzania. Hydrobiologia 832(1):257–268
Caballero A, Bravo I, Wang J (2016) Inbreeding load and purging: implications for the short-term survival and the conservation management of small populations. Heredity 118:177–185
Calcagnotto D, DeSalle R (2009) Population genetic structuring in pacu (Piaractus mesopotamicus) across the Paraná-Paraguay basin: evidence from microsatellites. Neotropic Ichthyol 7:607–616. https://doi.org/10.1590/s1679-62252009000400008
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144(4):2001–2014
Corvalán Romero C, Roselló R, Suárez M, Mitchell C (2014) Manual de procedimientos para el engorde de pacu. Ministerio de la Producción, Secretaría del Sistema Hidrico, Forestal y Minero, Gobierno de la Provincia de Santa Fe
Criscuolo-Urbinati E, Kuradomi RY, Urbinati EC, Batlouni SR (2012) The administration of exogenous prostaglandin may improve ovulation in pacu (Piaractus mesopotamicus). Theriogenology 78:2087–2094. https://doi.org/10.1016/j.theriogenology.2012.08.001
do Prado FD, Fernandez-Cebria R, Hashimoto DT, Senhorini JA, Foresti F, Martınez P, Porto-Foresti F (2017) Hybridization and genetic introgression patterns between two South American catfish along their sympatric distribution range. Hydrobiologia 788:319–343
Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimatorv2: 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
Duncan NJ, Sonesson AK, Chavanne H (2013) Principles of finfish broodstock management in aquaculture: control of reproduction and genetic improvement. Adv Aquacult Hatch Technol:23–75. https://doi.org/10.1533/9780857097460.1.23
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
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, 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
FAO (2010) The State of World Fisheries and Aquaculture 2010. Rome, Italy, 197. Available at: http://www.fao.org/3/a-i1820e.pdf. Accessed December 2020
FAO (2017) Planning for aquaculture diversification: the importance of climate change and other drivers. In: Harvey B, Soto D, Carolsfeld J, Beveridge M, Bartley DM (eds) FAO Technical Workshop, 23–25 June 2016, FAO Rome. FAO Fisheries and Aquaculture Proceedings. No. 47. FAO, Rome 166 pp
FAO (2018). The State of World Fisheries and Aquaculture 2018 - Meeting the sustainable development goals. Rome. Licence: CC BY-NC-SA 3.0 IGO
Flores Nava A (2007) Aquaculture seed resources in Latin America: a regional synthesis, pp. 91–102. In: M.G. Bondad-Reantaso (ed.). Assessment of freshwater fishseed resources for sustainable aquaculture. FAO Fisheries Technical Paper. No. 501.Rome, FAO. 628p
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318. https://doi.org/10.1046/j.1365-294x.2001.01190.x
Gjedrem T, Baranski M (2009) Selective breeding in aquaculture: an introduction. Rev: Methods Technol Fish Biol Fish. . doi:. https://doi.org/10.1007/978-90-481-2773-3
Gonçalves RA, dos Santos CH d A, de Sá Leitão CS, de Souza ÉMS, de Almeida-Val VMF (2019) Genetic basis of Colossoma macropomum broodstock: perspectives for an improvement program. J World Aquacult Soc 50:633–644. https://doi.org/10.1111/jwas.12564
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Lausanne University, Lausanne
Hashimoto DT, Mendonça FF, Senhorini JA, de Oliveira C, Foresti F, Porto-Foresti F (2011) Molecular diagnostic methods for identifying Serrasalmid fish (Pacu, Pirapitinga, and Tambaqui) and their hybrids in the Brazilian aquaculture industry. Aquaculture 321:49–53. https://doi.org/10.1016/j.aquaculture.2011.08.018
Hashimoto DT, Senhorini JA, Foresti F, Martínez P, Porto-Foresti F (2014) Genetic identification of F1 and Post-F1 Serrasalmid juvenile hybrids in Brazilian aquaculture. PLoS One 9:e89902. https://doi.org/10.1371/journal.pone.0089902
Honglang H (2007) Freshwater fish seed resources in China. pp. 185–199. In: Bondad-Reantaso MG (ed) Assessment of freshwater fish seed resources for sustainable aquaculture. FAO Fisheries Technical Paper. No. 501. FAO, Rome 628p
IBGE (2017) Instituto Brasileiro de Geografia e Estatística. Produção Pecuária Municipal 2016, Rio de Janeiro, Brazil, v. 44, p. 1–51
Iervolino F, de Resende EK, Hilsdorf AWS (2010) The lack of genetic differentiation of pacu (Piaractus mesopotamicus) populations in the Upper-Paraguay Basin revealed by the mitochondrial DNA D-loop region: implications for fishery management. Fish Res 101:27–31. https://doi.org/10.1016/j.fishres.2009.09.003
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
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
Jorge PH, Mastrochirico-Filho VA, Hata ME, Mendes NJ, Ariede RB, de Freitas MV, … Hashimoto DT (2018) Genetic characterization of the fish Piaractus brachypomus by Microsatellites derived from transcriptome sequencing. Frontiers in Genetics 9. doi:https://doi.org/10.3389/fgene.2018.00046
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. https://doi.org/10.1111/j.1365-294x.2007.03089.x
Kincaid HL (1983) Inbreeding in fish populations used for aquaculture. Aquaculture 33:215–227. https://doi.org/10.1016/0044-8486(83)90402-7
Kohlmann K, Kersten P, Flajšhans M (2005) Microsatellite-based genetic variability and differentiation of domesticated, wild and feral common carp (Cyprinus carpio L.) populations. Aquaculture 247:253–266. https://doi.org/10.1016/j.aquaculture.2005.02.024
Luchini L (2017) Piscicultura: el caso del “sistema de rotación arroz-pacu en el país. Dirección de Acuicultura – DNPP Subsecretaría de Pesca y Acuicultura, Ministerio de Agroindustria, Presidencia de la Nación Argentina. Available at: https://www.agroindustria.gob.ar/sitio/areas/acuicultura/publicaciones/_archivos//000000_Desarrollos%20Acu%C3%ADcolas/171200_Piscicultura,%20el%20caso%20del%20Sistema%20de%20Rotaci%C3%B3n%20Arroz-Pac%C3%BA%20en%20el%20pa%C3%ADs.pdf. Accessed December 2020
Mastrochirico-Filho VA, del Pazo F, Hata ME, Villanova GV, Foresti F, Vera M, Martínez P, Porto-Foresti F, Hashimoto DT (2019) Assessing genetic diversity for a pre-breeding program in Piaractus mesopotamicus by SNPs and SSRs. Genes 10:668. https://doi.org/10.3390/genes10090668
McKelvey KS, Young MK, Wilcox TM, Bingham DM, Pilgrim KL, Schwartz MK (2016) Patterns of hybridization among cutthroat trout and rainbow trout in northern Rocky Mountain streams. Ecol Evol 6:688–706. https://doi.org/10.1002/ece3.1887
Naish KA, Seamons TR, Dauer MB, Hauser L, Quinn TP (2013) Relationship between effective population size, inbreeding and adult fitness-related traits in a steelhead (Oncorhynchus mykiss) population released in the wild. Mol Ecol 22:1295–1309. https://doi.org/10.1111/mec.12185
O’Connell M, Wright JM (1997) Rev Fish Biol Fish 7:331–363. https://doi.org/10.1023/a:1018443912945
Panné Huidobro S (2016) Producción por Acuicultura en Argentina en el 2016. Informe de la Dirección de Acuicultura Dirección Nacional de Planificación Pesquera Subsecretaría de Pesca y Acuicultura Ministerio de Agroindustria. Available at: https://www.magyp.gob.ar/sitio/areas/acuicultura/boletin/_archivos//160000_2016/160800_Bolet%C3%ADn%20de%20la%20Direcci%C3%B3n%20de%20Acuicultura%20(Agosto%202016).pdf. Accessed December 2020
Posner V (2016) Desarrollo de herramientas biotecnológicas para el cultivo de pacu (Piaractus mesopotámicus). [Dissertation, Universidad Nacional de Rosario]. Facultad de Ciencias Bioquímicas y Farmacéuticas Repository. Universidad Nacional de Rosario
Povh JA, Ribeiro RP, Lopera-Barrero NM, Jacometo CB, Vargas L, Gomes PC, da Silva Lopes T (2011) Microsatellite analysis of pacu broodstocks used in the stocking program of Paranapanema River, Brazil. Sci Agric 68:308–313. https://doi.org/10.1590/s0103-90162011000300006
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258. https://doi.org/10.2307/2409206
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
Reid SM, Wilson CC, Mandrak NE, Carl LM (2008) Population structure and genetic diversity of black redhorse (Moxostoma duquesnei) in a highly fragmented watershed. Conserv Genet 9:531–546. https://doi.org/10.1007/s10592-007-9367-2
Resende EK (2003) Migratory fishes of the Paraguay-Paraná basin excluding the Upper Paraná River. In: Carolsfeld J, Harvey B, Ross C, Baers A (eds) Migratory fishes of South America: biology, fisheries and conservation states. World Bank, Victoria, pp 99–156
Ringuelet RA, Arámburu RH, de Aramburu AA (1967) Los peces argentinos de agua dulce. Comisión de Investigación Científica. Provincial de Buenos Aires. Available at: http://sedici.unlp.edu.ar/handle/10915/62009. Accessed December 2020
Rousset F (2008) genepop’007: a complete re-implementation 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
Silva SSD, De Silva SS, Nguyen TTT, Turchini GM, Amarasinghe US, Abery NW (2009) Alien species in aquaculture and biodiversity: a paradox in food production. AMBIO 38:24–28. https://doi.org/10.1579/0044-7447-38.1.24
Smith WS, Espindola ELG, Petrere Jr M, Rocha O (2003) Fishing modification due to dam, pollution and introduction fish species in the Tietê River, SP, Brazil. In: CA, Brebbia (ed.) River basin management II. Great Britain: WITPRESS. WIT Transactions on Ecology and the Environment, vol. 60
Valladão GMR, Gallani SU, Pilarski F (2018) South American fish for continental aquaculture. Rev Aquac 10:351–369. https://doi.org/10.1111/raq.12164
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
Vandeputte M, Haffray P (2014) Parentage assignment with genomic markers: a major advance for understanding and exploiting genetic variation of quantitative traits in farmed aquatic animals. Front Genet 5:432
Villanova GV, Vera M, Díaz J, Martinez P, Calcaterra NB, Arranz SE (2015) Isolation and characterization of 20 polymorphic microsatellite loci in the migratory freshwater fishLeporinus obtusidens(Characiformes: Anostomidae) using 454 shotgun pyrosequencing. J Fish Biol 86:1209–1217. https://doi.org/10.1111/jfb.12632
Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res 89:135–153. https://doi.org/10.1017/s0016672307008798
Wang J (2011) coancestry: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145. https://doi.org/10.1111/j.1755-0998.2010.02885.x
Weir BS, Clark Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358. https://doi.org/10.2307/2408641
Wicki G, Wiltchiensky E (2017) Producción de pacú en el nordeste argentino. Ministerio de agroindustria. Presidencia de la Nación. Available at: https://www.magyp.gob.ar/sitio/areas/acuicultura/economia/_archivos//171027_Producci%C3%B3n%20y%20an%C3%A1lisis%20econ%C3%B3mico%20de%20Pac%C3%BA%202017.pdf. Accessed December 2020
Wilson AJ, Gíslason D, Skúlason S, Snorrason SS, Adams CE, Alexander G, Danzmann RG, Ferguson MM (2004) Population genetic structure of Arctic charr, Salvelinus alpinus from northwest Europe on large and small spatial scales. Mol Ecol 13(5):1129–1142
Zhang J, Wang X, Yao J, Li Q, Liu F, Yotsukura N, … Duan D (2017) Effect of domestication on the genetic diversity and structure of Saccharina japonica populations in China. Sci Rep https://doi.org/10.1038/srep42158
Acknowledgments
We would like to thank Argentinian aquaculture farms and sport fishermen for their kind donation of samples. FdP is a postdoctoral fellow, and SS, AAS, and GVV are members of the Research Career from the National Council of Scientific and Technological Research (CONICET) from Argentina.
Funding
This work was supported by the National Agency for the Promotion of Science and technology from Argentina (ANPCyT) and the Government of Santa Fe state (grant numbers: PID 020-2013 and PICT 0510-2011).
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GVV, SA, and FdP conceived the study; FdP, SS, and VP conducted the experiments; FdP, AS, and GVV analyzed the data; and FdP, SA, and GVV wrote the manuscript. All authors read and approved the final version.
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This study was conducted in strict accordance with the recommendations of the Animal Ethical Committee at Facultad de Ciencias Bioquímicas y Farmacéuticas-Universidad Nacional de Rosario. Protocol approval has been received (protocol no. 302/2013).
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del Pazo, F., Sánchez, S., Posner, V. et al. Genetic diversity and structure of the commercially important native fish pacu (Piaractus mesopotamicus) from cultured and wild fish populations: relevance for broodstock management. Aquacult Int 29, 289–305 (2021). https://doi.org/10.1007/s10499-020-00626-w
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DOI: https://doi.org/10.1007/s10499-020-00626-w