Interspecific Genetic Differences and Historical Demography in South American Arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum)

. 2019 Sep 09 ; 10 (9) : . [epub] 20190909

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31505864

The South American arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum) are emblematic species widely distributed in the Amazon and surrounding basins. Arowana species are under strong anthropogenic pressure as they are extensively exploited for ornamental and food purposes. Until now, limited genetic and cytogenetic information has been available, with only a few studies reporting to their genetic diversity and population structure. In the present study, cytogenetic and DArTseq-derived single nucleotide polymorphism (SNP) data were used to investigate the genetic diversity of the two Osteoglossum species, the silver arowana O. bicirrhosum, and the black arowana O. ferreirai. Both species differ in their 2n (with 2n = 54 and 56 for O. ferreirai and O. bicirrhosum, respectively) and in the composition and distribution of their repetitive DNA content, consistent with their taxonomic status as different species. Our genetic dataset was coupled with contemporary and paleogeographic niche modeling, to develop concurrent demographic models that were tested against each other with a deep learning approach in O. bicirrhosum. Our genetic results reveal that O. bicirrhosum colonized the Tocantins-Araguaia basin from the Amazon basin about one million years ago. In addition, we highlighted a higher genetic diversity of O. bicirrhosum in the Amazon populations in comparison to those from the Tocantins-Araguaia basin.

Zobrazit více v PubMed

Antonelli A., Zizka A., Carvalho F.A., Scharn R., Bacon C.D., Silvestro D., Condamine F.L. Amazonia is the primary source of Neotropical biodiversity. Proc. Natl. Acad. Sci. USA. 2018;115:6034–6039. doi: 10.1073/pnas.1713819115. PubMed DOI PMC

Reis R.E., Albert J.S., Di Dario F., Mincarone M.M., Petry P., Rocha L.A. Fish biodiversity and conservation in South America. J. Fish Biol. 2016;89:12–47. doi: 10.1111/jfb.13016. PubMed DOI

Hubert N., Renno J.F. Historical biogeography of South American freshwater fishes. J. Biogeogr. 2006;33:1414–1436. doi: 10.1111/j.1365-2699.2006.01518.x. DOI

Hoorn C., Wesselingh F.P., ter Steege H., Bermudez M.A., Mora A., Sevink J., Sanmartin I., Sanchez-Meseguer A., Anderson C.L., Figueiredo J.P., et al. Amazonia Through Time: Andean Uplift, Climate Change, Landscape Evolution, and Biodiversity. Science. 2010;330:927–931. doi: 10.1126/science.1194585. PubMed DOI

Garzon-Orduna I.J., Benetti-Longhini J.E., Brower A.V.Z. Timing the diversification of the Amazonian biota: Butterfly divergences are consistent with Pleistocene refugia. J. Biogeogr. 2014;41:1631–1638. doi: 10.1111/jbi.12330. DOI

Rull V. Neotropical diversification: Historical overview and conceptual insights. Peer J. Prepr. 2018 doi: 10.7287/peerj.preprints.27294v1. DOI

Rull V. Pleistocene speciation is not refuge speciation. J. Biogeogr. 2015;42:602–604. doi: 10.1111/jbi.12440. DOI

Val A.L., Almeida-Val V.M.F. Fishes of the Amazon and Their Environment. Volume 32. Springer; Berlin/Heidelberg, Germany: 1995. The Amazon ichthyofauna; pp. 28–69.

Queiroz H.L., Camargo M. Biologia, Conservação e Manejo dos Aruanãs na Amazônia Brasileira. IDSM; Tefé, Brazil: 2008. 152p

Duponchelle F., Arce A.R., Waty A., Panfili J., Renno J.-F., Farfan F., Garcia-Vasquez A., Koo F.C., Davila C.G., Vargas G. Contrasted hydrological systems of the Peruvian Amazon induce differences in growth patterns of the silver arowana, Osteoglossum bicirrhosum. Aquat. Living Resour. 2012;25:55–66. doi: 10.1051/alr/2012005. DOI

Duponchelle F., Ruiz Arce A., Waty A., Garcia-Vasquez A., Renno J., Chu-Koo F., Garcia-Davila C., Vargas G., Tello S., Ortiz A. Variations in reproductive strategy of the silver Arowana, Osteoglossum bicirrhosum Cuvier, 1829 from four sub-basins of the Peruvian Amazon. J. Appl. Ichthyol. 2015;31:19–30. doi: 10.1111/jai.12973. DOI

Leal M.E.C., Sant’Anna V.B. Quantitative analysis of interspecific and ontogenetic variation in Osteoglossum species (Teleostei: Osteoglossiformes: Osteoglossidae) Zootaxa. 2006;1239:49–68. doi: 10.11646/zootaxa.1239.1.4. DOI

Saint-Paul U., Zuanon J., Correa M.A.V., García M., Fabré N.N., Berger U., Junk W.J. Fish communities in central Amazonian white-and blackwater floodplains. Environ. Biol. Fishes. 2000;57:235–250. doi: 10.1023/A:1007699130333. DOI

Duncan W.P., Fernandes M.N. Physicochemical characterization of the white, black, and clearwater rivers of the Amazon Basin and its implications on the distribution of freshwater stingrays (Chondrichthyes, Potamotrygonidae) Panam. J. Aquat. Sci. 2010;5:454–464.

Moreau M.-A., Coomes O.T. Potential threat of the international aquarium fish trade to silver arawana Osteoglossum bicirrhosum in the Peruvian Amazon. Oryx. 2006;40:152–160. doi: 10.1017/S0030605306000603. DOI

Amaral E.S.R., Arantes C.C. A pesca de aruanãs na região de Tefé. In: Queiroz H.L., Camargo M., editors. Biologia, Conservação e Manejo dos Aruanãs na Amazônia Brasileira. IDSM; Tefé, Brazil: 2008. pp. 61–74.

Rocha P., Ramíres P.F. Contribución a la Gestión Sostenible y al Conocimiento Biológico y Socio Económico de la Cadena de Valor de Peces Ornamentales de Puerto Carreño-Reserva de Biósfera el Tuparro (Vichada-Colombia) Fundación Omacha; Fundación Horizonte Verde; Bogotá, Colômbia: 2017.

Moreau M.-A., Coomes O.T. Aquarium fish exploitation in western Amazonia: Conservation issues in Peru. Environ. Conserv. 2007;34:12–22. doi: 10.1017/S0376892907003566. DOI

Reis R., Lima F. Osteoglossum ferreirai. The IUCN Red List of Threatened Species 2009. 2009. Available online: https://www.iucnredlist.org/species/167687/6367885. DOI

Mojica J.I., Usma J.S., Álvarez-León R., Lasso C.A. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Instituto de Ciencias Naturales de la Universidad Nacional de Colombia; WWF Colombia y Universidad de Manizales; Bogotá, Colômbia: 2012. Libro rojo de peces Dulceacuícolas de Colombia 2012.

Escobar L. M.D., Farias I.P., Taphorn B. D.C., Landines M., Hrbek T. Molecular diagnosis of the arowanas Osteoglossum ferreirai Kanazawa, 1966 and O. bicirrhossum (Cuvier, 1829) from the Orinoco and Amazon River basins. Neotrop. Ichthyol. 2013;11:335–340.

Olivares A.M., Hrbek T., Escobar M.D., Caballero S. Population structure of the black arowana (Osteoglossum ferreirai) in Brazil and Colombia: Implications for its management. Conserv. Genet. 2013;14:695–703. doi: 10.1007/s10592-013-0463-1. DOI

Ekblom R., Galindo J. Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity. 2011;107:1. doi: 10.1038/hdy.2010.152. PubMed DOI PMC

Garrick R.C., Bonatelli I.A.S., Hyseni C., Morales A., Pelletier T.A., Perez M.F., Rice E., Satler J.D., Symula R.E., Thomé M.T.C., et al. The evolution of phylogeographic data sets. Mol. Ecol. 2015;24:1164–1171. doi: 10.1111/mec.13108. PubMed DOI

Barby F.F., Bertollo L.A.C., de Oliveira E.A., Yano C.F., Hatanaka T., Ráb P., Sember A., Ezaz T., Artoni R.F., Liehr T., et al. Emerging patterns of genome organization in Notopteridae species (Teleostei, Osteoglossiformes) as revealed by Zoo-FISH and Comparative Genomic Hybridization (CGH) Sci. Rep. 2019;9:1112. doi: 10.1038/s41598-019-38617-4. PubMed DOI PMC

Jaccoud D., Peng K., Feinstein D., Kilian A. Diversity arrays: A solid state technology for sequence information independent genotyping. Nucleic Acids Res. 2001;29:e25. doi: 10.1093/nar/29.4.e25. PubMed DOI PMC

Kilian A., Wenzl P., Huttner E., Carling J., Xia L., Blois H., Caig V., Heller-Uszynska K., Jaccoud D., Hopper C. Diversity arrays technology: A generic genome profiling technology on open platforms. In: Pompanon F., Bonin A., editors. Data Production and Analysis in Population Genomics. Humana Press; Totowa, NJ, USA: 2012. pp. 67–89. PubMed

Cioffi M.D.B., Bertollo L.A.C. Chromosomal distribution and evolution of repetitive DNAs in fish. In: Garrido-Ramos M.A., editor. Genome Dynamics. Karger; Basel, Switzerland: 2012. pp. 197–221. v. 7. PubMed

Moraes R.L.R., Bertollo L.A.C., Marinho M.M.F., Yano C.F., Hatanaka T., Barby F.F., Troy W.P., Cioffi M.B. Evolutionary relationships and cytotaxonomy considerations in the genus Pyrrhulina (Characiformes, Lebiasinidae) Zebrafish. 2017;14:536–546. doi: 10.1089/zeb.2017.1465. PubMed DOI

Sember A., Bertollo L.A.C., Ráb P., Yano C.F., Hatanaka T., de Oliveira E.A., Cioffi M.D.B. Sex Chromosome Evolution and Genomic Divergence in the Fish Hoplias malabaricus (Characiformes, Erythrinidae) Front. Genet. 2018;9:1–12. doi: 10.3389/fgene.2018.00071. PubMed DOI PMC

Oliveira E.A., Sember A., Bertollo L.A.C., Yano C.F., Ezaz T., Moreira-Filho O., Hatanaka T., Trifonov V., Liehr T., Al-Rikabi A.B.H., et al. Tracking the evolutionary pathway of sex chromosomes among fishes: Characterizing the unique XX/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes) Chromosoma. 2018;127:115–128. doi: 10.1007/s00412-017-0648-3. PubMed DOI

Symonová R., Majtánová Z., Sember A., Staaks G.B.O., Bohlen J., Freyhof J. Genome differentiation in a species pair of coregonine fishes: An extremely rapid speciation driven by stress—Activated retrotransposons mediating extensive ribosomal DNA multiplications. BMC Evol. Biol. 2013;13:42–52. doi: 10.1186/1471-2148-13-42. PubMed DOI PMC

Bertollo L.A.C., Cioffi M.B., Moreira-Filho O. Direct chromosome preparation from Freshwater Teleost Fishes. In: Ozouf-Costaz C., Pisano E., Foresti F., Almeida Toledo L.F., editors. Fish Cytogenetic Techniques (Chondrichthyans and Teleosts) CRC Press; Enfield, CT, USA: 2015. pp. 21–26.

Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press; New York, NY, USA: 2001.

Zwick M.S., Hanson R.E., Mcknight T.D., Islam-Faridi M.H., Stelly D.M., Wing R.A., Price H.J. A rapid procedure for the isolation of C 0 t-1 DNA from plants. Genome. 1997;40:138–142. doi: 10.1139/g97-020. PubMed DOI

Symonová R., Sember A., Majtánová Z., Ráb P. Fish Cytogenet. Tech. Ray-Fin Fishes Chondrichthyans. CCR Press; Boca Raton, FL, USA: 2015. Characterization of fish genomes by GISH and CGH; pp. 118–131.

Akbari M., Wenzl P., Caig V., Carling J., Xia L., Yang S., Uszynski G., Mohler V., Lehmensiek A., Kuchel H. Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor. Appl. Genet. 2006;113:1409–1420. doi: 10.1007/s00122-006-0365-4. PubMed DOI

Wenzl P., Li H., Carling J., Zhou M., Raman H., Paul E., Hearnden P., Maier C., Xia L., Caig V., et al. A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genom. 2006;7:206. doi: 10.1186/1471-2164-7-206. PubMed DOI PMC

Eaton D.A.R., Overcast I. ipyrad v. 0.7.28 2017. [(accessed on 12 March 2019)]; Available online: https://github.com/dereneaton/ipyrad.

Foll M., Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics. 2008;180:977–993. doi: 10.1534/genetics.108.092221. PubMed DOI PMC

Meirmans P.G., van Tienderen P.H. genotype and genodive: Two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes. 2004;4:792–794. doi: 10.1111/j.1471-8286.2004.00770.x. DOI

Gruber B., Georges A., Berry O., Unmack P. dartR: Importing and Analysing SNP and Silicodart Data Generated by Genome-Wide Restriction Fragment Analysis. The R Foundation for Statistical Computing; Vienna, Austria: 2018. R package version 1.0.5.

Raj A., Stephens M., Pritchard J.K. fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets. Genetics. 2014;197:573–589. doi: 10.1534/genetics.114.164350. PubMed DOI PMC

Pritchard J.K., Stephens M., Donnelly P. Inference of Population Structure Using Multilocus Genotype Data. Genetics. 2000;155:945–959. PubMed PMC

Melville J., Melville J., Haines M.L., Boysen K., Hodkinson L., Kilian A., Date K.L.S., Potvin D.A., Parris K.M. Identifying hybridization and admixture using SNPs: Application of the DArTseq platform in phylogeographic research on vertebrates. R. Soc. Open Sci. 2017;4:161061. doi: 10.1098/rsos.161061. PubMed DOI PMC

Guillot G., Santos F., Estoup A. Population Genetics Analysis Using R and Geneland. Technical University of Denmark; Kongens Lyngby, Denmark: 2009.

Perez M.F., Franco F.F., Bombonato J.R., Bonatelli I.A.S., Khan G., Romeiro-Brito M., Fegies A.C., Ribeiro P.M., Silva G.A.R., Moraes E.M. Assessing population structure in the face of isolation by distance: Are we neglecting the problem? Divers. Distrib. 2018;24:1883–1889. doi: 10.1111/ddi.12816. DOI

Earl D.A. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 2012;4:359–361. doi: 10.1007/s12686-011-9548-7. DOI

Jakobsson M., Rosenberg N.A. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23:1801–1806. doi: 10.1093/bioinformatics/btm233. PubMed DOI

Kopelman N.M., Mayzel J., Jakobsson M., Rosenberg N.A., Mayrose I. Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Resour. 2015;15:1179–1191. doi: 10.1111/1755-0998.12387. PubMed DOI PMC

Hudson R.R. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics. 2002;18:337–338. doi: 10.1093/bioinformatics/18.2.337. PubMed DOI

Oliveira E.A. Ph.D. Thesis. Universidade Federal de São Carlos; São Carlos, Brazil: 2019. Evolução Cromossômica na Família Arapaimidae (Teleostei: Osteoglossiformes): Uma Abordagem Populacional e Intercontinental.

Perez M.F., Bonatelli I.A.S., Moraes E.M., Carstens B.C. Model-based analysis supports interglacial refugia over long-dispersal events in the diversification of two South American cactus species. Heredity. 2016;116:550–557. doi: 10.1038/hdy.2016.17. PubMed DOI PMC

Flagel L., Brandvain Y., Schrider D.R. The Unreasonable Effectiveness of Convolutional Neural Networks in Population Genetic Inference. Mol. Biol. Evol. 2019;36:220–238. doi: 10.1093/molbev/msy224. PubMed DOI PMC

Verba J.T., Rabello Neto J.G., Zuanon J., Farias I. Evidence of multiple paternity and cooperative parental care in the so called monogamous silver arowana Osteoglossum bicirrhosum (Osteoglossiformes: Osteoglossidae) Neotrop. Ichthyol. 2014;12:145–151. doi: 10.1590/S1679-62252014000100015. DOI

Thuiller W., Lafourcade B., Engler R., Araújo M.B. BIOMOD—A platform for ensemble forecasting of species distributions. Ecography. 2009;32:369–373. doi: 10.1111/j.1600-0587.2008.05742.x. DOI

Ripley B.D. Pattern Recognition and Neural Networks. Cambridge University Press; Cambridge, UK: 2014. Pattern recognition and neural networks.

Hastie T., Tibshirani R., Buja A. Flexible discriminant analysis by optimal scoring. J. Am. Stat. Assoc. 1994;89:1255–1270. doi: 10.1080/01621459.1994.10476866. DOI

Friedman J. Multivariate adaptive regression splines (with discussion) Ann. Stat. 1991;19:1–67. doi: 10.1214/aos/1176347963. DOI

Busby J.R. BIOCLIM—A bioclimate analysis and prediction system. Plant Prot. Q. 1991;6:8–9.

Breiman L., Friedman J.H., Olshen R.A., Stone C.I. Classification and Regression Trees. Chapman and Hall; Wadsworth, NY, USA: 1984.

McCullagh P., Nelder J.A. Generalized Linear Models. 2nd ed. Chapman and Hall/CRC Press; London, UK: 1989. (Series: Chapman & Hall/CRC Monographs on Statistics and Applied Probability).

Ridgeway G. The State of Boosting. Comput. Sci. Stat. 1999;31:172–181.

Breiman L. Randomforest. Mach. Learn. 2001;45:5–32. doi: 10.1023/A:1010933404324. DOI

Phillips S.J., Anderson R.P., Schapire R.E. Maximum entropy modeling of species geographic distributions. Ecol. Modell. 2006;190:231–259. doi: 10.1016/j.ecolmodel.2005.03.026. DOI

Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G. WorldClim interpolated global terrestrial climate surfaces. Int. J. Climatol. 2004 doi: 10.1002/joc.1276. DOI

Suzuki A., Taki Y., Urushido T. Karyotypes of two species of arowana, Osteoglossum bicirrhosum and O. ferreirai. Jpn. J. Ichthyol. 1982;29:220–222.

Gatti R., Atum Y., Schiaffino L., Jochumsen M., Manresa J.B. Convolutional Neural Networks Improve the Prediction of Hand Movement Speed and Force from Single-trial EEG. bioRxiv. 2019:492660. doi: 10.1101/492660. DOI

da Silva T., Hrbek T., Farias I.P. Microsatellite markers for the silver arowana (Osteoglossum bicirrhosum, Osteoglossidae, Osteoglossiformes) Mol. Ecol. Resour. 2009;9:1019–1022. doi: 10.1111/j.1755-0998.2009.02556.x. PubMed DOI

Cooke G.M., Chao N.L., Beheregaray L.B. Natural selection in the water: Freshwater invasion and adaptation by water colour in the Amazonian pufferfish. J. Evol. Biol. 2012;25:1305–1320. doi: 10.1111/j.1420-9101.2012.02514.x. PubMed DOI

Barby F., Rab P., Lavoue S., Ezaz T., Bertollo L.A.C., Kilian A., Maruyama S.R., Oliveira E.A., Artoni R.F., Santos M.H., et al. From chromosomes to genome: Insights into the evolutionary relationships and biogeography of Old World knifefishes (Notopteridae; Osteoglossiformes) Genes. 2018;9:306. doi: 10.3390/genes9060306. PubMed DOI PMC

Yue G.H., Ong D., Wong C.C., Lim L.C., Orban L. A strain-specific and a sex-associated STS marker for Asian arowana (Scleropages formosus, Osteoglossidae) Aquac. Res. 2003;34:951–957. doi: 10.1046/j.1365-2109.2003.00949.x. DOI

Landguth E.L., Fedy B.C., Oyler-McCance S.J., Garey A.L., Emel S.L., Mumma M., Wagner H.H., Fortin M., Cushman S.A. Effects of sample size, number of markers, and allelic richness on the detection of spatial genetic pattern. Mol. Ecol. Res. 2012;12:276–284. doi: 10.1111/j.1755-0998.2011.03077.x. DOI

Bagley J.C., Sandel M., Travis J., de Lourdes Lozano-Vilano M., Johnson J.B. Paleoclimatic modeling and phylogeography of least killifish, Heterandria formosa: Insights into Pleistocene expansion-contraction dynamics and evolutionary history of North American Coastal Plain freshwater biota. BMC Evol. Biol. 2013;13:223. doi: 10.1186/1471-2148-13-223. PubMed DOI PMC

McMahan C.D., Ginger L., Cage M., David K.T., Chakrabarty P., Johnston M., Matamoros W.A. Pleistocene to holocene expansion of the black-belt cichlid in Central America, Vieja maculicauda (Teleostei: Cichlidae) PLoS ONE. 2017;12:e0178439. doi: 10.1371/journal.pone.0178439. PubMed DOI PMC

Oberdorff T., Jézéquel C., Campero M., Carvajal-Vallejos F., Cornu J.F., Dias M.S., Tedesco P.A. Opinion Paper: How vulnerable are Amazonian freshwater fishes to ongoing climate change? J. App. Icht. 2015;31:4–9. doi: 10.1111/jai.12971. DOI

Rossetti D.F., Valeriano M.M. Evolution of the lowest amazon basin modeled from the integration of geological and SRTM topographic data. Catena. 2007;70:253–265. doi: 10.1016/j.catena.2006.08.009. DOI

Vitorino C.A., Nogueira F., Souza I.L., Araripe J., Venere P.C. Low genetic diversity and structuring of the arapaima (Osteoglossiformes, Arapaimidae) population of the Araguaia-Tocantins basin. Front. Genet. 2017;8:1–10. doi: 10.3389/fgene.2017.00159. PubMed DOI PMC

Torati L.S., Taggart J.B., Varela E.S., Araripe J., Wehner S., Migaud H. Genetic diversity and structure in Arapaima gigas populations from Amazon and Araguaia-Tocantins river basins. BMC Genet. 2019;20:13. doi: 10.1186/s12863-018-0711-y. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...