Population genetics of three threatened catfish species in heterogeneous environments of the Cauca River, Colombia

Natalia Restrepo-Escobar Anny Johanna Yepes-Acevedo Edna Judith Márquez About the authors

ABSTRACT

Neotropical catfishes Ageneiosus pardalis, Pimelodus grosskopfii and Sorubim cuspicaudus are migratory fishes of commercial importance that exhibit decreasing populations due to overfishing and other anthropic interventions. This study used species-specific microsatellite loci to test the hypothesis that threatened fish populations show genetic vulnerability signs and are genetically structured in the middle and lower sections of the Cauca River. The studied species exhibit genetic diversity levels higher than the average values reported for Neotropical Siluriformes; however, they seem to have suffered recent bottlenecks and they present significant endogamy levels that are higher for the critically endangered catfish P. grosskopfii. Furthermore, both Ageneiosus pardalis and S. cuspicaudus are each formed by one genetic group, while Pimelodus grosskopfii comprises two coexisting genetic groups. The information obtained in this study is useful for the decision making in management plans that are appropriate for the sustainability of these three species populations within the proposal for the expansion of the hydroelectric development and other anthropic activities.

Keywords:
Freshwater fish; Genetic diversity; Genetic structure; Microsatellites; Siluriformes

RESUMEN

Los bagres Neotropicales Ageneiosus pardalis, Pimelodus grosskopfii y Sorubim cuspicaudus, son peces migratorios de importancia comercial cuyas poblaciones han disminuido debido a la sobrepesca y otras intervenciones antrópicas. En este trabajo, se utilizaron loci microsatélites especie-específicos para contrastar la hipótesis de que las poblaciones de peces amenazadas muestran señales de vulnerabilidad genética y están genéticamente estructuradas en los sectores medio y bajo del río Cauca. Las especies estudiadas exhiben niveles de diversidad genética superiores a los promedios reportados para Siluriformes Neotropicales; sin embargo, parecen haber sufrido cuellos de botella recientes y presentan niveles significativos de endogamia que son más altos para el bagre en peligro crítico, P. grosskopfii. Además, Ageneiosus pardalis y S. cuspicaudus están conformados cada uno por un solo grupo genético, mientras que Pimelodus grosskopfii comprende dos grupos genéticos que coexisten. La información obtenida en este estudio es útil para la toma de decisiones en planes de manejo que sean adecuados para la sostenibilidad de las poblaciones de estas tres especies de bagre dentro de las propuestas para la expansión de desarrollo hidroeléctrico y otras actividades antrópicas.

Palabras clave:
Diversidad genética; Estructura genética; Microsatélites; Pez dulceacuícola; Siluriformes

INTRODUCTION

The Siluriformes order comprises 38 families, 15 of which are exclusively in Central and South America (Ferraris, 2007Ferraris CJ Jr. Checklist of catfishes, recent and fossil (Osteichthyes, Siluriformes), and catalogue of siluriform primary types. Zootaxa. 2007; 1418(1):1-128. https://doi.org/10.11646/zootaxa.1418.1.1
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; Fricke et al., 2020Fricke R, Eschmeyer WN, Van der Laan R. Eschmeyer’s catalog of fishes: genera, species, references [Internet]. San Francisco: California Academy of Science; 2020. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
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). Six of these families encompass the 86% of the 2347 catfish valid species of Neotropical distribution (Ferraris, 2007; Fricke et al., 2020): Auchenipteridae (125), Callichthyidae (221), Heptapteridae (226), Loricariidae (1000), Pimelodidae (114), and Trichomycteridae (327). These species, known as catfishes, have commercial importance in different regions as nourish source, ornamental fishes or even sport fishing (Usma-Oviedo et al., 2009Usma-Oviedo JS, Valderrama M, Escobar MD, Ajiaco-Martínez RE, Villa-Navarro FA, Castro F et al. Peces dulceacuícolas migratorios en Colombia. In: Naranjo LG, Amaya Espinel JD, editors. Plan nacional de las especies migratorias. Ministro de ambiente, Vivienda y Desarrollo Territorial, WWF Colombia; 2009. p.103-32. Available from: http://d2ouvy59p0dg6k.cloudfront.net/downloads/plan_migratorias_version_web.pdf
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; Nelson et al., 2016Nelson JS, Grande TC, Wilson MVH. Fishes of the world. Hoboken, New Jersey: John Wiley & Sons; 2016. https://doi.org/10.1007/bf00005935
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).

Population genetic studies in Neotropical catfishes are centered in members of commercial interest of Pimelodidae (17) family, and in lower proportion, of Loricariidae (6), Trichomycteridae (1), and Heptateridae (2) families. To the date, evidences for gene flow have been found in species that perform medium and large distance migrations during their lifecycle, such as Brachyplatystoma flavicans (Coronel et al., 2004Coronel JS, Maes GE, Claus S, Van Damme PA, Volckaert FAM. Differential population history in the migratory catfishes Brachyplatystoma flavicans and Pseudoplatystoma fasciatum (Pimelodidae) from the Bolivian Amazon assessed with nuclear and mitochondrial DNA markers. J Fish Biol . 2004; 65(3):859-68. https://doi.org/10.1111/j.0022-1112.2004.00498.x
https://doi.org/10.1111/j.0022-1112.2004...
), Brachyplatystoma rousseauxii (Batista, Alves-Gomes, 2006Batista JDS, Alves-Gomes JA. Phylogeography of Brachyplatystoma rousseauxii (Siluriformes - Pimelodidae) in the Amazon Basin offers preliminary evidence for the first case of “homing” for an Amazonian migratory catfish. Genet Mol Res. 2006; 5(4):723-40. Available from: http://www.funpecrp.com.br/gmr/year2006/vol4-5/pdf/gmr0231.pdf
http://www.funpecrp.com.br/gmr/year2006/...
), Pimelodus maculatus (Almeida et al., 2001Almeida FS, Fungaro MHP, Sodré LMK. RAPD and isoenzyme analysis of genetic variability in three allied species of catfish (Siluriformes: Pimelodidae) from the Tibagi River, Brazil. J Zool. 2001; 253(1):113-20. https://doi.org/10.1017/S0952836901000103
https://doi.org/10.1017/S095283690100010...
, 2003; Ramella et al., 2006Ramella MS, Kroth MA, Meurer S, Nuñer APDO, Zaniboni Filho E, Arisi ACM. Genetic variability in four fish species (Pimelodus maculatus, Prochilodus lineatus, Salminus brasiliensis and Steindachneridion scripta) from Uruguay River Basin. Braz Arch Biol Technol. 2006; 49(4):589-98. https://doi.org/10.1590/S1516-89132006000500008
https://doi.org/10.1590/S1516-8913200600...
; Ribolli et al., 2012Ribolli J, Melo CMR, Zaniboni-Filho E. Genetic characterization of the Neotropical catfish Pimelodus maculatus (Pimelodidae, Siluriformes) in the Upper Uruguay River. Genet Mol Biol . 2012; 35(4):761-69. https://doi.org/10.1590/S1415-47572012005000060
https://doi.org/10.1590/S1415-4757201200...
), Pseudoplatystoma fasciatum (Coronel et al., 2004Coronel JS, Maes GE, Claus S, Van Damme PA, Volckaert FAM. Differential population history in the migratory catfishes Brachyplatystoma flavicans and Pseudoplatystoma fasciatum (Pimelodidae) from the Bolivian Amazon assessed with nuclear and mitochondrial DNA markers. J Fish Biol . 2004; 65(3):859-68. https://doi.org/10.1111/j.0022-1112.2004.00498.x
https://doi.org/10.1111/j.0022-1112.2004...
), Pseudoplatystoma magdalenatium (Gallo, Díaz-Sarmiento, 2003Gallo H, Díaz-Sarmiento J. Variabilidad genética del bagre rayado Pseudoplatystoma fasciatum (Pisces: Pimelodidae) en el río Magdalena (Colombia). Rev Acad Colomb Cien Exactas, Fis Nat. 2003; 27(105):559-606.), Pseudoplatystoma corruscans (Dantas et al., 2013Dantas HL, Santos Neto MA, Oliveira KKC, Severi W, Diniz FM, Coimbra MRM. Genetic diversity of captive and wild threatened catfish Pseudoplatystoma corruscans in the São Francisco River. Rev Fish Sci. 2013; 21(3-4):237-46. https://doi.org/10.1080/10641262.2013.800787
https://doi.org/10.1080/10641262.2013.80...
; Vaini et al., 2016Vaini JO, Crispim BA, Silva DBS, Benites C, Russo MR, Grisolia AB. Genetic variability of pure Pseudoplatystoma corruscans and Pseudoplatystoma reticulatum individuals in the Paraná and Paraguay River basins. Fish Sci. 2016; 82:605-11. https://doi.org/10.1007/s12562-016-0999-3
https://doi.org/10.1007/s12562-016-0999-...
; Prado et al., 2018Prado FD, Fernández-Cebrián R, Foresti F, Oliveira C, Martínez P, Porto-Foresti F. Genetic structure and evidence of anthropogenic effects on wild populations of two Neotropical catfishes: baselines for conservation. J Fish Biol . 2018; 92(1):55-72. https://doi.org/10.1111/jfb.13486
https://doi.org/10.1111/jfb.13486...
), and Pseudoplatystoma reticulatum (Vaini et al., 2016Vaini JO, Crispim BA, Silva DBS, Benites C, Russo MR, Grisolia AB. Genetic variability of pure Pseudoplatystoma corruscans and Pseudoplatystoma reticulatum individuals in the Paraná and Paraguay River basins. Fish Sci. 2016; 82:605-11. https://doi.org/10.1007/s12562-016-0999-3
https://doi.org/10.1007/s12562-016-0999-...
; Prado et al., 2018Prado FD, Fernández-Cebrián R, Foresti F, Oliveira C, Martínez P, Porto-Foresti F. Genetic structure and evidence of anthropogenic effects on wild populations of two Neotropical catfishes: baselines for conservation. J Fish Biol . 2018; 92(1):55-72. https://doi.org/10.1111/jfb.13486
https://doi.org/10.1111/jfb.13486...
).

Nevertheless, genetic structure of populations of some species has been found and it seems to be explained by various types of behaviors: (1) sedentarism and short-distance migration range in Steindachneridion parahybae (Fonseca et al., 2017Fonseca FS, Domingues RR, Hallerman EM, Hilsdorf AWS. Genetic diversity of an imperiled Neotropical catfish and recommendations for its restoration. Front Genet. 2017; 8:196. https://doi.org/10.3389/fgene.2017.00196
https://doi.org/10.3389/fgene.2017.00196...
), Trichogenes longipinnis (Zamudio et al., 2009Zamudio KR, Robertson JM, Chan LM, Sazima I. Population structure in the catfish Trichogenes longipinnis: Drift offset by asymmetrical migration in a tiny geographic range. Biol J Linn Soc. 2009; 97(2):259-74. https://doi.org/10.1111/j.1095-8312.2009.01209.x
https://doi.org/10.1111/j.1095-8312.2009...
), Iheringichthys labrosus, and Pimelodus cf. absconditus (Almeida et al., 2001Almeida FS, Fungaro MHP, Sodré LMK. RAPD and isoenzyme analysis of genetic variability in three allied species of catfish (Siluriformes: Pimelodidae) from the Tibagi River, Brazil. J Zool. 2001; 253(1):113-20. https://doi.org/10.1017/S0952836901000103
https://doi.org/10.1017/S095283690100010...
); (2) fidelity to breeding or spawning sites (homing) in P. corruscans (Pereira et al., 2009Pereira LHG, Foresti F, Oliveira C. Genetic structure of the migratory catfish Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) suggests homing behaviour. Ecol Freshw Fish . 2009; 18(2):215-25. https://doi.org/10.1111/j.1600-0633.2008.00338.x
https://doi.org/10.1111/j.1600-0633.2008...
), P. reticulatum (Abreu et al., 2009Abreu MM, Pereira LHG, Vila VB, Foresti F, Oliveira C. Genetic variability of two populations of Pseudoplatystoma reticulatum from the Upper Paraguay River Basin. Genet Mol Biol. 2009; 32(4):868-73. https://doi.org/10.1590/S1415-47572009005000075
https://doi.org/10.1590/S1415-4757200900...
), and Rhamdia quelen (Ríos et al., 2019Ríos N, Bouza C, García G. Past hybridisation and introgression erased traces of mitochondrial lineages evolution in the Neotropical silver catfish Rhamdia quelen (Siluriformes: Heptapteridae). Hydrobiologia . 2019; 830:161-77. https://doi.org/10.1007/s10750-018-3861-z
https://doi.org/10.1007/s10750-018-3861-...
), and (3) presence of natural or artificial geographical barriers in P. maculatus in Paranapanema River (Almeida et al., 2003Almeida FS, Sodré LMK, Contel EPB. Population structure analysis of Pimelodus maculatus (Pisces, Siluriformes) from the Tietê and Paranapanema Rivers (Brazil). Genet Mol Biol . 2003; 26(3):301-05. https://doi.org/10.1590/S1415-47572003000300014
https://doi.org/10.1590/S1415-4757200300...
), P. corruscans in Paraná River (Sekine et al., 2002Sekine ES, Prioli AJ, Prioli SMAP, Júlio Júnior HF. Genetic differentiation among populations of Pseudoplatystoma corruscans (Agassiz, 1829) (Osteichthyes, Pimelodidae) isolated by the Guaíra Falls in the Paraná River. Acta Sci. 2002; 24(2):507-12. Available from: http://repositorio.uem.br:8080/jspui/bitstream/1/5222/1/375.pdf
http://repositorio.uem.br:8080/jspui/bit...
), and between Paraná and São Francisco rivers (Carvalho et al., 2012Carvalho DC, Oliveira DAA, Beheregaray LB, Torres RA. Hidden genetic diversity and distinct evolutionarily significant units in an commercially important Neotropical apex predator, the catfish Pseudoplatystoma corruscans. Conserv Genet. 2012; 13:1671-75. https://doi.org/10.1007/s10592-012-0402-6
https://doi.org/10.1007/s10592-012-0402-...
), and P. corruscans and P. reticulatum in Paraná and Paraguay rivers (Prado et al., 2018Prado FD, Fernández-Cebrián R, Foresti F, Oliveira C, Martínez P, Porto-Foresti F. Genetic structure and evidence of anthropogenic effects on wild populations of two Neotropical catfishes: baselines for conservation. J Fish Biol . 2018; 92(1):55-72. https://doi.org/10.1111/jfb.13486
https://doi.org/10.1111/jfb.13486...
).

Contrary to the majority of population genetics studies in Amazonas and Paraná basins, very few have been performed in Colombian basins, most of which are found in grey literature (see Mancera-Rodríguez et al., 2013Mancera-Rodríguez NJ, Márquez EJ, Hurtado-Alarcón JC. Uso de citogenética y técnicas moleculares en estudios de diversidad genética en peces colombianos. In: López-H A, editor. Biología Molecular aplicada a la producción animal y la conservación de especies silvestres., Medellín: Universidad Nacional de Colombia; 2013. p.237-312.; Márquez et al., 2020Márquez E, Restrepo-Escobar N, Yepes-Acevedo AJ, Narváez JC. Diversidad y estructura genética de los peces de la cuenca del Magdalena, Colombia. In: Jiménez-Segura LF, Lasso CA, editors. XIX. Peces de la cuenca del río Magdalena, Colombia: diversidad, conservación y uso sostenible. Serie Editorial Recursos Hidrobiológicos y Pesqueros Continentales de Colombia. Bogotá, (D.C): Instituto de Investigación de Recursos Biológicos Alexander von Humboldt; 2020. p.115-57.). For the remaining freshwater catfishes in northwestern South America, there is still unawareness of genetic diversity, demography and population structure which limits the implementation of effective rules for their management and protection.

The latter is important since populations of these species have been affected by overfishing and other indirect effects of anthropogenic activities like mining, dam construction, gravel sand extraction, basins contamination and continuous water extraction for agricultural and livestock purposes, which have led to the decay and decrease of the populations of said species in all Colombian basins (Galvis, Mojica, 2007Galvis G, Mojica JI. The Magdalena River fresh water fishes and fisheries. Aquat Ecosyst Health Manag. 2007; 10(2):127-39. https://doi.org/10.1080/14634980701357640
https://doi.org/10.1080/1463498070135764...
; Usma-Oviedo et al., 2009Usma-Oviedo JS, Valderrama M, Escobar MD, Ajiaco-Martínez RE, Villa-Navarro FA, Castro F et al. Peces dulceacuícolas migratorios en Colombia. In: Naranjo LG, Amaya Espinel JD, editors. Plan nacional de las especies migratorias. Ministro de ambiente, Vivienda y Desarrollo Territorial, WWF Colombia; 2009. p.103-32. Available from: http://d2ouvy59p0dg6k.cloudfront.net/downloads/plan_migratorias_version_web.pdf
http://d2ouvy59p0dg6k.cloudfront.net/dow...
; Barletta et al., 2010Barletta M, Jaureguizar AJ, Baigun C, Fontoura NF, Agostinho AA, Almeida-Val VMF et al. Fish and aquatic habitat conservation in South America: A continental overview with emphasis on Neotropical systems. J Fish Biol. 2010; 76(9):2118-76. https://doi.org/10.1111/j.1095-8649.2010.02684.x
https://doi.org/10.1111/j.1095-8649.2010...
; Jiménez-Segura et al., 2016Jiménez-Segura LF, Galvis-Vergara G, Cala-Cala P, García-Alzate CA, López-Casas S, Ríos-Pulgarín MI et al. Freshwater fish faunas, habitats and conservation challenges in the Caribbean river basins of north-western South America. J Fish Biol . 2016; 89(1):65-101. https://doi.org/10.1111/jfb.13018
https://doi.org/10.1111/jfb.13018...
).

To contrast the hypothesis that threatened fish populations show genetic vulnerability signs in Cauca River sections exposed to anthropic activities, three catfish species were chosen, with differences in their standard length, migration range and reproductive strategies. Ageneiosus pardalis Lütken, 1874, is a medium size species (standard length between 12.83-42.98 cm; Ribeiro et al., 2017Ribeiro FRV, Rapp Py-Daniel LH, Walsh SJ. Taxonomic revision of the South American catfish genus Ageneiosus (Siluriformes: Auchenipteridae) with the description of four new species. J Fish Biol . 2017; 90(4):1388-478. https://doi.org/10.1111/jfb.13246
https://doi.org/10.1111/jfb.13246...
), with short-distance migration range (< 100 km), marked sexual dimorphism (Dahl, 1971Dahl G. Los peces del Norte de Colombia. Bogotá (D.C.): Ministerio de Agricultura, Instituto de desarrollo de los recursos naturales renovables (INDRENA); 1971.; Mojica et al., 2012aMojica JI, Castellanos C, Álvarez -León R, Villa-Navarro FA. Ageneiosus pardalis Lütken 1874. In: Mojica JI, Usma-Oviedo JS, Álvarez-León R, Lasso CA, editors. Libro rojo peces dulceacuícolas de Colombia 2012. Bogotá (D.C.): Investigación de Recursos Biológicos Alexander von Humboldt, Instituto de Ciencias Naturales de la Universidad Nacional de Colombia, WWF Colombia y Universidad de Manizales; 2012a. p.71-73.), elaborated courtship and copulation (Galvis et al., 1997Galvis G, Mojica JI, Camargo M. Peces del Catatumbo. Bogotá (D.C.): ECOPETROL; 1997.) and distribution from south Panamá to north Venezuela; Pimelodus grosskopfii Steindachner, 1879, is a small size species (standard length between 10.17-32.12 cm; Villa-Navarro et al., 2017Villa-Navarro FA, Acero P A, Cala-Cala P. Taxonmic review of Trans-Andean species of Pimelodus (Siluriformes: Pimelodidae), with the description of two new species. Zootaxa. 2017; 4299(3):337-60. https://doi.org/10.11646/zootaxa.4299.3.2
https://doi.org/10.11646/zootaxa.4299.3....
), with medium migration range (100-500 km), external reproduction, endemic of the Magdalena-Cauca Colombian basin (Mojica et al., 2006Mojica JI, Galvis G, Sánchez-Duarte P, Castellanos C, Villa-Navarro FA. Peces del valle medio del río Magdalena, Colombia. Biota Colomb. 2006; 7(1):23-37.; Ortega-Lara et al., 2006Ortega-Lara A, Usma JS, Bonilla PA, Santos NL. Peces de la cuenca alta del río Cauca, Colombia. Biota Colomb . 2006; 7(1):39-54.), and Sorubim cuspicaudusLittmann, Burr & Nass, 2000Littmann MW, Burr BM, Nass P. Sorubim cuspicaudus, a new long-whiskered catfish from northwestern South America (Siluriformes: Pimelodidae). Proc Biol Soc Wash. 2000; 113(4):900-17., a medium size species (can reach lengths greater than 80 cm; Littmann et al., 2000Littmann MW, Burr BM, Nass P. Sorubim cuspicaudus, a new long-whiskered catfish from northwestern South America (Siluriformes: Pimelodidae). Proc Biol Soc Wash. 2000; 113(4):900-17.), with medium-distance migration range (100-500 km), external reproduction and distribution in the rivers Catatumbo (Ortega-Lara et al., 2012Ortega-Lara A, Lasso-Alcalá OM, Lasso CA, Pasquier GA, Bogotá-Gregory JD. Peces de la subcuenca del río Catatumbo, cuenca del Lago de Maracaibo, Colombia y Venezuela. Biota Colomb . 2012; 13(1):71-99. Available from: http://revistas.humboldt.org.co/index.php/biota/article/view/258
http://revistas.humboldt.org.co/index.ph...
), Magdalena (Mojica et al., 2006Mojica JI, Galvis G, Sánchez-Duarte P, Castellanos C, Villa-Navarro FA. Peces del valle medio del río Magdalena, Colombia. Biota Colomb. 2006; 7(1):23-37.; Villa-Navarro et al., 2006Villa-Navarro FA, Zúñiga-Upegui PT, Castro-Roa D, García-Melo JE, García-Melo LJ, Herrada-Yara ME. Peces del alto Magdalena, cuenca del río Magdalena, Colombia. Biota Colomb . 2006; 7(1):3-22.), Sinú and Cauca (Littmann et al., 2000Littmann MW, Burr BM, Nass P. Sorubim cuspicaudus, a new long-whiskered catfish from northwestern South America (Siluriformes: Pimelodidae). Proc Biol Soc Wash. 2000; 113(4):900-17.) in northwestern South America.

The appointed species are a good model for population genetics analysis since they are exposed to anthropic interventions such as loss of habitats, deforestation, river-course fragmentation, introduction of exotic fish species, contamination and overfishing (Barletta et al., 2010Barletta M, Jaureguizar AJ, Baigun C, Fontoura NF, Agostinho AA, Almeida-Val VMF et al. Fish and aquatic habitat conservation in South America: A continental overview with emphasis on Neotropical systems. J Fish Biol. 2010; 76(9):2118-76. https://doi.org/10.1111/j.1095-8649.2010.02684.x
https://doi.org/10.1111/j.1095-8649.2010...
; FAO, 2015FAO. Colombia: pesca en cifras/2014. Bogotá (D.C.): Ministerio de Agricultura y desarrollo rural, Organización de las naciones unidas para la alimentación y la agricultura (FAO); 2015. Available from: https://www.aunap.gov.co/wp-content/uploads/2016/05/Pesca_en_cifras.pdf
https://www.aunap.gov.co/wp-content/uplo...
; Jiménez-Segura et al., 2016Jiménez-Segura LF, Galvis-Vergara G, Cala-Cala P, García-Alzate CA, López-Casas S, Ríos-Pulgarín MI et al. Freshwater fish faunas, habitats and conservation challenges in the Caribbean river basins of north-western South America. J Fish Biol . 2016; 89(1):65-101. https://doi.org/10.1111/jfb.13018
https://doi.org/10.1111/jfb.13018...
; AUNAP, 2020Autoridad Nacional de Acuacultura y Pesca (AUNAP). SEPEC-Servicio Estadístico Pesquero Colombiano [Internet]. Bogotá; 2020. Available from: http://sepec.aunap.gov.co/
http://sepec.aunap.gov.co/...
). The decreasing population density of the three species led to their classification as vulnerable in the Colombian red list of freshwater fishes (Mojica et al., 2012bMojica JI, Usma-Oviedo JS, Álvarez-León R, Lasso CA. Libro Rojo de peces dulceacuicolas de Colombia 2012. Bogotá (D.C.): Instituto de Investigación de los Recursos Biológicos Alexander von Humboldt, Instituto de Ciencias Naturales de la Universidad Nacional de Colombia, WWF Colombia, Universidad de Manizales; 2012b. https://doi.org/10.1007/s13398-014-0173-7.2
https://doi.org/10.1007/s13398-014-0173-...
). Additionally, due to this decline in populations, P. grosskopfii was included as a critically endangered threatened species in the red list of threatened species of the International Union for Conservation of Nature - IUCN (Villa-Navarro et al., 2016Villa-Navarro FA, Usma-Oviedo JS, Mesa-Salazar L, Sanchez-Duarte P. Pimelodus grosskopfii. The IUCN red list of threatened species 2016:eT49829828A61473588 [Internet]. http://dx.doi.org/10.2305/IUCN.UK.2016-1.RLTS.T49829828A61473588.en
http://dx.doi.org/10.2305/IUCN.UK.2016-1...
). Thus, the a priori expectation was that the species showed high values of inbreeding and recent bottlenecks, as they are exposed to different anthropic interventions that might affect the density of their populations.

Moreover, the studied area comprises the middle and lower sections of the Cauca River, which includes near 500 km of the main channel of the river, 110 km of torrents and 40.000 ha of swamps. This area also includes the Cauca River canyon, the steepest margin of the Antioqueño Plateau in the northern portion of the Central Cordillera (Restrepo-Moreno et al., 2009Restrepo-Moreno SA, Foster DA, Stockli DF, Parra-Sánchez LN. Long-term erosion and exhumation of the Altiplano Antioqueño, Northern Andes (Colombia) from apatite (U-Th)/He thermochronology. Earth Planet Sci Lett. 2009; 278(1-2):1-12. https://doi.org/10.1016/j.epsl.2008.09.037
https://doi.org/10.1016/j.epsl.2008.09.0...
), which has been considered a geographic barrier for many fish species (Dahl, 1971Dahl G. Los peces del Norte de Colombia. Bogotá (D.C.): Ministerio de Agricultura, Instituto de desarrollo de los recursos naturales renovables (INDRENA); 1971.). Additionally, this area presents differences in habitats, water speeds, temperatures and it constitutes the influence zone of the Ituango hydroelectric project. In this context, this study also tested the hypothesis that populations of these species, collected before the beginning of the construction of the hydroelectric, were genetically structured. The a priori expectation was that the environmental heterogeneity of the zone caused genetic structuration. The answer to these queries generates information of interest to propose rules of management and conservation, suitable for the preservation of natural populations of these fish species.

MATERIAL AND METHODS

A total of 492 preserved in alcohol muscle tissues of A. pardalis (193), P. grosskopfii (170), and S. cuspicaudus (129) were analyzed. Said tissues were provided by Integral S.A through the scientific cooperation agreement CT-2013-002443, framed in the environmental license of Ministerio de Ambiente, Vivienda y Desarrollo Territorial # 0155 of January 30th, 2009. Samples were collected between 2011-2014 in the middle (sections S1-S4) and lower (sections S5-S8) sections of the Cauca River, located upstream (S1) and downstream (S2-S8) of the construction zone of Ituango hydroelectric project (Fig. 1; Tab. 1). The middle section of the Cauca River encompasses the Cauca River canyon, characterized by a steep topography with the presence of rapid zones (S1-S3) followed by a vast alluvial plain surrounded by mountains, with swamp ecosystems connected with the main river channel (S4). The section S5 includes the mouth of the Nechí River, a hydrologically monomodal river prone to flooding and scouring, and the remaining lower section (S6-S8) shows soft topography with flat and wavy surfaces wherein several swamps connected to rivers through canals are formed, conforming complex swampy systems (Mejía-Rivera et al., 2007Mejía-Rivera O, Betancur-Vargas T, Londoño-Ciro L. Aplicación de técnicas geoestadisticas en la hidrogeología del bajo Cauca antioqueño. Dyna. 2007; 74(152):137-49. Available from: http://www.scielo.org.co/pdf/dyna/v74n152/a12v74n152.pdf
http://www.scielo.org.co/pdf/dyna/v74n15...
; Betancur-Vargas et al., 2009Betancur T, Mejía O, Palacio C. Conceptual hydrogeology model to Bajo Cauca antioqueño: a tropical aquifer system. Rev Fac Ing Univ Antioquia. 2009; 48(1):107-18.).

FIGURE 1
| Location of sampling sites of Pimelodus grosskopfii, Sorubim cuspicaudus, and Ageneiosus pardalis in the middle and lower sections of the Cauca River.

DNA extraction was performed with the commercial kit PureLink® Genomic DNA (ThermoFisher Scientific), following the instructions of the manufacturer. PCR conditions previously described by Landínez-García, Marquez (2016Landínez-García RM, Márquez EJ. Development and characterization of 24 polymorphic microsatellite loci for the freshwater fish Ichthyoelephas longirostris (Characiformes: Prochilodontidae). PeerJ. 2016; 4:e2419. https://doi.org/10.7717/peerj.2419
https://doi.org/10.7717/peerj.2419...
, 2018) were employed to amplify between 13 and 20 microsatellite loci for A. pardalis (Apar03, Apar04, Apar05, Apar11, Apar12, Apar14, Apar18, Apar19, Apar20, Apar21, Apar22, Apar23, Apar25, Apar27, Apar28, Apar30, Apar32, Apar34, Apar35, Apar36); P. grosskopfii (Pgrk01, Pgrk02, Pgrk03, Pgrk08, Pgrk10, Pgrk14, Pgrk15, Pgrk19, Pgrk24, Pgrk27, Pgrk28, Pgrk31, Pgrk40), and S. cuspicaudus (Scus03, Scus10, Scus12, Scus15, Scus16, Scus17, Scus18, Scus20, Scus21, Scus22, Scus23, Scus24, Scus25, Scus28, Scus32, Scus35, Scus39, Scus40, Scus41; Restrepo-Escobar, Marquez, 2020Restrepo-Escobar N, Márquez EJ. Microsatellite loci development for three catfish species from northwestern South America. Neotrop Ichthyol. 2020; 18(1):e190079. https://doi.org/10.1590/1982-0224-2019-0079
https://doi.org/10.1590/1982-0224-2019-0...
). PCR products were separated in an automatic sequencer ABI 3130 (Applied Biosystems, USA) using GeneScan-500 LIZ dye size standard (Applied Biosystems, USA) as internal marker and the allelic fragments were denoted according to their molecular size and scored using GeneMapper (Applied Biosystems, USA). Before the statistical analysis, the Micro-Checker v2.2.1 software (Van Oosterhout et al., 2004Oosterhout C Van, Hutchinson WF, Wills DPM, Shipley P. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004; 4(3):535-38. https://doi.org/10.1111/j.1471-8286.2004.00684.x
https://doi.org/10.1111/j.1471-8286.2004...
) was used to detect possible genotyping errors.

For samples of each studied section and genetic group, it was determined the genetic diversity calculating the expected and observed heterozygosities and the average number of alleles per locus with GenAlex v6.502 software (Peakall, Smouse, 2012Peakall R, Smouse PE. GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics. 2012; 28(19):2537-39. https://doi.org/10.1093/bioinformatics/bts460
https://doi.org/10.1093/bioinformatics/b...
). Additionally, the Arlequin v3.5.2.2 software (Excoffier, Lischer, 2010Excoffier L, Lischer HEL. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010; 10(3):564-67. https://doi.org/10.1111/j.1755-0998.2010.02847.x
https://doi.org/10.1111/j.1755-0998.2010...
) was employed to test departures of the Hardy-Weinberg equilibrium, linkage equilibrium and calculate the inbreeding coefficient (FIS) by population. In multiple comparisons, the statistical significance was adjusted by the Bonferroni sequential correction (Rice, 1989Rice WR. Analyzing Tables of Statistical Tests. Evolution (N Y). 1989; 43(1):223-25. https://doi.org/10.2307/2409177
https://doi.org/10.2307/2409177...
). Finally, two tests were used to determine whether the populations of these species have suffered a recent genetic bottleneck, the one-tailed test of Wilcoxon (Luikart, Cornuet, 1998Luikart G, Cornuet J. Empirical evaluation of a test for identifying allele recently data bottlenecked populations from frequency. Conserv Biol. 1998; 12(1):228-37. https://doi.org/10.1111/j.1523-1739.1998.96388.x
https://doi.org/10.1111/j.1523-1739.1998...
), and M ratio of Garza, Williamson (2001Garza JC, Williamson EG. Detection of reduction in population size using data from microsatellite loci. Mol Ecol . 2001; 10(2):305-18. https://doi.org/10.1046/j.1365-294x.2001.01190.x
https://doi.org/10.1046/j.1365-294x.2001...
) calculated respectively in Bottleneck v1.2.02 software (Piry et al., 1999Piry S, Luikart G, Cornuet JM. BOTTLENECK: a computer program for detecting recent reduction in the effective population size using allele frequency data. J Hered. 1999; 90(4):502-03. https://doi.org/10.1093/jhered/90.4.502
https://doi.org/10.1093/jhered/90.4.502...
) and the Arlequin v3.5.2.2. program (Excoffier, Lischer, 2010).

To determine the number of possible genetic groups for A. pardalis, P. grosskopfii, and S. cuspicaudus in the middle and lower basins of the Cauca River, it was used different complementary approaches. The Bayesian clustering method with STRUCTURE v2.3.4 software (Pritchard et al., 2000Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000; 155(2):945-59. Available from: https://www.genetics.org/content/genetics/155/2/945.full.pdf
https://www.genetics.org/content/genetic...
) used the following conditions: 100000 MCM, 10000 burn-in, admixture model, correlated allele frequency, and LOCPRIOR option. Simulations were repeated 20 times per each number of evaluated probable populations: 1-6 for A. pardalis, 1-8 for S. cuspicaudus, and 1-9 for P. grosskopfii. The most probable number of population was calculated using the ΔK method (Evanno et al., 2005Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005; 14(8):2611-20. https://doi.org/10.1111/j.1365-294X.2005.02553.x
https://doi.org/10.1111/j.1365-294X.2005...
) and the estimators MedMedK, MedMeaK, MaxMedK, and MaxMeaK (Puechmaille, 2016Puechmaille SJ. 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. 2016; 16(3):608-27. https://doi.org/10.1111/1755-0998.12512
https://doi.org/10.1111/1755-0998.12512...
) with the web-based software STRUCTURESELECTOR (Li, Liu, 2018Li YL, Liu JX. StructureSelector: a web-based software to select and visualize the optimal number of clusters using multiple methods. Mol Ecol Resour. 2018; 18(1):176-77. https://doi.org/10.1111/1755-0998.12719
https://doi.org/10.1111/1755-0998.12719...
). The STRUCTURE results were summarized using the integrated software CLUMPAK (Kopelman et al., 2015Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 2015; 15(5):1179-91. https://doi.org/10.1111/1755-0998.12387
https://doi.org/10.1111/1755-0998.12387...
) to generate a graphical representation of the results. Wherein STRUCTURE detected different genetic groups, the allocation of each individual to each group was determined by the coancestry coefficient from the Q-matrix generated by CLUMPAK (Kopelman et al., 2015Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 2015; 15(5):1179-91. https://doi.org/10.1111/1755-0998.12387
https://doi.org/10.1111/1755-0998.12387...
) from the 20 simulations produced by STRUCTURE. Moreover, the genetic differentiation of each of the species among sectors of the Cauca River was calculated with the Analysis of Molecular Variance AMOVA and the standardized estimators F’ST (Meirmans, 2006Meirmans PG. Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution (N Y). 2006; 60(11):2399-402. https://doi.org/10.1111/j.0014-3820.2006.tb01874.x
https://doi.org/10.1111/j.0014-3820.2006...
) and Jost’s Dest (Meirmans, Hedrick, 2011Meirmans PG, Hedrick PW. Assessing population structure: FST and related measures. Mol Ecol Resour. 2011; 11(1):5-18. https://doi.org/10.1111/j.1755-0998.2010.02927.x
https://doi.org/10.1111/j.1755-0998.2010...
) using the GenAlex v6.502 software (Peakall, Smouse, 2012Peakall R, Smouse PE. GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics. 2012; 28(19):2537-39. https://doi.org/10.1093/bioinformatics/bts460
https://doi.org/10.1093/bioinformatics/b...
), and a Discriminant Analysis of Principal Components (DAPC) was performed using the package adegenet (Jombart, 2008Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008; 24(11):1403-05. https://doi.org/10.1093/bioinformatics/btn129
https://doi.org/10.1093/bioinformatics/b...
) for R v3.4.0 program (R Development Core Team, 2017R Development Core Team. R: A Language and Environment for Statistical Computing; 2017. Available from: https://www.R-project.org/
https://www.R-project.org/...
).

RESULTS

The sampling performed by Integral S.A. between 2011-2014 revealed that A. pardalis, P. grosskopfii, and S. cuspicaudus were differentially distributed in the middle and lower sections of the Cauca River. Namely, and despite having the same migration range, P. grosskopfii was found in all sampled sites, including upstream of the Cauca River canyon, whereas S. cuspicaudus was found in the downstream area of Cauca River canyon and the construction zone of the dam (S3-S8). In contrast, short-distance migration range A. pardalis was only captured in the lower basin of the river (S5-S8; Tab. 1).

TABLE 1
| Number of individuals of Pimelodus grosskopfii, Sorubim cuspicaudus, and Ageneiosus pardalis analyzed in the middle and lower basin of the Cauca River. S1-S4: Middle section of the Cauca River, S1 and S2-S4 are located upstream and downstream of the construction zone of the dam, respectively. S5-S8: Lower section of the Cauca River.

Genetic diversity and population demographics. Pimelodus grosskopfii showed similar or nearly similar genetic diversity values in all evaluated sections (Na=10.308-13.308; He=0.849-0.866; Ho=0.607-0.682) and in the genetic groups proposed by the genetic structure analysis described below (Na=12.846-16.615; He=0.858-0.866; Ho=0.614-0.664; Tab. 2), further to statistical significance in heterozygosity deficit and inbreeding coefficients (FIS=0.108-0.218; P<0.000; Tab. 2).

TABLE 2
| Genetic diversity, M-ratio estimator and bottleneck for populations and genetic groups of Pimelodus grosskopfii, Sorubim cuspicaudus, and Ageneiosus pardalis in the middle and lower sections of the Cauca River. N: Number of analyzed individuals, Na: Average number of alleles/locus, Ho: Observed heterozygosity, He: Expected heterozygosity, P: statistical significance of Hardy-Weinberg equilibrium; FIS: inbreeding coefficient, M-ratio: M estimator of Garza, Williamson (2001Garza JC, Williamson EG. Detection of reduction in population size using data from microsatellite loci. Mol Ecol . 2001; 10(2):305-18. https://doi.org/10.1046/j.1365-294x.2001.01190.x
https://doi.org/10.1046/j.1365-294x.2001...
), IAM: infinite alleles model, TPM: two phase model, SMM: stepwise model. Values in bold denote statistical significance.

Likewise, S. cuspicaudus exhibited similar values of genetic diversity within the analyzed sections (Na=8.105-9.368; He=0.771-0.785; Ho=0.745-0.795; Tab. 2); however, in this case the genotypic frequencies behaved according to Hardy-Weinberg equilibrium except from S5 wherein the heterozygosity deficit was significant. Moreover, the inbreeding coefficient was significant in S5 (FIS=0.045; P=0.026) and S8 (FIS=0.058; P=0.032; Tab. 2).

In accordance with the other two species, A. pardalis showed similar genetic diversity values (Na=10.850-12.550; He=0.832-0.839; Ho=0.791-0.822; Tab. 2); statistical significance in heterozygosity deficits and coefficients of inbreeding in all the evaluated samples (FIS=0.026-0.086; P<0.007) although in lesser magnitude than in P. grosskopfii (Tab. 2).

The analysis for detecting bottleneck showed significant values for all the species in the evaluated sections under the IAM, while no significance was found under the SMM and the TPM showed significance in all or almost all of the evaluated sections in A. pardalis, P. grosskopfii (except S8), and S. cuspicaudus (except S4, S6, and S7/8). Additionally, the three species showed values of the M ratio of Garza, Williamson, (2001Garza JC, Williamson EG. Detection of reduction in population size using data from microsatellite loci. Mol Ecol . 2001; 10(2):305-18. https://doi.org/10.1046/j.1365-294x.2001.01190.x
https://doi.org/10.1046/j.1365-294x.2001...
) lower than 0.680 (P. grosskopfii: 0.197-0.227; S. cuspicaudus: 0.229-0.258; A. pardalis: 0.242-0.245; Tab. 2), which has been proposed as limit value for inferring that the population has suffered a recent decline in population (Garza, Williamson, 2001).

Genetic structure analysis. In the distribution range of the evaluated samples in middle and lower sections of the Cauca River, the Bayesian analysis of STRUCTURE showed the homogeneous distribution of two coexisting genetic groups in P. grosskopfii (K=2; MedMedK=2; MedMeanK=2; MaxMedK=2; MaxMeanK=2; Fig. 2A), one genetic group in S. cuspicaudus, wherein each individual exhibits a similar genetic admixture of two biological groups (K=2; MedMedK=1; MedMeanK=1; MaxMedK=2; MaxMeanK=2; Fig. 2B), and one main genetic group with some genetic admixture in A. pardalis (ΔK=2; MedMedK=1; MedMeanK=1; MaxMedK=1; MaxMeanK=1; Fig. 2C).

The homogeneous distribution of the genetic groups of P. grosskopfii (FST: 0.004, P: 0.075), S. cuspicaudus (FST: 0.003, P: 0.084) and A. pardalis (FST: 0.001, P: 0.066) in the middle and lower sections of the Cauca River was corroborated by AMOVA, the pairwise comparisons with standardized estimators F´ST and Dest (Tab. 3), and DAPC (Figs. 2D-F).

FIGURE 2
| Population structure suggested by STRUCTURE (A-C) and the Discriminant Analysis of the Principal Components (D-F) for Pimelodus grosskopfii (A, D), Sorubim cuspicaudus (B, E), and Ageneiosus pardalis (C, F).

TABLE 3
| Statistical values F’ST and Dest by pairs of the Pimelodus grosskopfii, Sorubim cuspicaudus, and Ageneiosus pardalis populations in middle and lower sections of the Cauca River.

DISCUSSION

This study employed species-specific microsatellite loci to acknowledge the level of genetic diversity, demographic status and genetic structure degree of three species of Colombian endemic Neotropical catfishes that coexist in the middle and lower sections of the Cauca River basin. The a priori expectation was that the species showed high values of inbreeding and recent bottlenecks as they are subject of different anthropic interventions that might affect the density of their populations. Furthermore, it was expected a population genetic structure concordant with some heterogeneous features of the basin.

Genetic diversity and population demography. The three studied species showed higher levels of genetic diversity than the average values reported for Neotropical catfishes (Na=7.470, He=0.609; revision of Hilsdorf, Hallerman, 2017Hilsdorf AWS, Hallerman EM. Genetic resources of Neotropical fishes. New York: Springer International Publishing; 2017. https://doi.org/10.1007/978-3-319-55838-7
https://doi.org/10.1007/978-3-319-55838-...
) although S. cuspicaudus showed lower diversity (Na=8.547, He=0.779) than A. pardalis (Na=11.783, He=0.835) and P. grosskopfii (Na=11.143, He=0.847).

The average expected heterozygosity values in the three species were higher than in other Neotropical catfishes such as T. longipinnis (He=0.393, Zamudio et al., 2009Zamudio KR, Robertson JM, Chan LM, Sazima I. Population structure in the catfish Trichogenes longipinnis: Drift offset by asymmetrical migration in a tiny geographic range. Biol J Linn Soc. 2009; 97(2):259-74. https://doi.org/10.1111/j.1095-8312.2009.01209.x
https://doi.org/10.1111/j.1095-8312.2009...
), S. parahybae (He=0.470, Fonseca et al., 2017Fonseca FS, Domingues RR, Hallerman EM, Hilsdorf AWS. Genetic diversity of an imperiled Neotropical catfish and recommendations for its restoration. Front Genet. 2017; 8:196. https://doi.org/10.3389/fgene.2017.00196
https://doi.org/10.3389/fgene.2017.00196...
), P. reticulatum (He=0.498-0.751, Abreu et al., 2009Abreu MM, Pereira LHG, Vila VB, Foresti F, Oliveira C. Genetic variability of two populations of Pseudoplatystoma reticulatum from the Upper Paraguay River Basin. Genet Mol Biol. 2009; 32(4):868-73. https://doi.org/10.1590/S1415-47572009005000075
https://doi.org/10.1590/S1415-4757200900...
; Vaini et al., 2016Vaini JO, Crispim BA, Silva DBS, Benites C, Russo MR, Grisolia AB. Genetic variability of pure Pseudoplatystoma corruscans and Pseudoplatystoma reticulatum individuals in the Paraná and Paraguay River basins. Fish Sci. 2016; 82:605-11. https://doi.org/10.1007/s12562-016-0999-3
https://doi.org/10.1007/s12562-016-0999-...
; Prado et al., 2017Prado FD, Fernández-Cebrián R, Hashimoto DT, Senhorini JA, Foresti F, Martínez P, Porto-Foresti F. Hybridization and genetic introgression patterns between two South American catfish along their sympatric distribution range. Hydrobiologia. 2017; 788:319-43. https://doi.org/10.1007/s10750-016-3010-5
https://doi.org/10.1007/s10750-016-3010-...
), and P. corruscans (He=0.709-0.760, Pereira et al., 2009Pereira LHG, Foresti F, Oliveira C. Genetic structure of the migratory catfish Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) suggests homing behaviour. Ecol Freshw Fish . 2009; 18(2):215-25. https://doi.org/10.1111/j.1600-0633.2008.00338.x
https://doi.org/10.1111/j.1600-0633.2008...
; Dantas et al., 2013Dantas HL, Santos Neto MA, Oliveira KKC, Severi W, Diniz FM, Coimbra MRM. Genetic diversity of captive and wild threatened catfish Pseudoplatystoma corruscans in the São Francisco River. Rev Fish Sci. 2013; 21(3-4):237-46. https://doi.org/10.1080/10641262.2013.800787
https://doi.org/10.1080/10641262.2013.80...
; Vaini et al., 2016Vaini JO, Crispim BA, Silva DBS, Benites C, Russo MR, Grisolia AB. Genetic variability of pure Pseudoplatystoma corruscans and Pseudoplatystoma reticulatum individuals in the Paraná and Paraguay River basins. Fish Sci. 2016; 82:605-11. https://doi.org/10.1007/s12562-016-0999-3
https://doi.org/10.1007/s12562-016-0999-...
). Nonetheless, the genetic diversity observed in this study was lower than those found in R. quelen (He=0.614-0.909, Ríos et al., 2017Ríos N, Bouza C, Gutiérrez V, García G. Species complex delimitation and patterns of population structure at different geographic scales in Neotropical silver catfish (Rhamdia: Heptapteridae). Environ Biol Fishes. 2017; 100:1047-67. https://doi.org/10.1007/s10641-017-0622-1
https://doi.org/10.1007/s10641-017-0622-...
; 2019Ríos N, Bouza C, García G. Past hybridisation and introgression erased traces of mitochondrial lineages evolution in the Neotropical silver catfish Rhamdia quelen (Siluriformes: Heptapteridae). Hydrobiologia . 2019; 830:161-77. https://doi.org/10.1007/s10750-018-3861-z
https://doi.org/10.1007/s10750-018-3861-...
), P. punctifer (He=0.783, Telles et al., 2014Telles MP, Collevatti RG, Braga RS, Guedes LBS, Castro TG, Costa MC et al . Geographical genetics of Pseudoplatystoma punctifer (Castelnau, 1855) (Siluriformes, Pimelodidae) in the Amazon basin. Genet Mol Res . 2014; 13(2):3656-66. https://doi.org/10.4238/2014.May.9.8
https://doi.org/10.4238/2014.May.9.8...
), P. corruscans (He=0.862, Prado et al., 2017Prado FD, Fernández-Cebrián R, Hashimoto DT, Senhorini JA, Foresti F, Martínez P, Porto-Foresti F. Hybridization and genetic introgression patterns between two South American catfish along their sympatric distribution range. Hydrobiologia. 2017; 788:319-43. https://doi.org/10.1007/s10750-016-3010-5
https://doi.org/10.1007/s10750-016-3010-...
), and P. maculatus (He=0.871, Ribolli et al., 2012Ribolli J, Melo CMR, Zaniboni-Filho E. Genetic characterization of the Neotropical catfish Pimelodus maculatus (Pimelodidae, Siluriformes) in the Upper Uruguay River. Genet Mol Biol . 2012; 35(4):761-69. https://doi.org/10.1590/S1415-47572012005000060
https://doi.org/10.1590/S1415-4757201200...
).

In S. cuspicaudus, genotypic frequencies were distributed according to Hardy-Weinberg equilibrium and the inbreeding values were not significant save for sections S5 and S8 in which values lower than 10% suggest a careful management to prevent adverse effects regarding fitness (Frankham et al., 2014Frankham R, Bradshaw CJA, Brook BW. Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv. 2014; 170:56-63. https://doi.org/10.1016/j.biocon.2013.12.036
https://doi.org/10.1016/j.biocon.2013.12...
). On the contrary, and despite their high genetic diversity, A. pardalis and P. grosskopfii exhibited a heterozygosity deficit that cannot be explained by the Wahlund effect in the only genetic group formed by A. pardalis nor in each of the two genetic groups of P. grosskopfii that co-migrate in the studied area, wherein the heterozygosity deficit stayed significant.

Unlike P. grosskopfii, which has external reproduction (Loir et al., 1989Loir M, Cauty C, Planquette P, Le Bail PY. Comparative study of the male reproductive tract in seven families of South-Arnerican catfishes. Aquat Living Resour. 1989; 2(1):45-56. https://doi.org/10.1051/alr:1989005
https://doi.org/10.1051/alr:1989005...
), the assortative mating can explain the heterozygosity deficit in A. pardalis since it has internal insemination and elaborated courtships (Galvis et al., 1997Galvis G, Mojica JI, Camargo M. Peces del Catatumbo. Bogotá (D.C.): ECOPETROL; 1997.) and the females store spermatozoa inside their ovaries (Contreras et al., 2012Contreras-C P, Zapata-B B, Rosado-P R. Aspectos preliminares del manejo reproductivo en cautiverio de la doncella (Ageneiosus pardalis Lütken, 1874). Rev MVZ Cordoba. 2012; 17(3):3147-53. Available from: http://www.scielo.org.co/pdf/mvz/v17n3/v17n3a08.pdf
http://www.scielo.org.co/pdf/mvz/v17n3/v...
). However, to verify this hypothesis, it remains necessary to further research the reproductive behavior of these species.

Alternatively, the heterozygosity deficit could be explained by inbreeding as A. pardalis (2.600-8.600%) and P. grosskopfii (10.800-21.800%) showed significant FIS values. This effect may result from different anthropic activities like overfishing due to diminishments in captures since 1994 (Jiménez-Segura,Villa-Navarro, 2011Jiménez-Segura LF, Villa-Navarro FA. Pimelodus grosskopfii Steindachner 1879. In: Lasso CA, Agudelo Córdoba E, Jiménez-Segura LF, Ramírez-Gil H, Morales-Betancourt M, Ajiaco-Martínez RE et al., editors. I. Catálogo de recursos pesqueros continentales de Colombia. Serie Editorial Recursos Hidrobiológicos y Pesqueros Continentales de Colombia. Bogotá (D.C.): Instituto de investigaciones de Recursos Biológicos Alexander von Humboldt; 2011, p.466-71.) and their presence in the first 10 species captured for the Magdalena-Cauca basin (AUNAP, 2020Autoridad Nacional de Acuacultura y Pesca (AUNAP). SEPEC-Servicio Estadístico Pesquero Colombiano [Internet]. Bogotá; 2020. Available from: http://sepec.aunap.gov.co/
http://sepec.aunap.gov.co/...
). Other factor that could negatively contribute to the studied catfish species is the contamination in basins caused by mining as in the studied zone there is gold, silver, and platinum extraction (UPME, 2019Unidad de planeación minero energética (UPME). Producción, regalías y comercio exterior [Internet]. Bogotá (D.C.): Sistema de información minero colombiano (SIMCO).; 2019. Available from: http://www1.upme.gov.co/simco/Cifras-Sectoriales/Paginas/Informacion-estadistica-minera.aspx
http://www1.upme.gov.co/simco/Cifras-Sec...
), and there is evidence of mercury bioaccumulation, a residual contaminant of this activity, in several species that cohabit in the zone (Marrugo-Negrete et al., 2008Marrugo-Negrete J, Verbel JO, Ceballos EL, Benítez LN. Total mercury and methylmercury concentrations in fish from the Mojana region of Colombia. Environ Geochem Health. 2008; 30:21-30. https://doi.org/10.1007/s10653-007-9104-2
https://doi.org/10.1007/s10653-007-9104-...
; Álvarez et al., 2012Álvarez S, Jessick AM, Palacio JA, Kolok AS. Methylmercury concentrations in six fish species from two Colombian rivers. Bull Environ Contam Toxicol. 2012; 88:65-68. https://doi.org/10.1007/s00128-011-0458-x
https://doi.org/10.1007/s00128-011-0458-...
).

All those factors above mentioned may explain the recent decline in populations suggested by bottlenecks in the three studied species, supporting the hypothesis of genetic vulnerability of fishes due to anthropic interventions. A non-excluding alternative considers the climate factor as an additional influence of the demographic aspects of the populations of these species. Extreme changes in the Cauca River flow as consequences of the climatic phenomenon El niño-Southern Oscillation (ENSO) presented in the region in the prior years, wherein since 2007 there has been extreme NIÑA (2007-2008 and 2010-2011) and NIÑO (2009-2010, Hoyos et al., 2013Hoyos N, Escobar J, Restrepo JC, Arango AM, Ortiz JC. Impact of the 2010-2011 La Niña phenomenon in Colombia, South America: the human toll of an extreme weather event. Appl Geogr. 2013; 39:16-25. https://doi.org/10.1016/j.apgeog.2012.11.018
https://doi.org/10.1016/j.apgeog.2012.11...
) phenomena, could have caused bottlenecks as described in the same region for Curimata mivartii (Landínez-García, Marquez, 2018Landínez-García RM, Márquez EJ. Microsatellite loci development and population genetics in Neotropical fish Curimata mivartii (Characiformes: Curimatidae). PeerJ. 2018; 6:e5959. https://doi.org/10.7717/peerj.5959
https://doi.org/10.7717/peerj.5959...
). This climate factor could contribute to bottlenecks phenomena associated to overfishing, which has been described for other Neotropical catfishes as P. corruscans, P. reticulatum, and B. flavicans (Coronel et al., 2004Coronel JS, Maes GE, Claus S, Van Damme PA, Volckaert FAM. Differential population history in the migratory catfishes Brachyplatystoma flavicans and Pseudoplatystoma fasciatum (Pimelodidae) from the Bolivian Amazon assessed with nuclear and mitochondrial DNA markers. J Fish Biol . 2004; 65(3):859-68. https://doi.org/10.1111/j.0022-1112.2004.00498.x
https://doi.org/10.1111/j.0022-1112.2004...
; Prado et al., 2018Prado FD, Fernández-Cebrián R, Foresti F, Oliveira C, Martínez P, Porto-Foresti F. Genetic structure and evidence of anthropogenic effects on wild populations of two Neotropical catfishes: baselines for conservation. J Fish Biol . 2018; 92(1):55-72. https://doi.org/10.1111/jfb.13486
https://doi.org/10.1111/jfb.13486...
).

Genetic structure analysis. This study did not find significant differences among individuals of middle and lower sections of the Cauca River, which indicates that the environmental heterogeneity of the basin and, in particular, the steep slope of the Cauca River canyon is not a barrier for the gene flow of P. grosskopfii. However, such slope seems to limit of dispersion of S. cuspicaudus and A. pardalis in the middle section of the Cauca River since no individuals of these species were captured in the higher sections of the studied area in the sampled period (2011-2014). This result is not surprising for a short migrator like A. pardalis; nonetheless, the spatial distribution differed in the middle range migrators S. cuspicaudus and P. grosskopfii, suggesting that besides from their migration range, other factors as body conformation, habitat preferences and behavior, can play an important role in the observed spatial distribution, which is an important approach for future researches. A strong limitation to spatial distribution by the Cauca River canyon is also observed in Pseudopimelodus atricaudus, a new species described in the lower section of the Cauca River that diverged about 16 mya from its congener P. magnus distributed upstream the Cauca River canyon (Rangel-Medrano et al., 2020Rangel-Medrano JD, Ortega-Lara A, Márquez EJ. Ancient genetic divergence in bumblebee catfish of the genus Pseudopimelodus (Pseudopimelodidae: Siluriformes) from northwestern South America. PeerJ. 2020; 8:e9028. https://doi.org/10.7717/peerj.9028
https://doi.org/10.7717/peerj.9028...
; Restrepo-Gómez et al., 2020Restrepo-Gómez AM, Rangel-Medrano JD, Márquez EJ, Ortega-Lara A. Two new species of Pseudopimelodus Bleeker, 1858 (Siluriformes: Pseudopimelodidae) from the Magdalena Basin, Colombia. PeerJ. 2020; 8:e9723. https://doi.org/10.7717/peerj.9723
https://doi.org/10.7717/peerj.9723...
).

In the spatial distribution analyzed for each species, the Bayesian analysis of STRUCTURE, the DAPC, the AMOVA and the pairwise distances showed absence of geographic population structure in the studied species. These results concord with the ones described for other Neotropical catfishes that perform medium and large distance migrations as P. maculatus (Almeida et al., 2001Almeida FS, Fungaro MHP, Sodré LMK. RAPD and isoenzyme analysis of genetic variability in three allied species of catfish (Siluriformes: Pimelodidae) from the Tibagi River, Brazil. J Zool. 2001; 253(1):113-20. https://doi.org/10.1017/S0952836901000103
https://doi.org/10.1017/S095283690100010...
, 2003; Ribolli et al., 2012Ribolli J, Melo CMR, Zaniboni-Filho E. Genetic characterization of the Neotropical catfish Pimelodus maculatus (Pimelodidae, Siluriformes) in the Upper Uruguay River. Genet Mol Biol . 2012; 35(4):761-69. https://doi.org/10.1590/S1415-47572012005000060
https://doi.org/10.1590/S1415-4757201200...
), B. flavicans (Coronel et al., 2004Coronel JS, Maes GE, Claus S, Van Damme PA, Volckaert FAM. Differential population history in the migratory catfishes Brachyplatystoma flavicans and Pseudoplatystoma fasciatum (Pimelodidae) from the Bolivian Amazon assessed with nuclear and mitochondrial DNA markers. J Fish Biol . 2004; 65(3):859-68. https://doi.org/10.1111/j.0022-1112.2004.00498.x
https://doi.org/10.1111/j.0022-1112.2004...
), B. rousseauxii (Batista, Alves-Gomes, 2006Batista JDS, Alves-Gomes JA. Phylogeography of Brachyplatystoma rousseauxii (Siluriformes - Pimelodidae) in the Amazon Basin offers preliminary evidence for the first case of “homing” for an Amazonian migratory catfish. Genet Mol Res. 2006; 5(4):723-40. Available from: http://www.funpecrp.com.br/gmr/year2006/vol4-5/pdf/gmr0231.pdf
http://www.funpecrp.com.br/gmr/year2006/...
), P. corruscans and P. reticulatum (Vaini et al., 2016Vaini JO, Crispim BA, Silva DBS, Benites C, Russo MR, Grisolia AB. Genetic variability of pure Pseudoplatystoma corruscans and Pseudoplatystoma reticulatum individuals in the Paraná and Paraguay River basins. Fish Sci. 2016; 82:605-11. https://doi.org/10.1007/s12562-016-0999-3
https://doi.org/10.1007/s12562-016-0999-...
; Prado et al., 2018Prado FD, Fernández-Cebrián R, Foresti F, Oliveira C, Martínez P, Porto-Foresti F. Genetic structure and evidence of anthropogenic effects on wild populations of two Neotropical catfishes: baselines for conservation. J Fish Biol . 2018; 92(1):55-72. https://doi.org/10.1111/jfb.13486
https://doi.org/10.1111/jfb.13486...
). Nevertheless, our results with A. pardalis and S. cuspicaudus contrast with the results for P. corruscans in the basin of rivers Paraguay and Paraná wherein the authors hypothesize a possible homing behavior for the species (Pereira et al., 2009Pereira LHG, Foresti F, Oliveira C. Genetic structure of the migratory catfish Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) suggests homing behaviour. Ecol Freshw Fish . 2009; 18(2):215-25. https://doi.org/10.1111/j.1600-0633.2008.00338.x
https://doi.org/10.1111/j.1600-0633.2008...
; Dantas et al., 2013Dantas HL, Santos Neto MA, Oliveira KKC, Severi W, Diniz FM, Coimbra MRM. Genetic diversity of captive and wild threatened catfish Pseudoplatystoma corruscans in the São Francisco River. Rev Fish Sci. 2013; 21(3-4):237-46. https://doi.org/10.1080/10641262.2013.800787
https://doi.org/10.1080/10641262.2013.80...
).

Distinct from A. pardalis and S. cuspicaudus, each formed by one genetic group, P. grosskopfii represented two coexisting genetic groups in the evaluated sections of the Cauca River. This result in P. grosskopfii could reflect a possible spatial reproductive isolation, considering the preference for reproductive sites (homing) described for other species of Pimelodidae family as B. rousseauxii (Batista, Alves-Gomes, 2006Batista JDS, Alves-Gomes JA. Phylogeography of Brachyplatystoma rousseauxii (Siluriformes - Pimelodidae) in the Amazon Basin offers preliminary evidence for the first case of “homing” for an Amazonian migratory catfish. Genet Mol Res. 2006; 5(4):723-40. Available from: http://www.funpecrp.com.br/gmr/year2006/vol4-5/pdf/gmr0231.pdf
http://www.funpecrp.com.br/gmr/year2006/...
), P. corruscans (Pereira et al., 2009Pereira LHG, Foresti F, Oliveira C. Genetic structure of the migratory catfish Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) suggests homing behaviour. Ecol Freshw Fish . 2009; 18(2):215-25. https://doi.org/10.1111/j.1600-0633.2008.00338.x
https://doi.org/10.1111/j.1600-0633.2008...
; Dantas et al., 2013Dantas HL, Santos Neto MA, Oliveira KKC, Severi W, Diniz FM, Coimbra MRM. Genetic diversity of captive and wild threatened catfish Pseudoplatystoma corruscans in the São Francisco River. Rev Fish Sci. 2013; 21(3-4):237-46. https://doi.org/10.1080/10641262.2013.800787
https://doi.org/10.1080/10641262.2013.80...
), and P. reticulatum (Abreu et al., 2009Abreu MM, Pereira LHG, Vila VB, Foresti F, Oliveira C. Genetic variability of two populations of Pseudoplatystoma reticulatum from the Upper Paraguay River Basin. Genet Mol Biol. 2009; 32(4):868-73. https://doi.org/10.1590/S1415-47572009005000075
https://doi.org/10.1590/S1415-4757200900...
). Another non-excluding alternative is that P. grosskopfii experiences temporary reproductive isolation as the Cauca River presents two hydrological periods of shallow and deep waters that could benefit two reproductive periods of the fish species that habit this basin (Jiménez-Segura et al., 2010Jiménez-Segura LF, Palacio J, Leite R. River flooding and reproduction of migratory fish species in the Magdalena River basin, Colombia. Ecol Freshw Fish. 2010; 19(2):178-86. https://doi.org/10.1111/j.1600-0633.2009.00402.x
https://doi.org/10.1111/j.1600-0633.2009...
; López-Casas et al., 2016López-Casas S, Jiménez-Segura LF, Agostinho AA, Pérez CM. Potamodromous migrations in the Magdalena River basin: Bimodal reproductive patterns in Neotropical rivers. J Fish Biol . 2016; 89(1):157-71. https://doi.org/10.1111/jfb.12941
https://doi.org/10.1111/jfb.12941...
). This explanation is supported in the observation of a greater number of individuals of P. grosskopfii participating in the migration during the first period compared to the second hydrological period of the Magdalena River (López-Casas et al., 2016). Despite the latter, to the date, there is no detailed information as per the reproductive periods and behaviors of P. grosskopfii that allows to elucidate the origin of the genetic groups.

Under this context, it is recommended that the information obtained in this study regarding the structure and diversity of three coexisting species of catfishes in the middle and lower sections of the Cauca River is considered within the expansion proposals of the hydroelectric development for Colombia (Angarita et al., 2018Angarita H, Wickel AJ, Sieber J, Chavarro J, Maldonado-Ocampo JA, Herrera-R GA et al. Basin-scale impacts of hydropower development on the Mompós Depression wetlands, Colombia. Hydrol Earth Syst Sci. 2018; 22(5):2839-65. https://doi.org/10.5194/hess-22-2839-2018
https://doi.org/10.5194/hess-22-2839-201...
) and of other anthropic activities. The higher values of the inbreeding coefficient were found for P. grosskopfii, included in 2016 as a critical danger species in the red list of the International Union for Conservation of Nature - IUCN (Villa-Navarro et al., 2016Villa-Navarro FA, Usma-Oviedo JS, Mesa-Salazar L, Sanchez-Duarte P. Pimelodus grosskopfii. The IUCN red list of threatened species 2016:eT49829828A61473588 [Internet]. http://dx.doi.org/10.2305/IUCN.UK.2016-1.RLTS.T49829828A61473588.en
http://dx.doi.org/10.2305/IUCN.UK.2016-1...
), for which it is necessary to enforce the proposed measures for the recovery and conservation of natural populations of the species. Despite the inbreeding values found for S. cuspicaudus and A. pardalis are lower than 10%, which is the suggested limit to avoid substantial losses in the reproductive features (Soulé, 1980Soulé ME. Thresholds for survival: maintaining fitness and evolutionary potential. In: Soulé ME, Wilcox B, editors. Conservation biology: an evolutionary-ecological Perspective. Sunderland: Sinauer Associates Inc; 1980. p.151-69.), it is advisable to continue monitoring these populations to evaluate the changes of the species over time since it has been indicated that inbreeding values higher than cero (FIS>0) can cause negative effects in the fitness of natural populations (Frankham et al., 2014Frankham R, Bradshaw CJA, Brook BW. Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv. 2014; 170:56-63. https://doi.org/10.1016/j.biocon.2013.12.036
https://doi.org/10.1016/j.biocon.2013.12...
).

In conclusion, employing species-specific microsatellite loci, this study determined the diversity and possible genetic structure in the middle and lower sections of the Cauca River for the Neotropical catfishes A. pardalis, P. grosskopfii and S. cuspicaudus. The genetic diversity levels of the three species (expected heterozygosity and number of alleles/locus) are high; however, all the studied species seem to have suffered recent bottlenecks and exhibit significant inbreeding values, which are greater for P. grosskopfii, currently in a higher risk category. Furthermore, P. grosskopfii shows the coexistence of two genetic groups while A. pardalis and S. cuspicaudus are mainly represented by a genetic group. Contrary to the expectations, none of the evaluated species showed population structure related to some heterogeneous features of the basin. It was also evidenced that the cannon of the Cauca River in this zone does not represent a barrier to the gene flow of P. grosskopfii but it seems to limit the dispersion of A. pardalis and S. cuspicaudus.

ACKNOWLEDGMENTS

This work was funded by the Universidad Nacional de Colombia, Sede Medellín and Empresas Públicas de Medellín, Grant CT-2013-002443-R1 “Variación genotípica y fenotípica de poblaciones de especies reófilas presentes en el área de influencia del proyecto hidroeléctrico Ituango”, Grant Convenio CT-2019-000661 “Variabilidad genética de un banco de peces de los sectores medio y bajo del Río Cauca”.

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Restrepo-Escobar N, Yepes-Acevedo AJ, Márquez EJ. Population genetics of three threatened catfish species in heterogeneous environments of the Cauca River, Colombia. Neotrop Ichthyol. 2021; 19(1):e200040. https://doi.org/10.1590/1982-0224-2020-0040

Publication Dates

  • Publication in this collection
    08 Mar 2021
  • Date of issue
    2021

History

  • Received
    22 May 2020
  • Accepted
    29 Dec 2020
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