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Genetic Diversity of Invasive and Native Cichla (Pisces: Perciformes) Populations in Brazil with Evidence of Interspecific Hybridization

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Genetic Diversity of Invasive and Native Cichla (Pisces: Perciformes) Populations in Brazil with Evidence of Interspecific Hybridization Journal of Fish Biology (2006) 69 (Supplement B), 260–277 doi:10.1111/j.1095-8649.2006.01291.x, available online at http://www.blackwell-synergy.com Genetic diversity of invasive and native Cichla (Pisces: Perciformes) populations in Brazil with evidence of interspecific hybridization A. V. OLIVEIRA*†, A. J. PRIOLI*‡§, S. M. A. P. PRIOLI*‡, T. S. BIGNOTTO*, H. F. JU´LIO JR*‡, H. CARRERk, C. S. AGOSTINHO{ AND L. M. PRIOLI*# *Nu´cleo de Pesquisas em Limnologia, Ictiologia e Aqu¨icultura (Nupelia), Universidade Estadual de Maringa´, Av. Colombo 5790, Bloco G-90, 87020-900 Maringa´, PR, Brasil, ‡Departamento de Biologia Celular e Gene´tica, Universidade Estadual de Maringa´,Av. Colombo 5790, Bloco H-67, 87020-900 Maringa´, PR, Brasil, kDepartamento de Cieˆncias Biolo´gicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de Sa˜o Paulo, Av. Pa´dua Dias 11, 13418-900 Piracicaba, SP, Brasil, {Universidade Federal do Tocantins, Jardim dos Ipeˆs, 77500-000 Porto Nacional, TO, Brasil and #Departamento de Biologia, Universidade Estadual de Maringa´, Av. Colombo 5790, Bloco H-78, 87020-900 Maringa´, PR, Brasil (Received 7 July 2005, Accepted 1 August 2006) Invasive and native populations of the Amazonian fishes ‘peacock bass’ Cichla monoculus and of a not yet described species ‘blue tucunare´’ here referred as Cichla sp. ‘Azul’ were analysed for genetic diversity using the hypervariable domain of the mitochondrial DNA (mtDNA) control region plus steady diagnostic random amplified polymorphic DNA loci. There is no detailed historical record of the introduction of Cichla species into the Upper Parana´River basin, where they became invasive and a potential threat to local ichthyofauna. Genetic diversity among invasive populations confirmed the hypothesis of multiple introductions in this hydrographic basin. Moreover, a large and previously unknown population of natural fertile hybrids between C. cf. monoculus and Cichla sp. ‘Azul’ was identified in the Itaipu hydroelectric reservoir and in the floodplain of the Upper Parana´River. Crossbred morphotypes were similar to C. cf. monoculus, but their morphological identification was not unequivocal. This hybrid population was characterized by high genetic diversity and it was composed of hybrids possessing concurrently nuclear DNA fragments specific for C. cf. monoculus as well as fragments specific for Cichla sp. ‘Azul’. The nuclear DNA markers indicated that reproductive isolation between C. cf. monoculus and Cichla sp. ‘Azul’ has broken down in the new environment, and mtDNA sequences revealed that both species can be the female donor in the interspecific crosses. The data presented herein are potentially useful for future taxonomic, genetic and evolutionary studies in the complex Cichla group, for monitoring of invasive populations, and for further development of ecological guidelines. # 2006 The Authors Journal compilation # 2006 The Fisheries Society of the British Isles Key words: Cichla; Cichlid; D-loop; interspecific hybrids; peacock bass; tucunare´. §Author to whom correspondence should be addressed. Tel. and fax: þ55 44 3263 1424; email: [email protected] †Present address: Centro Universita´rio de Maringa´(Cesumar), Av. Guedner 1610, 87050-390 Maringa´, PR, Brasil. 260 # 2006 The Authors Journal compilation # 2006 The Fisheries Society of the British Isles GENETIC DIVERSITY OF CICHLA POPULATIONS 261 INTRODUCTION Non-native freshwater fishes have been deliberately introduced in Neotropical hydrographic basins even though these habitats are naturally abundant with native fish species. During the last decades, Brazil has received the highest number of non-native fishes in spite of its currently >2100 catalogued fish spe- cies, which comprise c. 21% of the world list (Buckup & Menezes, 2003). In- troductions have included fishes from other countries and also transfers among Brazilian hydrographic basins (Agostinho et al., 1994, 2003; Ju´lio & Agostinho, 2003). As extensively reported, non-native introduced fishes may become invasive and have a serious impact on aquatic ecosystems. As discussed by Agostinho et al. (2005), in Brazilian inland waters, fish species introductions have been recognized as one of the principal direct causes of biodiversity loss. Such introductions have been done mainly for aquaculture, fish stocking and recreational fisheries, and generally without considering their potential adverse impact on the environment and on the biodiversity of local aquatic ecosystems. The Upper Parana´River floodplain, a unique ecosystem with >250 reported fish species, has been strongly affected by non-native introduced fishes. It com- prises an environmental protected area, as well as the only remaining running water stretch of the Parana´River in Brazilian territory, which is not restrained by hydroelectric dams. In 1982, when the Itaipu hydroelectric dam was closed, the floodplain received a massive introduction of at least 35 fish species from the Middle Parana´River basin (Agostinho et al., 2003; Ju´lio & Agostinho, 2003). These fishes were introduced because the resulting Itaipu reservoir submerged the Guaı´ra Falls (Seven Falls), which had previously formed the natural geographic barrier between these two ichthyological provinces. As a consequence, c. 150 km of the Parana´River downstream of the falls were merged with the Upper Parana´River. On top of that, during the past three decades populations of both non-native and local fishes have been intentionally introduced in the Upper Parana´River basin. Amazonian piscivores have been the most successful colonizers in this basin where they have spread out of res- ervoirs and are now affecting areas with high abundance of endemic species, including the floodplain (Agostinho et al., 2004, 2005). Fishes of the genus Cichla Schneider, 1801, are among the species that were deliberately introduced in many hydrographic basins, including in the Upper Parana´(Agostinho et al., 1994, 2003, 2004; Shafland, 1996; Ju´lio & Agostinho, 2003). Most Cichla species are native to the Amazon and Orinoco basins. Morphological traits have been the basis of Cichla taxonomy, but this genus remains problematic. Although 15 different Cichla morphotypes have been reported (Kullander, 1986; Kullander & Nijssen, 1989), presently only five species are described: Cichla temensis Humboldt, 1821 (Orinoco, Negro and Tapajo´s Rivers); Cichla monoculus Spix & Agassiz, 1831 (Amazon basin, includ- ing the Tocantins–Araguaia sub-basin); Cichla ocellaris Bloch & Schneider, 1801 (Guyana rivers, from the Marowijne drainage in Suriname and French Guyana to the Essequibo drainage in Guyana); Cichla orinocensis Humboldt, 1821 (Orinoco and Negro rivers); Cichla intermedia Machado-Allison, 1971 (Upper Negro River and Middle Orinoco River). # 2006 The Authors Journal compilation # 2006 The Fisheries Society of the British Isles, Journal of Fish Biology 2006, 69 (Supplement B), 260–277 262 A. V. OLIVEIRA ET AL. In 1985, a few specimens identified as C. monoculus species, which is popularly known as ‘tucunare´’, ‘peacock bass’ and ‘pavo´n’, were found for the first time in the Itaipu hydroelectric reservoir (Agostinho et al., 1994, 2004). Sometime later, a not yet described Cichla species (S. Kullander, pers. comm.), which is popularly known as ‘tucunare´azul’ and ‘blue tucunare´’ and native to the Tocantins– Araguaia sub-basin of the Amazon River basin, was found in the Itaipu reser- voir. Initially, both Cichla populations seemed to be present at low density, but they increased rapidly and spread from the reservoir into many rivers and streams. Diverse morphotypes resembling C. monoculus, but of unclear identifica- tion as regards their morphological analysis, have also been found in the Itaipu reservoir and in the floodplain (C. S. Pavanelli, pers. comm.). Taxonomy, origin and introduction of Cichla in the Upper Parana´River basin remain unclear. It has been assumed that multiple Cichla introductions might have occurred into this basin, particularly in waters that are regulated by dams. Supposedly, Cichla were introduced by sport fishing associations but incidental escapes from pisci- culture might also have occurred occasionally (Orsi & Agostinho, 1999). More recently, Cichla populations have also been found in other areas of the Upper Parana´basin, mainly in reservoirs, but as far as is known, there is no record of their introductions. Cichla species are voracious predators feeding on a wide range of prey and displaying complex reproductive strategies (Fontanele & Peix- oto, 1979; Novaes et al., 2004). The introduction of Cichla populations in the Upper Parana´basin has developed into a controversial issue because while they became the most important species for sport fishery, they also have become highly invasive and voracious piscivores, a menace to local fishes, including endemic species (Fontenele & Peixoto, 1979; Agostinho et al., 2003, 2004). Knowledge of their genetic diversity and distinctive taxonomy is crucial for monitoring introduced Cichla populations, particularly those that are now invasive and a steady part of the current fauna in many areas of the Upper Parana´River basin. Mitochondrial genome and nuclear DNA fragments have proved useful in taxonomic and genetic studies. The hypervariable domain of the mitochondrial DNA (mtDNA) control region has been the main nucleotide sequence of choice for population and phylogenetic studies among closely related species. Diagnostic nuclear DNA fragments such as steady random amplified polymorphic DNA (RAPD) markers (Williams et al.,
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