Restricted accessResearch articleFirst published online 2015-02
Evolutionary Divergence Among Oligosarcus spp. (Ostariophysi,Characidae) from the São Francisco and Doce River Basins: Oligosarcus solitarius Menezes,1987 Shows the Highest Rates of Chromosomal Evolution in the Neotropical Region
The Doce River, in southeastern Brazil, is a coastal drainage, configured since the Late Cretaceous, when South America separated from Africa. Of the 77 native fish species of the Doce River Basin, 37 are potentially endangered—Oligosarcus solitarius, Menezes 1987, is the only endemic species of the quaternary lakes in the middle portion of this drainage and Oligosarcus argenteus, Günther 1864, is distributed in the Doce River channel and headwaters. This study characterizes the morphological, cytogenetic, and mitochondrial DNA variation in the Oligosarcus spp. populations from the Doce and São Francisco River Basins. The principal component analysis indicates three morphological groups. Cytogenetic data corroborate existence of the O. solitarius and O. argenteus fish species in the Doce River Basin, with high levels of population cytogenetic polymorphism. Taking into consideration the Pleistocene–Holocene formation of the lacustrine system in the middle Doce River, with low molecular differentiation and high levels of chromosomal variation among the O. solitarius populations, we concluded that O. solitarius has the highest rate of chromosomal evolution observed in Neotropical freshwater fishes. The morphological and cytogenetic patterns of the Oligosarcus sp. population collected at the Das Velhas River headwaters suggest that it may represent an undescribed species.
Get full access to this article
View all access options for this article.
References
1.
AlbertJS, ReisRE: Historical Biogeography of Neotropical Freshwater Fishes. University of California Press, Berkeley, CA, 2011.
SaadiA, MachetteMN, HallerKM, DartRL, BradleyL, de SouzaAMPD. Map and Database of Quaternary Faults and Lineaments in Brazil. U.S. Geological Survey, Open-File Report 02-230 (available at http://pubs.usgs.gov/of/2002/ofr-02-230), 2002.
5.
MeisMRM, MonteiroAMF. Upper Quaternary “rampas,” Rio Doce Valley: S.E. Brazilian plateau. Zusammenfassun für Geomorphologie, 1979; 23:132–151.
6.
TundisiJG, MeisMRM: Geomorphology and limnological processes at the Middle Rio Doce Valley lakes. In: Water Research Institute, Limnological Studies in Central Brazil. Chikusa-Ku (ed), pp. 11–17, Nagoya University, Nagoya, Japan, 1985.
7.
VieiraF: A ictiofauna do rio Santo Antônio, bacia do rio Doce, MG: proposta de conservação. Universidade Federal de Minas Gerais, Minas Gerais, Brazil, 2006.
8.
LatiniAO: Inventário rápido e identificação de variáveis que limitam a dispersão de exóticos: um estudo sobre peixes no médio rio Doce (MG, Brasil). Doctor Thesis. Universidade de Campinas, Campinas, Brazil, 2005.
9.
BarrosLC, SantosU, ZanuncioJC, DergamJA. Plagioscion squamosissimus (Sciaenidae) and Parachromis managuensis (Cichlidae): a threat to native fishes of the Doce River in Minas Gerais, Brazil. Plos One, 2012; 7:39138.
10.
GodinhoAL, VieiraF: Ictiofauna. Áreas prioritárias para a conservação da biodiversidade do Estado de Minas Gerais. In: Biodiversidade em Minas Gerais: um Atlas para sua Conservação. CostaC (ed), pp. 44–46, Fundação Biodiversitas, Belo Horizonte, Brazil, 1998.
11.
MenezesNA. Três espécies novas de Oligosarcus Günther, 1864 e redefinição taxonômica das demais espécies do gênero (Osteichthyes, Teleostei, Characidae). Bol Zool, 1987; 11:1–39.
12.
GüntherA: Catalogue of the Physostomi, containing the families Siluridae, Characinidae, Haplochitonidae, Sternoptychidae, Scopelidae, Stomiatidae in the collection of the British Museum. Catalogue of the Fishes in the British Museum. Trustees, London, 1864, xxii+455 p.
13.
MenezesNA. Systematics and evolution of the tribe Acestrohynchini (Pisces: Characidae). Arq Zool São Paulo, 1969; 18:1–150.
14.
SteindachnerF. Ichthyologische Beiträge (IV). Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften. Mathematisch-Naturwissenschaftliche Classe, 1876; 72:551–616.
15.
MirandeMJ, AguileraG, AzpelicuetaMLM. A threatened new species of Oligosarcus and its phylogenetic relationships, with comments on Astyanacinus (Teleostei: Characidae). Zootaxa, 2011; 2994:1–20.
16.
MenezesNA, RibeiroAC. Oligosarcus jacuiensis (Characiformes: Characidae), a new species from the Uruguay and Jacuí River Basins, southern Brazil. Neotrop Ichthyol, 2010; 8:649–653.
17.
Hermes-SilvaS, MeurerS, Zaniboni-FilhoE. Biologia alimentar e reprodutiva do peixe-cachorro (Oligosarcus jenynsii Günther, 1864) na região do alto rio Uruguai - Brasil. Acta Scientiarum Biol Sci, 2004; 26:175–179.
18.
SantosU, VolckerUCM, BeleiFA, CioffiMB, BertolloLAC, PaivaSR, DergamJA. Molecular and karyotypic phylogeography in the neotropical Hoplias malabaricus (Erythrinidae) fish in eastern Brazil. J Fish Biol, 2009; 75:2326–2343.
19.
PereiraTL, SantosU, SchaeferCE, SouzaGO, PaivaSR, MalabarbaLRM, SchmidtEE, DergamJA. Dispersal and vicariance of Hoplias malabaricus (Bloch, 1794) (Teleostei, Erythrinidae) populations of the Brazilian continental margin. J Biogeogr, 2013; 40:905–914.
20.
MartinezERM, OliveiraC, Julio-JuniorH. Cytogenetic analysis of species of the genera Acestrorhynchus, Oligosarcus and Rhaphiodon (Teleostei: Characiformes). Caryologia, 2004; 57:294–299.
21.
KavalcoKF, PazzaR, BertolloLAC, Moreira-FilhoO. Molecular cytogenetics of Oligosarcus hepsetus (Teleostei, Characiformes) from two Brazilian locations. Genetica, 2005; 124:85–91.
22.
CentofanteL, BertolloLAC, Moreira-FilhoO. Chromosomal differentiation between populations of Oligosarcus hepsetus (Teleostei, Characidae) from small tributaries at opposite margins of the Paraíba do Sul River (Brazil). Braz Arch Biol Technol, 2006; 6:981–987.
23.
RubertM, MargaridoPV. Cytogenetic studies in three species of the genus Oligosarcus. Braz Arch Biol Technol, 2007; 50:127–135.
24.
CalcagnottoD, SchaeferSA, DeSalleR. Relationships among characiform fishes inferred from analysis of nuclear and mitochondrial gene sequences. Mol Phylogenet Evol, 2005; 36:135–153.
25.
JavonilloR, MalabarbaLR, WeitzmanSH, BurnsJR. Relationships among major lineages of characid fishes (Teleostei: Ostariophysi: Characiformes), based on molecular sequence data. Mol Phylogenet Evol, 2010; 54:498–511.
HowellWM, BlackDA. Controlled silver staining of nucleolus organizing regions with a protective colloidal developer: a one-step method. Experimentia, 1980; 36:1014–1015.
30.
SchweizerD. Simultaneous fluorescent staining of R-bands and specific heterochromatic regions (DAPI bands) in human chromosomes. Cytogenet Cell Genet, 1980; 27:190–193.
31.
SolaL, RossiAR, LaselliV, RaschEM, MonacoPJ. Cytogenetics of bisexual/unisexual species of Poecilia II. Analysis of heterochromatin and nucleolar organizer regions in Poecilia mexicana mexicana by C-banding and DAPI, quinacrine, chromomycin A3, and silver staining. Cytogenet Cell Genet, 1992; 60:229–235.
32.
LevanA, FregdaK, SandbergAA. Nomenclature for centromeric position on chromosomes. Hereditas, 1964; 52:210–220.
33.
PinkelD, StraumeT, GrayJ. Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proc Natl Acad Sci U S A, 1986; 83:2934–2938.
34.
MartinsC, FerreiraIA, OliveiraC, ForestiF, GalettiPM. A tandemly repetitive centromeric DNA sequence of the fish Hoplias malabaricus (Characiformes: Erythrinidae) is derived from 5S rDNA. Genetica, 2006; 127:133–141.
35.
BoyceTM, ZwickME, AquadroCF. Mitochondrial DNA in the bark weevils: size, structure and heteroplasmy. Genetics, 1989; 123:825–836.
36.
HillisDM, MableBK, LarsonA, DavisSK, ZimmerE: Nucleic acids IV: sequencing and cloning. In: Molecular Systematics. HillisDM, MoritzC, and MableBK (eds), pp. 321–383, Sinauer Associates, Inc., Sunderland, MA, 1996.
37.
LibradoP, RozasJ. DnaSP v 5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 2009; 25:1451–1452.
38.
WhiteMJD: Modes of Speciation. W.H. Freeman publishers, San Francisco, CA, 1978.
39.
KingM: Species Evolution: The Role of Chromosome Change. Cambridge University Press, Cambridge, United Kingdom, 1993.
40.
FariaR, NavarroA. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol, 2010; 25:660–669.
41.
PazzaR, KavalcoKF. Rates of chromosomal changes in neotropical Characiformes (Teleostei). Curr Topics Genet, 2010; 4:11–19.
42.
GraurD, LiWH: Fundamentals of Molecular Evolution; Dynamics of Genes in Population. Sinauer Associates, Sunderland, MA, 2000.
43.
FalcãoJN. Estudos citogenéticos em Acestrorhynchinae e Cynopotaminae (Pisces, Characidae). Master's Thesis, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil, 1983.
MartinsC, GalettiPM. Organization of 5S rDNA in species of the fish Leporinus: two different genomic locations are characterized by distinct nontranscribed spacers. Genome, 2001; 44:903–910.
46.
WaskoAP, MartinsC, WrightJM, GalettiPM. Molecular organization of 5S rDNA in fishes of the genus Brycon. Genome, 2001; 44:893–902.
47.
KavalcoKF, PazzaR, BertolloLAC, Moreira-FilhoO. Gene mapping of 5S rDNA in eight fish species from the Paraíba do Sul River Basin, Brazil. Cytogenet Genome Res, 2004; 106:107–110.
48.
MartinsC, GalettiPM. Chromosomal localization of 5S rDNA genes in Leporinus fish (Anostomidae, Characiformes). Chromosome Res, 1999; 7:363–367.
49.
CaramaschiEP: Distribuição da ictiofauna de riachos das bacias do Tietê e do Paranapanema, junto ao divisor de águas (Botucatu, SP). Doctor's Thesis, Universidade Federal de São Carlos, São Carlos, Brazil, 1986.
50.
RibeiroAC: Filogenia and biogeografia do gênero Oligosarcus Günther, 1864 (Ostariophysi: Characidae). Doctor's Thesis, Uiversidade Estadual Paulista, Botucatu, Brazil, 2007.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
