The current analysis investigates whether the uplift of the Serra da Esperança and the Ponta Grossa Arch in the Serra Geral resulted in ichthyofaunistic changes in adjacent basins. For this, we describe the phylogeographic structure among populations of Trichomycterus collected in hydrographic basins in southern Brazil by using partial nucleotide sequences of the mitochondrial gene Cytochrome C Oxidase subunit I. Analyses revealed that the nomenclature Trichomycterus davisi fails to contain the whole genetic diversity range found in the collected specimens and indicates at least six genetic lineages in Trichomycterus. Diagnostic morphological characteristics not associated to T. davisi could be identified in some specimens from the Iguaçu Piquiri haplogroup, indicating the occurrence of species Trichomycterus stawiarski. The lack of morphological differences among the other clades clearly suggests a cryptic species case. Molecular analyses revealed at least five new species besides T. davisi in the hydrographic basins and support the interpretation that genetic structure in T. davisi species complex is explained by tectonic events intrinsic to the areas of influence of Serra da Esperança and the Ponta Grossa Arch which occurred around 1.7 My.
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References
1.
AviseJC. Phylogeography: retrospect and prospect. J Biogeogr, 2009; 36:3–15.
2.
BurridgeCP, CrawD, JackDC, KingTM, WatersJW. Does fish ecology predict dispersal across a river drainage divide?. Evolution, 2008; 62:1484–1499.
3.
ThomazA, ChristieMR, KnowlesL. The architecture of river networks can drive the evolutionary dynamics of aquatic populations. Evolution, 2016; 70:731–739.
4.
HirschmannA, MalabarbaLR, ThomazAT, FagundesNJR. Riverine habitat specificity constrains dispersion in a Neotropical fish (Characidae) along Southern Brazilian drainages. Zool Scr, 2015; 44:374–382.
5.
ThomazAT, MalabarbaLR, BonattoSL, KnowlesLL. Testing the effect of palaeodrainages versus habitat stability on genetic divergence in riverine systems: study of a Neotropical fish of the Brazilian coastal Atlantic Forest. J Biogeogr, 2015; 42:2389–2401.
6.
IngenitoLFS, BuckupPA. The serra da Mantiqueira, South-Eastern Brazil, as a biogeographical barrier for fishes. J Biogeogr, 2007; 34:1173–1182.
7.
RibeiroAC. Tectonic history and the biogeography of the freshwater fishes from the costal drainages of eastern Brazil: an example of fauna evolution associated with a divergent continental margin. Neotrop Ichthyol, 2006; 4:225–246.
8.
MenaM, VilasJF. Serra Geral formation: new lower cretaceous paleomagnetic pole for Gondwana. Geophys Res Abstr, 2005; 7:08894.
StrugaleM, RostirollaSP, ManciniF, Portela FilhoCV, FerreiraFJF, FreitasRC. Structural framework and Mesozoic-Cenozoic evolution of Ponta Grossa Arch, Paraná Basin, southern Brazil. J South Am Earth Sci, 2007; 24:203–227.
11.
BreaM, ZucolAF: The Paraná-Paraguay Basin: geology and paleoenvironments. In: Historical Biogeography of Neotropical Freshwater Fishes. AlbertJS and ReisRE (eds), pp. 69–87, University of California Press, Berkeley, London, 2011.
12.
FrotaA, GonçalvesEVR, DepráGC, GraçaWJ. Inventory of the ichthyofauna from the Jordão and Areia river basins (Iguaçu drainage, Brazil) reveals greater sharing of species than thought. Check List, 2016; 12:1995.
13.
FroeseR, PaulyD. FishBase, World Wide Web electronic publication. 2017. Available at: www.fishbase.org/search.php (last accessed on May11, 2017).
14.
de PinnaMCC, WosiackiW: Family Trichomycteridae. In: Check List of the Freshwater Fishes of South America. ReisRE, KullanderSO and FerrarisCJJr. (eds), pp. 270–290, EDIPUCRS, Porto Alegre, RS, 2003.
15.
HasemanJD. Some new species of fishes from the Rio Iguassú. Ann Carnegie Museum, 1911; 7:374–387.
16.
IngenitoLFS, DubocLF, AbilhoaV. Contribution to the knowledge of the ichthyofauna from the Upper Iguaçu River basin, Paraná, Brazil. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, 2004; 7:23–36.
17.
CostaADA, FerreiraDG, SilvaWF, ZanattaAS, ShibattaOA, GalindoBA. Fishes (Osteichthyes: Actinopterygii) from the Penacho stream, upper Paraná River basin, Paraná State, Brazil. Check List, 2013; 95:19–523.
18.
DelarivaRL, SilvaJC. Fish fauna of headwater streams of Perobas Biological Reserve, a conservation unit in the Atlantic Forest of the Northwestern Paraná State, Brazil. Check List, 2013; 9:549–554.
19.
HoffmannAC, NascimentoRHC, ShibattaOA. Fish fauna from tributaries throughout the Tibagi River basin, upper Paraná basin, Brazil. Check List, 2015; 11:1815.
20.
FrotaA, DepráGC, PetenucciLM, GraçaWJ. Inventory of the fish fauna from Ivaí River basin, Paraná State, Brazil. Biota Neotrop, 2016; 16:e20150151
21.
de PinnaMCC: Phylogenetic relationships of neotropical Siluriformes (Teleostei: Ostariophysi): historical overview and synthesis of hypotheses. In: Phylogeny and Classification of Neotropical Fishes. MalabarbaLR, ReisRE, VariRP, LucenaZMS and LucenaCAS (eds), pp. 279–330, EDIPUCRS, Porto Alegre, RS, 1998.
22.
MalabarbaL, FialhoCB, AnzaJÁ, SantosJF, MendesGN: Peixes. In: Biodiversidade dos Campos do planalto das araucárias. BoldriniI (ed), pp. 131–156, MMA, Brasília, DF, 2009.
23.
NogueiraC, BuckupPA, MenezesNA, OyakawaOT, KaseckerTP, Ramos NetoMB, et al.Restricted-range fishes and the conservation of Brazilian freshwaters. PLoS One, 2010; 5:1–10.
24.
FerrerJ, MalabarbaLR. A new Trichomycterus lacking pelvic fins and pelvic girdle with a very restricted range in southern Brazil (Siluriformes: Trichomycteridae). Zootaxa, 2011; 2912:59–67.
25.
BorinLA, Martins-SantosIC. Intra-individual numerical chromosomal polymorphism in Trichomycterus davisi (Siluriformes, Trichomycteridae) from the Iguaçu River basin in Brazil. Genet Mol Biol, 2000; 23:605–607.
26.
BorinLA, Martins-SantosIC, OliveiraC. A natural triploid in Trichomycterus davisi (Siluriformes, Trichomycteridae): mitotic and meiotic characterization by chromosome banding and synaptonemal complex analyses. Genetica, 2002; 115:253–258.
27.
HebertPDN, RatnasinghamS, WaardJR. Barcoding animal life: cytochrome c oxidase subunit 1 divergence among closely related species. Proc Biol Sci, 2003; 270:S96–S99.
28.
WaughJ. DNA barcoding in animal species: progress, potential and pitfalls. Bioessays, 2007; 29:188–197.
29.
HebertPDN, GregoryTR. The promise of DNA barcoding for taxonomy. Mol Syst Biol, 2004; 54:852–859.
30.
Valdez-MorenoM, IvanovaNV, Elías-GutiérrezM, Contreras-BalderasS, HebertPD. Probing diversity in freshwater fishes from Mexico and Guatemala with DNA barcodes. J Fish Biol, 2009; 74:377–402.
31.
CarvalhoDC, OliveiraDA, PompeuPS, LealCG, OliveiraC, HannerR. Deep barcode divergence in Brazilian freshwater fishes: the case of the São Francisco River basin. Mitochondrial DNA, 2011; 22:80–86.
32.
PereiraLHG, MaiaGM, HannerR, ForestiF, OliveiraC. DNA barcodes discriminate freshwater fishes from the Paraíba do Sul River Basin, São Paulo, Brazil. Mitochondrial DNA, 2011; 22:71–79.
33.
PereiraLHG, MaiaGM, HannerR, ForestiF, OliveiraC. DNA barcoding reveals hidden diversity in the Neotropical freshwater fish Piabina argentea (Characiformes: Characidae) from the Upper Paraná Basin of Brazil. Mitochondrial DNA, 2011; 22:87–96.
34.
PereiraLHG, HannerR, ForestiF, OliveiraC. Can DNA barcoding accurately discriminate mega divere Neotropical freshwater fish fauna?. BMC Genet, 2013; 14:1–14.
35.
MeloBF, OchoaLE, VariRP, OliveiraC. Cryptic species in the Neotropical fish genus Curimatopsis (Teleostei, Characiformes). Zool Scr, 2016; 45:650–658.
AydinZ, MarcussenT, ErtekinAS, OxelmanB. Marginal likelihood estimate comparisons to obtain optimal species delimitations in Silene sect. Cryptoneurae (Caryophyllaceae). PLoS One, 2014; 9:1–9.
38.
FujitaMK, LeachéAD, BurbrinkFT, McGuireJA, MoritzC. Coalescent-based species delimitation in na integrative taxonomy. Trends Ecol Evol, 2012; 27:480–488.
39.
PonsJ, BarracloughTG, Gomez-ZuritaJ, CardosoA, DuranDP, HazellS, et al.Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol, 2006; 55:595–609.
40.
TalaveraG, DincaV, VilaR. Factors affecting species delimitations with the GMYC model: insights from a butterfly survey. Methods Ecol Evol, 2013; 4:1101–1110.
41.
IvanovaNV, ZemlakTS, HannerRH, HebertPDN. Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes, 2007; 7:544–548.
42.
RosenthalA, CoutelleO, CraxtonM. Large-scale of DNA sequencing templates by microtitre format PCR. Nucleic Acids Res, 1993; 21:173–174.
43.
ThompsonJD, HigginsDG, GibsonTJ, ClustalW. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res, 1994; 22:4673–4680.
LibradoP, RozasJ. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 2009; 25:1451–1452.
46.
BouckaertR, HeledJ, KühnertD, VaughanT, WuCH, XieD, et al.BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Comput Biol, 2014; 10:1–6.
47.
BerminghamE, McCaffertyS, MartinAP: Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus. In: Molecular Systematics of Fishes. StepienC and KocherT (eds), pp. 113–128, Academic Press, New York, NY, 1997.
48.
LanfearR, CalcottB, HoSYW, GuindonS. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol, 2012; 29:1695–1701.
49.
SilvestroD, MichalakI. raxmlGUI: a graphical front-end for RaxML. Org Divers Evol, 2012; 12:335–337.
50.
HusonDH, BryantD. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol, 2006; 23:254–267.
51.
BryantD, MoultonV. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol, 2004; 21:255–265.
52.
FujisawaT, BarracloughTG. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol, 2013; 62:707–724.
53.
ZhangJ, KapliP, PavlidisP, StamatakisA. A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 2013; 29:2869–2876.
54.
PuillandreN, LambertA, BrouilletS, AchazG. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol, 2012; 21:1864–1877.
55.
QueirozK. Species concepts and species delimitation. Syst Biol, 2007; 6:879–886.
56.
OyakawaOT, AkamaA, MautariKC, NolascoJC: Peixes de riachos da Mata Atlântica nas Unidades de Conservação do Vale do Rio Ribeira de Iguape no Estado de São Paulo. Neotropica, São Paulo, SP, 2006.
57.
BaumgartnerG, PavanelliCS, BaumgartnerD, BifiAG, DebonaT, FranaVA: Peixes do baixo rio Iguaçu. EDUEM, Maringá, PR, 2012.
58.
SaaidA, MachetteMN, HallerKM, DartRL, BradleyL, SouzaAMPD. Map and database of Quaternary faults and lineaments in Brazil. 2002. Available at: http://pubs.usgs.gov/of/2002/ofr-02-230 (last accessed on May11, 2017).
59.
AlmeidaFFM, CarneiroCDR. Origin and evolution of the Serra do Mar. Revista brasileira de Geociências, 1998; 28:135–150.
60.
Franco-MagalhaesAOB, HackspacherPC, GlasmacherUA, SaadAR. Rift to post-rift evolution of a “passive” continental margin: the Ponta Grossa Arch, SE Brazil. Int J Earth Sci, 2010; 99:1599–1613.
61.
LarentisC, DelarivaRL, GomesLC, BaumgartnerD, RamosIP, SereiaDAO. Ichthyofauna of streams from the lower Iguaçu River basin, Paraná State, Brazil. Biota Neotrop, 2016; 16:e20150117.
62.
AviseJC, ArnoldJ, BallRM, BerminghamE, LambT, NeigelJE, et al.Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst, 1987; 18:498–522.
63.
WardRD. DNA barcode divergence among species and genera of birds and fishes. Mol Ecol Resour, 2009; 9:1077–1085.
64.
AgostinhoAA, GomesLC: Manejo e monitoramento de recursos pesqueiros: perspectivas para o reservatório de Segredo. In: Reservatório de Segredo: Bases Ecológicas para o Manejo. AgostinhoAA and GomesLC (eds), pp. 319–364, EDUEM, Maringá, PR, 1997.
65.
PetriS, FulvaroVJ: Geologia do Brasil. EDUSP, São Paulo, SP, 1983.
66.
BuckupPA: The Eastern Brazilian Shield. In: Historical Biogeography of Neotropical Freshwater Fishes. AlbertJS and ReisRE (eds), pp. 203–210, University of California Press, London, 2011.
67.
MeloMRS, BuckupPA, OyakawaOT. A new species of Characidium Reinhardt, 1867 (Characiformes: Crenuchidae) endemic to the Atlantic Forest in Paraná State, southern Brazil. Neotrop Ichthyol, 2016; 14:e160014.
68.
MorroneJJ. On the identification of areas of endemism. Syst Biol, 1994; 43:438–444.
69.
Löwenberg-NetoP, CarvalhoCJB. Análise Parcimoniosa de Endemicidade (PAE) na delimitação de áreas de endemismos: inferências para conservação da biodiversidade na Região Sul do Brasil. Natureza Conservação, 2004; 2:58–65.
70.
MME (Ministério das Minas e Energias). Diagnóstico e Planejamento da Utilização dos Recursos Hídricos da Bacia do Iguaçu. Companhia Pesqueira e Recursos Minerais, 1990; 1:33.
71.
RoxoFF, LujanNK, TagliacolloVA, WaltzBT, SilvaGSC, OliveiraC, et al.Shift slow- to fast-water habitats accelerates lineage and phenotype evolution in a clade of Neotropical suckermouth catfishes (Loricariidae: Hypoptopomatinae). PLoS One, 2017; 12:e0178240.
72.
LososJB. Adaptive radiation, ecological opportunity, and evolutionary determinism. Am Nat, 2010; 175:623–639.
73.
GomesLC, PessaliTC, SalesNG, PompeuPS, CarvalhoDC. Integrative taxonomy detects cryptic and overlooked fish species in a neotropical river basin. Genetica, 2015; 143:581–588.
74.
MeierR, ShiyangK, VaidyaG, NgPKL. DNA barcoding and taxonomy in diptera: a tale of high intraspecific variability and low identification success. Syst Biol, 2006; 55:715–728.
75.
WiemersM, FiedlerK. Does the DNA barcoding gap exist?—a case study in blue butterflies (Lepidoptera: Lycaenidae). Front Zool, 2007; 4:8–12.
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