Genetic relationships of Plagioscion ... - Wiley Online Library

Journal of Fish Biology (2017) 91, 375–384 doi:10.1111/jfb.13347, available online at wileyonlinelibrary.com

Genetic relationships of Plagioscion squamosissimus (Perciformes, Sciaenidae) from five Neotropical river basins evaluated using mitochondrial atpase6/8 gene sequences N. A. Diamante*†, S. M. A. P. Prioli‡§, A. V. Oliveira‡§, T. M. C. Fabrin‖, L. M. Prioli‡ and A. J. Prioli‡ *Programa de Pós-graduação em Biologia Comparada, Universidade Estadual de Maringá, Maringá, PR, Brazil, ‡Nucleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia), Universidade Estadual de Maringá, Maringá, PR, Brazil, §Departamento de Biotecnologia, Genética e Biologia Celular, Universidade Estadual de Maringá, Maringá, PR, Brazil and ‖Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais, Universidade Estadual de Maringá, Bloco G-90, Av. Colombo 5790, 87020-900, Maringá, PR, Brazil (Received 25 October 2016, Accepted 10 May 2017) The genetic relationships of native or introduced Plagioscion squamosissimus in five Brazilian Neotropical basins were evaluated using the mitochondrial atpase6/8 genes. Results revealed that the population of the Tocantins River basin is more basal than the native populations of the Amazon and Parnaíba River basins. Moreover, the populations of P. squamosissimus that were introduced in the São Francisco and upper Paraná River basins originated from the population of the Parnaíba River. © 2017 The Fisheries Society of the British Isles

Key words: atpase; corvina; genetic variability; introduced species; molecular markers.

In Brazil, Plagioscion squamosissimus (Heckel 1840) is naturally distributed in the Amazon (Soares et al., 1978), Tocantins (Merona, 1986) and Parnaíba (Silva & Menezes, 1950) river basins. It was also introduced to other river basins and several artificial reservoirs (Fontenele & Peixoto, 1978; Torloni et al., 1993; Casatti, 2005; Barros et al., 2012), among which the upper Paraná and São Francisco River basins should be emphasized. The story of introducing P. squamosissimus to Brazilian waters started in 1933 when the Brazilian public works department against drought (DNOCS) introduced fingerlings in the dam reservoirs of north-eastern Brazil (Fontenele & Peixoto, 1978). Moreover, between 1966 and 1973, the electricity company of São Paulo brought specimens of P. squamosissimus to the state of São Paulo from the DNOCS Pisciculture post of Lima Campos in the state of Ceará, Brazil to repopulate the rivers and lakes in São Paulo †Author to whom correspondence should be addressed. Tel.: +55 44 3011 4685; email: [email protected]

375 © 2017 The Fisheries Society of the British Isles

376

N . A . D I A M A N T E E T A L.

(Torloni et al., 1993). There are no records of the origin of these populations introduced by DNOCS. The first successful introduction in the state of São Paulo occurred in the Limoeiro Reservoir on the Pardo River. It was from this point that P. squamosissimus specimens dispersed into the Grande River and subsequently established themselves in the Paraná River by 1972 (Machado, 1974). Plagioscion squamosissimus has colonised practically all the habitats of the upper Paraná River basin during the past 30 years and may be considered the best example of a successfully introduced species (Agostinho et al., 2008). Plagioscion squamosissimus is an effective predator and has been a threat to the local ichthyofauna (Agostinho et al., 2004), but, at the same time, it has become an important species for commercial fisheries in the area (Torloni et al., 1993; Petrere et al., 2002). Molecular studies based on random amplification of polymorphic DNA (RAPD) and D-loop markers have recently demonstrated that the populations of P. squamosissimus that were introduced in the Paraná River basin originated from the native populations of the Parnaíba River basin (Panarari-Antunes et al., 2012, 2015). The origin of the introduced populations in the São Francisco River, however, remains unknown. The identification of haplotypes in regions where populations are native will be useful for comparison with the haplotypes present in the regions where the species are introduced. In regions where P. squamosissimus is native, few phylogenetic and biogeographic studies employing molecular markers (Cooke et al., 2012; Santos et al., 2013; Boeger et al., 2014) have been conducted. Avise et al. (1987) observed that mitochondrial DNA haplotypes of some of these populations have specific geographic locations, introducing phylogenetics into discussions of population structure. Thus, the degree of divergence of mitochondrial (mt)DNA haplotype sequences may be related to the geographic distribution of the species (Avise, 2000). The current study aimed to evaluate the genetic variability of native and introduced populations of P. squamosissimus in several Neotropical river basins using mitochondrial atpase6/8 gene sequences to investigate the phylogeography of native populations and the origin of introduced populations. Specimens of P. squamosissimus (n = 78) were captured from the floodplain of the upper Paraná River basin, Parnaíba, Tocantins and São Francisco River basins (Table I and Fig. 1). Specimens were anaesthetized with an overdose of clove oil and subsequently sacrificed (Griffiths, 2000). Samples of muscular tissues were removed, fixed in ethanol and stored at −20∘ C in the tissue bank of the Laboratory of Genetics of the Research Nucleus in Limnology, Ichthyology and Aquaculture (Nupélia) of the Universidade Estadual de Maringá, Maringá, PR, Brazil. Total DNA was extracted from tissue samples using the phenol–chloroform protocol (Monesi et al., 1998). The mitochondrial atpase6/8 region was amplified, as described by Corrigan et al. (2008). PCR products were purified and sequencing reactions were performed using the Big Dye Terminator kit (ThermoFisher; www.thermofisher.com). The ABI 3500 automatic sequencer (ThermoFisher) was used to determine nucleotide sequences, according to the manufacturer’s instructions. Nucleotide sequences were manually edited using BioEdit 7.2.0 (Hall, 1999) and aligned in Clustal W (Thompson et al., 1994) using Mega 6.0 (Tamura et al., 2013). Haplotypes of each specimen were selected using DnaSP 5.1 (Librado & Rozas, 2009). Sequence composition, haplotype and nucleotide diversity indices were performed using the Arlequin 3.5 software (Excoffier & Lischer, 2010). A haplotype network

© 2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, 91, 375–384

377

G E N E T I C R E L AT I O N S H I P S O F P. S Q U A M O S I S S I M U S

Table I. Collection sites and number of specimens Plagioscion squamosissimus collected in neotropical river basins River basin

Locality

Parnaíba

Lagoon Nazareth near Nazaré do Piauí township, Piauí, Brazil. Lagoons Porta and Meio, near Miguel Alves township, Piauí, Brazil. Mesa da Pedra Reservoir in Poty River, Piauí. Brazil. Tocantins River, near Peixe township, Tocantins, Brazil. Lajeado Reservoir near Porto Nacional township, Tocantins, Brazil. Tocantins River near Ipueiras, Tocantins, Brazil. Santa Tereza River near Peixe township, Tocantins, Brazil. Upper Paraná River floodplain near Porto Rico township, Paraná, Brazil. São Francisco River, near Petrolina township, Pernambuco, Brazil. Cooke et al., 2013

Tocantins

Upper Paraná River São Francisco

Amazon

Co-ordinates

Sample size (n)

07∘ 00′ S 42∘ 39′ W

25

04∘ 02′ S 42∘ 49′ W 06∘ 10′ S 41∘ 58′ W 11∘ 52′ S 48∘ 35′ W

22

10∘ 37′ S 48∘ 24′ W 11∘ 14′ S 48∘ 27′ W 08∘ 58′ S 48∘ 10′ W 22∘ 47′ S 53∘ 19′ W

20

09∘ 27′ S 40∘ 35′ W

11

Total

73 151

was built to verify the spatial distribution of haplotypes in all populations using the median-joining method in PopArt (http://popart.otago.ac.nz/). Phylogenetic analyses were performed using the maximum-likelihood (ML) method with 1000 bootstrap resamplings and a phylogenetic tree was built using Mega6. Divergence time estimation was carried out using the BEAST 2 package (Beast, BEAUti, TreeAnnotator, LogCombiner; Bouckaert et al., 2014). A strict clock model was used and calibrations were made according to Bermingham et al. (1997). A constant size coalescent tree prior was specified and the best nucleotide substitution model TIM3 + I + Γ was estimated in jModelTest 2.1.7 (Darriba et al., 2012), according to the Bayesian information criterion (BIC). A Monte-Carlo Markov chain (MCMC) of 20 million generations was performed and sampled every 1000 generations. Results were checked using Tracer 1.6 (Rambaut et al., 2014; effective sample size > 200). The first 10% of the chain was discarded as burn-in. The ultrametric tree was edited with FigTree (http://tree.bio.ed.ac.uk/software/figtree/). All partial sequences that were obtained and analysed during this study were deposited in GenBank (KX065110–KX065187). Obtained sequences of 816 bp comprised the mitochondrial atpase6/8 genes from 78 native or introduced P. squamosissimus specimens that were collected from four Brazilian Neotropical river basins. Seventy-three haplotypes from P. squamosissimus mitochondrial DNA atpase6/8 genes


378


80°

70°

5°

60°

50°

na

íba

Amazon

5°

N

5°

ra

N

Pa

0

5° 10°

tins

300 km

10°

45°

15°

40°

10°

Toca n

N

15°

1000 km

5°

20°

300 km

55°

Brazil N

50°

40°

São Francisco

15°

N

Upper Paraná

N

300 km

16° 45°

20°

40°

20° 1000 km

South America

24° 300 km

55°

50°

45°

Fig. 1. Locations ( ) in Brazilian river basins from which specimens of Plagioscion squamosissimus analysed in current assay were collected.

from the Amazon River basin were also obtained from GenBank for phylogenetic comparisons (JN683723.1–JN683796.1) (Table I). Seventy-eight polymorphic sites, featuring 81 mutations and 41 informative sites were identified. The estimated transition–transversion ratio was 2·26, where 69·4 and 30·6% of substitutions were transitions and transversions, respectively. Mean frequency of the four nucleotides of the P. squamosissimus specimens were C, 33·97%; T, 28·36%; A, 25·63% and G, 12·04%. Only the sequences obtained in this study (n = 78) were included for estimative haplotype and nucleotide diversity indices, as the sequences from the Amazon River basin (GenBank) were merely singletons population analyses were inappropriate. The most frequent haplotype was H9, which was shared by 53 specimens from three different sites: the native populations of the Parnaíba River basin and the introduced populations of both the upper Paraná and São Francisco River basins; the other haplotypes were not shared. The populations of the Tocantins and Parnaíba River basins have seven and one exclusive haplotypes, respectively (Table II). The haplotype diversity index (h) for all specimens of the four analysed populations was 0·530, whereas the nucleotide diversity index 𝜋 = 0·00635. The haplotype and nucleotide diversities among the native populations were high in those from the Tocantins River basin. The populations of the Parnaíba River basin featured low


379


Table II. Distribution of nine haplotypes of Plagioscion squamosissimus associated with samples of upper Paraná, Parnaíba, São Francisco, and Tocantins River basins Haplotype H1 H2 H3 H4 H5 H6 H7 H8 H9 Total

Paraná

Parnaíba

Tocantins

São Francisco

Total

– – – – – – – – 20 20

– – – – – – – 3 22 25

5 1 3 4 4 4 1 – – 22

– – – – – – – – 11 11

5 1 3 4 4 4 1 3 53 78

diversity rates, which were c. 30% of the rates of the population from the Tocantins River basin. When the introduced populations were considered, the haplotype and nucleotide diversity rates were null (Table III). The nucleotide substitution model for the phylogenetic reconstruction of the P. squamosissimus population was TN93 + G + I. The tree that was generated by the maximum-likelihood method [Fig. 2(a)] provided three great clades. The populations of the Tocantins River basin were the basal group and those of the São Francisco, upper Paraná and Parnaíba River basins constituted a single group, which was closely related to the clade formed from the Amazon River basin population that is included in this Discussion section. The support of the ultrametric tree [Fig. 2(b)] followed the bootstrap support of the likelihood analysis. According to the divergence time estimated in the analysis, the divergence between specimens sampled in upper Paraná, São Francisco, Parnaíba and Amazon (Genbank) basins and the Tocantins basin is between 1·1 and 2·35 million years (Myear) in age (95% highest posterior density; HPD), with a mean of 1·75 Myear in age. The results of the haplotype network, generated by PopArt, revealed that three were groups formed: group 1, by exclusive haplotypes of specimens from the Tocantins River basin; group 2, by shared haplotypes of specimens of the Parnaíba, São Francisco and upper Paraná River basins; group 3, comprising two groups formed by haplotypes of specimens from the Amazon River basin (Fig. 3). Robust

Table III. Haplotype and nucleotide diversity index for Plagioscion squamosissimus populations from different Brazilian river basins River upper Paraná Parnaíba Tocantins S. Francisco

Sequences

Haplotypes

Haplotype diversity (h)

Nucleotide diversity (𝜋)

20 25 22 11

1 2 7 1

0·000 ± 0·000 0·220 ± 0·100 0·866 ± 0·032 0·000 ± 0·000

0·00000 ± 0·00000 0·00054 ± 0·00024 0·00287 ± 0·00021 0·00000 ± 0·00000


380


0·95

(a)

86

(b)

1 0·98 0·42

0·47 77 0·38 43 0·13 0·47 14

1

0·99

0·99 1

77 0·75

Plagioscion ternetzi 0·008

1·0 Myear 0

1

2

3

Fig. 2. Trees constructed from atpase6/8 sequences of Plagioscion squamosissimus populations in different Brazilian river basins. (a) Maximum-likelihood tree, with 1000 bootstrap resampling. (b) Bayesian ultrametric tree, with numbers above branches representing posterior probability values. Node bars = 95% highest posterior-density interval of the time estimation. , Amazon River basin; , Parnaíba, São Francisco and upper Paraná river basins; , Tocantins River basin.

differentiation may be perceived by the absence of intermediary haplotypes among the haplogroups. The sites of the Amazon River basin specimens are referenced per the sequence information in GenBank and according to Cooke et al. (2012). The FishBase website (www.fishbase.org) does not mention the occurrence of P. squamosissimus in the Parnaíba River basin. This population, however, is important as it appears to have the highest repercussions on Neotropical ichthyofauna outside the Amazon River basin. In addition, this population is economically relevant in regions where it was introduced (Petrere et al., 2002). According to the current analyses and studies by Torloni et al. (1993), the population of P. squamosissimus in the Paraná River basin, which was introduced in the upper river basin and dispersed towards the lower Paraná River, originated from the populations of the Parnaíba River basin. The results showed that this introduced population shares its single haplotype with the populations of the Parnaíba River. Panarari-Antunes et al. (2012) revealed that P. squamosissimus offspring from the Parnaíba River basin occur only in the Paraná River basin and these have no kinship with the populations of the



381

10 samples 1 sample

Fig. 3. Network of Plagioscion squamosissimus haplotypes sampled in the Amazon ( ), Parnaíba ( ), upper Paraná ( ), São Francisco ( ) and Tocantins ( ) river basins, based on sequences of mitochondrial atpase6/8 genes. , Hypothetical haplotypes.

Amazon River basin. Thus, their findings support the current results. Furthermore, the results of this study showed that the population of the São Francisco River basin also originated from that of the Parnaíba River basin. Despite the small number of specimens sampled from this basin, this conclusion was based on the finding that the single haplotype in the São Francisco River basin also occurred in the Parnaíba River and upper Paraná River basins. Haplotypes from the Amazon River basin, however, have not been registered. In invasive fish species, maintenance of genetic variability depends upon the number of introduced individuals and upon multiple introductions from different populations (Salmenkova, 2008). When the history of the introduction of this species in the upper Paraná and São Francisco River basins is evaluated, the introduced populations of P. squamosissimus have a lower genetic variability than the native populations, considering the possible events of genetic drift that result from the insufficient sampling of native populations. Low genetic diversity rates (haplotype diversity and nil nucleotides) were also observed in this study. Carvalho et al. (2014) identified low genetic variability in successful invading populations of Cichla Bloch & Schneider 1801 in south-eastern Brazil, which is possibly explained by factors such as reproduction strategies, the evolutionary-trap effect and the hypothesis of biotic resistance. In the case of introduced P. squamosissimus populations, others factors may also be related to its successful invasion. P. squamosissimus successfully colonised all the habitats of the Paraná River basin (Agostinho et al., 2008), despite the low genetic diversity rates observed in the current analyses and by Panarari-Antunes et al. (2012, 2015). Considering native populations, results showed that despite the genetic flow between fish populations of the Amazon region and the Tocantins River basin, the populations of P. squamosissimus in the two basins are greatly differentiated. Although the Tocantins River basin is not clearly isolated, the two regions do, in fact, share the same species of


382


fish. Approximately 150 of 554 species are endemic (Ruiz, 2009), therefore, ecological barriers that are not easily identified may hinder the movement of P. squamosissimus specimens and consequently, genetic flow. This separation, whether physical or biological, appears to have been in effect for a long enough period to integrate deep haplotype differences, such as those reported between the populations of the Tocantins River basin and the other populations. A more extreme situation exists when the populations of the Tocantins and Parnaíba River basins are compared. The absence of common haplotypes reveals that the separation of these two populations is older than the separation of the populations from the Tocantins and Amazon River basins. Such a condition was expected given the physical separation that is represented by the flow restrictions of the Parnaíba River, which physically impairs genetic flow via migration between the two river basins. As mentioned previously, the divergence time analysis estimated that upper Paraná, São Francisco, Parnaíba and Amazon basins and Tocantins basin, are separated by 1·1–2·35 Myear, with a mean of 1·75 Myear. The results regarding population divergence are preliminary, considering the estimated time of divergence among the different populations is close to the estimated time for the formation of the entire Amazon basin, some 2·5 Myear ago (Campbell et al., 2006). The separation of these populations would have occurred subsequent to that event. Phylogenetic trees revealed that the population of the Tocantins River basin occupies a more basal position, which is closer to the Plagioscion ternetzi Boulenger 1895 outgroup than the populations of the Amazon and Parnaíba River basins. Although bootstrap values has been low, the most basal condition is the preliminary evidence that the population of the Tocantins River basin is older than the other populations analysed here, contrary to molecular data by Cooke et al. (2012). Cooke et al. (2012) suggested that the speciation of P. squamosissimus occurred in the north-western region of South America and that the demographic dispersion and expansion occurred after the complete formation of the Amazon River, some 2·5 Myear ago (Campbell et al., 2006). The ancestral population would have dispersed and colonised several other regions. If this route is correct, one may suppose that, prior to dispersion, the ancestral population would have been closer to the current population of the Tocantins River basin than that of the Amazon River basin. Consequently, ancestral subpopulations that occupied the Amazon River basin would have been replaced by the more recently derived populations that experienced a new period of demographic expansion. The populations of the Amazon and Parnaíba River basins are more closely related to each other than they are to those of the Tocantins River basin. Such a supposition may be confirmed by the positions of the Amazon and Parnaíba River basins populations in the phylogenetic tree. Haplotypes of the Amazon haplogroup are abundant and differ among themselves by one or more nucleotides (Cooke et al., 2012). High haplotype and nucleotide diversity suggests a long evolutionary history (Grant & Bowen, 1998), as observed in the Amazon River basin. Therefore, the population of the Parnaíba River basin also would have been more recently derived than the current population of the Tocantins River basin. The current analysis revealed the genetic diversity between the populations of P. squamosissimus from five Neotropical river basins. Results also revealed that P. squamosissimus, which was introduced in the São Francisco and upper Paraná River basins, was derived from the population of the Parnaíba River basin. Mitochondrial



383

atpase6/8 gene sequences are an important tool for evaluating intraspecies genetic variability, corroborating data previously obtained using the D-loop region in P. squamosissimus. These data, however, are preliminary and future studies using other markers will provide a more complete understanding of these population dynamics. References Agostinho, A. A., Gomes, L. C. & Latini, J. D. (2004). Fisheries management in Brazilian reservoirs: lessons from/for South America. Interciencia 29, 334–338. Agostinho, A. A., Pelicice, F. M. & Gomes, L. C. (2008). Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazilian Journal of Biology 68, 1119–1132. Avise, J. C. (2000). Phylogeography: The History and Formation of Species. Cambridge, MA: Harvard University Press. Avise, J. C., Arnold, J., Ball, R. M., Bermingham, E., Lamb, T., Neigel, J. E., Reeb, C. A. & Saunders, N. C. (1987). Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics 18, 489–522. Barros, L. C., Santos, U., Zanuncio, J. C. & Dergam, J. A. (2012). Plagioscion squamosissimus (Sciaenidae) and Parachromis managuensis (Cichlidae): a threat to native fishes of the Doce River in Minas Gerais, Brazil. PLoS One 7, 39–138. Bermingham, E., McCafferty, S. & Martin, A. P. (1997). Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus. In Molecular Systematics of Fishes (Kocher, T. D. & Stepien, C. A., eds), pp. 113–128. San Diego, CA: Academic Press. Boeger, W. A., Marteleto, F. M., Zagonel, L. & Braga, M. P. (2014). Tracking the history of an invasion: the freshwater croakers (Teleostei: Sciaenidae) in South America. Zoologica Scripta 44, 250–262. Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M. A., Rambaut, A. & Drummond, A. J. (2014). BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537. Campbell, K. E., Frailey, C. D. & Romero-Pittman, L. (2006). The Pan-Amazonian Ucayali Peneplain, late Neogene sedimentation in Amazonia and the birth of the modern Amazon River system. Palaeogeography, Palaeoclimatology, Palaeoecology 239, 166–219. Carvalho, D. C., Oliveira, D. A. A., Sampaio, I. & Beheregaray, L. B. (2014). Analysis of propagule pressure and genetic diversity in the invasibility of a freshwater apex predator: the peacock bass (genus Cichla). Neotropical Ichthyology 12, 105–116. Casatti, L. (2005). Revision of the South American freshwater genus Plagioscion (Teleostei, Perciformes, Sciaenidae). Zootaza 1080, 39–64. Cooke, G. M., Chao, N. L. & Beheregaray, L. B. (2012). Marine incursions, cryptic species and ecological diversification in Amazonia: the biogeographic history of the croaker genus Plagioscion (Sciaenidae). Journal of Biogeography 39, 724–738. Corrigan, S., Huveneers, C., Schwartz, T. S., Harcourt, R. G. & Beheregaray, L. B. (2008). Genetic and reproductive evidence for two species of ornate wobbegong shark Orectolobus spp. on the Australian east coast. Journal of Fish Biology 73, 1662–1675. Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772. Excoffier, L. & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567. Fontenele, O. & Peixoto, J. T. (1978). Análise dos resultados de introdução da pescada do Piauí, Plagioscion squamosissimus (Heckel, 1840), nos açudes do Nordeste. Boletim Técnico DNOCS 36, 85–112. Grant, W. S. & Bowen, B. W. (1998). Shallow populations histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. Journal of Heredity 89, 415–426. Griffiths, S. P. (2000). The use of clove oil as an anaesthetic and method for sampling intertidal rockpool fishes. Journal of Fish Biology 57, 1453–1464.


384


Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98. Librado, P. & Rozas, J. (2009). DnaSP v5: a software for comprehensives analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452. Machado, C. E. M. (1974). Ação da CESP no meio ambiente. São Paulo: CESP. Merona, B. (1986). Aspectos ecológicos da ictiofauna no baixo Tocantins. Acta Amazonica 16, 109–124. Monesi, N., Jacobs-Lorena, L. & Paço-Larson, M. L. (1998). DNA puff BhC4-1 gene from Bradysia hygida is specifically transcribed in early prepupal salivary glands of Drosophila melanogaster. Chromosoma 107, 559–569. Panarari-Antunes, R. S., Prioli, A. J., Prioli, S. M. A. P., Gomes, V. N., Júlio, H. F. Jr., Agostinho, C. S., Silva Filho, J. P., Boni, T. A. & Prioli, L. M. (2012). Genetic divergence among invasive and native populations of Plagioscion squamosissimus (Perciformes, Sciaenidae) in Neotropical regions. Journal of Fish Biology 80, 2434–2447. Panarari-antunes, R. S., Prioli, A. J., Prioli, S. M. A. P., Júlio, H. F. Jr., Oliveira, A. V., Agostinho, C. S., Silva Filho, J. P. & Prioli, L. M. (2015). Genetic characterization of native and invasive Plagioscion squamosissimus (Perciformes, Sciaenidae) populations in Brazilian hydrographic basins. Genetics and Molecular Research 14, 14314–14324. Petrere, M. Jr., Agostinho, A. A., Okada, E. K. & Júlio, H. F. Jr. (2002). Review of the fisheries in the Brazilian portion of the Paraná/Pantanal basin. In Management and Ecology of Lake and Reservoir Fisheries (Cowx, I. G., ed), pp. 123–143. Oxford: Fishing News Books. Ruiz, W. B. G. (2009). Cinco espécies novas de Microglanis (Siluriformes: Pseudopimelodidae) da bacia do Tocantins-Araguaia, Brasil, com um catálogo das espécies de peixes da Bacia. Non-published Master ́ s Dissertation, Universidade Estadual de Londrina, Londrina, Brazil. Available at http://www.bibliotecadigital.uel.br/document/? code=vtls000148865/ Salmenkova, E. A. (2008). Population genetic processes in introduction of fish. Genetika 44, 874–884. Santos, S., Gomes, M. F., Ferreira, A. R. S. & Sampaio, I. (2013). Molecular phylogeny of the western South Atlantic Sciaenidae based on mitochondrial and nuclear data. Molecular Phylogenetics and Evolution 66, 423–428. Silva, S. L. O. & Menezes, R. S. (1950). Alimentação da corvina, Plagioscion squamosissimus (Heckel, 1840) da lagoa de Nazaré, Piauí (Actinopterygii, Sciaenidae). Revista Brasileira Biologia 10, 257–264. Soares, P. C., Landim, P. M. B. & Fúlfaro, V. J. (1978). Tectonic cycles and sedimentary sequences in the Brazilian intracratonic basins. Bulletin of the Geological Society of America 89, 181–191. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013). Mega 6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680. Torloni, C. E. C., Santos, J. J., Carvalho, A. A. & Correa, A. R. A. (1993). A pescada-dopiauí Plagioscion squamosissimus (Heckel, 1840) (Osteichthyes, Perciformes) nos reservatórios da CESP – Companhia Energética de São Paulo. Série Pesquisa e Desenvolvimento 84, 1–23.

Electronic Reference Rambaut, A., Suchard, M.A., Xie, D. & Drummond, A.J. (2014). Tracer v1.6, Available at http:// beast.bio.ed.ac.uk/Tracer/ (last accessed 1 December 2016).
