Systematic and historical biogeography of the Bryconidae (Ostariophysi: Characiformes) suggesting a new rearrangement of its genera and an old origin of Mesoamerican ichthyofauna

Abstract

Background: Recent molecular hypotheses suggest that some traditional suprageneric taxa of Characiformes require revision, as they may not constitute monophyletic groups. This is the case for the Bryconidae. Various studies have proposed that this family (considered a subfamily by some authors) may be composed of different genera. However, until now, no phylogenetic study of all putative genera has been conducted.

Results: In the present study, we analyzed 27 species (46 specimens) of all currently recognized genera of the Bryconidae (ingroup) and 208 species representing all other families and most genera of the Characiformes (outgroup). Five genes were sequenced: 16SrRNA, Cytochrome b, recombination activating gene 1 and 2 and myosin heavy chain 6 cardiac muscle. The final matrix contained 4699 bp and was analyzed by maximum likelihood, maximum parsimony and Bayesian analyses. The results show that the Bryconidae, composed of Brycon, Chilobrycon, Henochilus and Salminus, is monophyletic and is the sister group of Gasteropelecidae + Triportheidae. However, the genus Brycon is polyphyletic. Fossil studies suggest that the family originated approximately 47 million years ago (Ma) and that one of the two main lineages persisted only in trans-Andean rivers, including Central American rivers, suggesting a much older origin of Mesoamerican ichthyofauna than previously accepted.

Conclusion: Bryconidae is composed by five main clades, including the genera Brycon, Chilobrycon, Henochilus and Salminus, but a taxonomic review of these groups is needed. Our results point to a possible ancient invasion of Central America, dating about 20.3 ± 5.0 Ma (late Oligocene--early Miocene), to explain the occurrence of Brycon in Central America.

Figure 1

Geographical distribution of the Bryconidae samples. 1-Brycon moorei; 2-Brycon chagrensis, Brycon petrosus; 3-Brycon moorei, Salminus affinis; 4-Brycon amazonicus, Brycon falcatus; 5-Brycon amazonicus; 6-Brycon falcatus; 7-Brycon pesu; 8-Brycon pesu; 9-Salminus sp.; 10-Brycon amazonicus; 11-Brycon melanopterus; 12-Chilobrycon deuterodon; 13-Brycon aff. atrocaudatus; 14-Brycon falcatus; 15-Brycon gouldingi; 16-Brycon cf. falcatus; 17-Brycon hilarii; 18-Brycon pesu; 19-Brycon sp.; 20-Brycon hilarii; 21-Brycon hilarii; 22-Brycon orthotaenia, Salminus franciscanus; 23-Brycon ferox, Brycon vermelha, Henochilus wheatlandii; 24-Brycon insignis; 25-Brycon nattereri; 26-Brycon opalinus; 27-Brycon opalinus; 28-Brycon orbignyanus, Salminus brasiliensis; 29-Salminus hilarii; 30-Brycon nattereri. Map constructed with the program QGIS 2.2.0 (http://www.qgis.org) using layers obtained in the websites http://www.earthobservatory.nasa.gov and http://www.ibge.gov.br/home/geociencias.

Figure 2

Summary tree showing relationships among major lineages obtained by a maximum likelihood (ML) partitioned analysis of the concatenated dataset and emphasizing the relationships among species of Bryconidae (bold). A series of three numbers (e.g., 1/100/87) at each of the main nodes represents the posterior probability for that split obtained in the Bayesian analysis (B), percentage of bootstrap support obtained by ML analysis, and percentage of bootstrap support obtained by MP analysis, respectively (1000 bootstrap replicates). Dashes represent values less than 0.5 (B) or 50% (ML, MP). Asterisks represent nodes that were not obtained by B or MP analyses.

Figure 3

Best maximum likelihood (ML) tree of the Bryconidae obtained in the partitioned analysis of the concatenated dataset. Numbered nodes as referenced in text and values shown in Figure 2. Numbers after species names, between braches, refer to collecting sites shown in the Figure 1; dashes represent fishes from aquaculture without known locality.

Figure 4

The BEAST chronogram tree from 50 million generations, indicating the divergence over time of the family Bryconidae. Red circle shows the calibration points based on the fossil Lignobrycon ligniticus (28.5 ± 5.5 Ma). Scale = millions of years before present.