Accelerated Diversification Explains the Exceptional Species Richness of Tropical Characoid Fishes

Abstract

The Neotropics harbor the most species-rich freshwater fish fauna on the planet, but the timing of that exceptional diversification remains unclear. Did the Neotropics accumulate species steadily throughout their long history, or attain their remarkable diversity recently? Biologists have long debated the relative support for these museum and cradle hypotheses, but few phylogenies of megadiverse tropical clades have included sufficient taxa to distinguish between them. We used 1288 ultraconserved element loci spanning 293 species, 211 genera, and 21 families of characoid fishes to reconstruct a new, fossil-calibrated phylogeny and infer the most likely diversification scenario for a clade that includes a third of Neotropical fish diversity. This phylogeny implies paraphyly of the traditional delimitation of Characiformes because it resolves the largely Neotropical Characoidei as the sister lineage of Siluriformes (catfishes), rather than the African Citharinodei. Time-calibrated phylogenies indicate an ancient origin of major characoid lineages and reveal a much more recent emergence of most characoid species. Diversification rate analyses infer increased speciation and decreased extinction rates during the Oligocene at around 30 Ma during a period of mega-wetland formation in the proto-Orinoco-Amazonas. Three species-rich and ecomorphologically diverse lineages (Anostomidae, Serrasalmidae, and Characidae) that originated more than 60 Ma in the Paleocene experienced particularly notable bursts of Oligocene diversification and now account collectively for 68% of the approximately 2150 species of Characoidei. In addition to paleogeographic changes, we discuss potential accelerants of diversification in these three lineages. While the Neotropics accumulated a museum of ecomorphologically diverse characoid lineages long ago, this geologically dynamic region also cradled a much more recent birth of remarkable species-level diversity. [Biodiversity; Characiformes; macroevolution; Neotropics; phylogenomics; ultraconserved elements.].

Figure 1.

Time-calibrated phylogeny of Characoidei and related otophysan taxa including 325 characoids (293 species and 211 genera) based on the best maximum likelihood tree of the 75% complete matrix of ultraconserved elements (1288 loci; 345,179 bp). Node ages were obtained from Bayesian analysis of the 92% complete matrix (57 loci; 17,400 bp) and six fossil calibrations (†). White circles represent nodes with lower than 100% bootstrap support at the family level. African clades denoted in grey silhouettes of the continent. Fish photographs by B. Melo, C. Robertson, J. García-Melo, J. Sullivan, L. García-Melo, M. Sabaj, M. Taylor, R. Schmidt, and Proyeto CaVFish Colombia.

Figure 2.

a) Time-calibrated phylogeny of characoid fishes and species diversity for each family; horizontal gray bars at nodes are 95% highest posterior density (HPD) intervals; African clades denoted in gray silhouettes of the continent. b) Results of BAMM analysis showing accelerated rates of speciation (warm colors) in three clades: Anostomidae, Serrasalmidae, and Characidae (except Spintherobolinae); shifts in diversification rate (red circles) occur only in Anostomidae and Characidae excluding Spintherobolinae. c) Summary results of the TESS-CoMET analysis for Characoidei, indicating moderate support for a tree-wide increase in speciation rates and decrease in extinction rates at around 30 Ma; rate estimates are represented by solid lines enveloped by a shaded 95% confidence interval; points illustrate statistical support for a shift in rates at a given time interval [in 2 ln (Bayes Factors)]. Vertical gray bars highlight the time period during which characoid diversification is estimated to have increased.