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 1,288 ultraconserved element loci (UCE) 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 million years ago (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 2,150 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.

Biogeography of curimatid fishes reveals multiple lowland–upland river transitions and differential diversification in the Neotropics (Teleostei, Curimatidae)

“…The second calibration is a constraint on the root of the tree selected to match the timing of the split between Curimatidae and Chilodontidae, as estimated from the molecular analysis of Characiformes (Melo et al, 2021 ). This analysis included 356 taxa and six fossil calibrations, and the time‐calibrated phylogeny revealed the split of Chilodontidae and Curimatidae at approximately 54.9 Ma (64.2–46.2 Ma, 95% highest posterior density; HPD) (Melo et al, 2021 ); therefore, we assigned a normally distributed prior on the root of our phylogeny (offset = 54.9 Ma; stdev = 7.5).…”

“…The second calibration is a constraint on the root of the tree selected to match the timing of the split between Curimatidae and Chilodontidae, as estimated from the molecular analysis of Characiformes (Melo et al, 2021 ). This analysis included 356 taxa and six fossil calibrations, and the time‐calibrated phylogeny revealed the split of Chilodontidae and Curimatidae at approximately 54.9 Ma (64.2–46.2 Ma, 95% highest posterior density; HPD) (Melo et al, 2021 ); therefore, we assigned a normally distributed prior on the root of our phylogeny (offset = 54.9 Ma; stdev = 7.5). The other available curimatid fossil † Plesiocurimata alvarengai (Figueiredo & Costa‐Carvalho, 1999 ) is controversial because of the incompleteness of informative characters preventing any phylogenetic placement of the fossil species within the family (Figueiredo & Costa‐Carvalho, 1999 ).…”

“…Conversely, an evolutionary cradle is a region of net species overproduction, in which regional speciation rates exceed extinction rates, resulting in an increase of species richness and biogeographic range expansion ( i.e ., dispersal) to adjacent regions (Figure 1 ) (Albert et al, 2011 ; Rangel et al, 2018 ; Stebbins, 1974 ). Although these simple macroevolutionary models do not fully summarize the complexity of most biogeographic regions, the museum‐cradle paradigm is widely used in contemporary analyses of tropical diversification (Azevedo et al, 2020 ; Cássia‐Silva et al, 2020 ; Dagallier et al, 2020 ; Matos‐Maraví et al, 2019 ; Melo et al, 2021 ; Meseguer et al, 2020 ; Rangel et al, 2018 ). Some caveats that apply to these models are that the taxa of a given region are not expected to be monophyletic with respect to that of adjacent regions (Figure 1 ) (Albert et al, 2011 ) and that a region may simultaneously serve as a cradle for some taxa and a museum for others (McKenna & Farrell, 2006 ; Moreau & Bell, 2013 ).…”

“…Although the original museum/cradle concept of Stebbins ( 1974 ) was qualitative and descriptive, these terms are now used as shorthand for quantitative models that compare rates of net diversification among regions ( e.g ., Jablonski et al, 2006 ; Moreau & Bell, 2013 ). Although these macroevolutionary models have been tested in other tropical groups (Gaston & Blackburn, 1996 ; McKenna & Farrell, 2006 ; Moreau & Bell, 2013 ), none have yet been tested explicitly in the NFF fauna (see Albert et al, 2011 , but see Melo et al, 2021 ).…”

Tracking the Evolutionary Trends Among Small-Size Fishes of the Genus Pyrrhulina (Characiforme, Lebiasinidae): New Insights From a Molecular Cytogenetic Perspective

“…Characiformes comprise a very diverse and abundant freshwater order (Nelson et al, 2016), in which the family Lebiasinidae is represented by 75 valid species (Fricke et al, 2021) widely distributed across South and Central America (Weitzman and Weitzman, 2003). The phylogenetic relationships of the Lebiasinidae remained in doubt for a long time, but more recent phylogenetic analysis indicate their proximity to the Ctenoluciidae (Calcagnotto et al, 2005;Oliveira et al, 2011), which was also reinforced by the different studies (Arcila et al, 2017;Betancur-R et al, 2019;Melo et al, 2021). Most Lebiasinidae species reach about 60 mm of Standard Length (SL), but miniature species, not surpassing a maximum of 26 mm SL, is found within the Pyrrhulininae, whereas medium-sized species up to 150 mm SL can be found within Lebiasininae (Weitzman and Weitzman, 2003).…”