Testing Wallace's intuition: water type, reproductive isolation and divergence in an Amazonian fish

Abstract

Alfred Russel Wallace proposed classifying Amazon rivers based on their colour and clarity: white, black and clear water. Wallace also proposed that black waters could mediate diversification and yield distinct fish species. Here, we bring evidence of speciation mediated by water type in the sailfin tetra (Crenuchus spilurus), a fish whose range encompasses rivers of very distinct hydrochemical conditions. Distribution of the two main lineages concords with Wallace's water types: one restricted to the acidic and nutrient-poor waters of the Negro River (herein Rio Negro lineage) and a second widespread throughout the remaining of the species' distribution (herein Amazonas lineage). These lineages occur over a very broad geographical range, suggesting that despite occurring in regions separated by thousands of kilometres, individuals of the distinct lineages fail to occupy each other's habitats, hundreds of metres apart and not separated by physical barrier. Reproductive isolation was assessed in isolated pairs exposed to black-water conditions. All pairs with at least one individual of the lineage not native to black waters showed significantly lower spawning success, suggesting that the water type affected the fitness and contributed to reproductive isolation. Our results endorse Wallace's intuition and highlight the importance of ecological factors in shaping diversity of the Amazon fish fauna.

A Review on Fish Sensory Systems and Amazon Water Types With Implications to Biodiversity

“…It has been suggested that the strikingly different limnological characteristics of the rivers, streams and other water bodies that comprise the Amazon basin are important sources of the divergent selection pressures that may have originated its remarkable fish diversity (Amado et al, 2011;Cooke et al, 2012bCooke et al, ,c, 2014Beheregaray et al, 2015;Pires et al, 2018). Although some authors have suggested the importance of speciation processes mediated by Amazon water types (Cooke et al, 2012b,c;Beheregaray et al, 2015), as far as we know only one study directly evaluated the potential for reproductive isolation among populations exposed to divergent water quality characteristics (Pires et al, 2018). Previous reviews focused on the relative importance of allopatric vs. sympatric speciation but did not explicitly consider mechanisms of speciation, being mostly restricted to the biogeography of speciation.…”

“…Many hypotheses considering different factors as evolutionary drivers of the Amazon fish biodiversity have been developed (Dagosta and de Pinna, 2018). Alfred Russell Wallace (1853) was the first to hint possible ecological reasons for Amazonian fish diversity (Pires et al, 2018). Wallace (1853) highlighted the differences of Amazon fish composition varied according to a classification based on water color (later known as water types) and suggested that those environmental differences could represent an important component of fish diversification.…”

Evidence for divergence between sympatric stone charr and Dolly Varden along unique environmental gradients in Kamchatka

“…We suggest the natural selection for an early‐life resistance to toxicosis may accelerate SC metabolism in general promote a specialization to piscivory and lay the ground for further isolation of SC from the basal DV group. Similar mechanisms were suggested to promote diversification in Amazonian fishes, that is, divergence associated with acidic and normal water (Cooke, Chao, & Beheregaray, 2012; Pires et al, 2018).…”

Natural toxic impact and thyroid signaling interplay orchestrates riverine adaptive divergence of Dolly Varden.

“…SC being resistant to the adverse effects of flavonoids and terpenoids reproduce in the coniferous forest zone, while DV has to migrate upstream to the leaf krummholz zone. This situation to some extent resembles a diversification scenario of Amazonian fishes inhabiting acidic and normal water currents(Cooke et al, 2012;Pires et al, 2018).…”