Multifactorial genetic divergence processes drive the onset of speciation in an Amazonian fish

Abstract

Understanding the processes that drive population genetic divergence in the Amazon is challenging because of the vast scale, the environmental richness and the outstanding biodiversity of the region. We addressed this issue by determining the genetic structure of the widespread Amazonian common sardine fish Triportheus albus (Characidae). We then examined the influence, on this species, of all previously proposed population-structuring factors, including isolation-by-distance, isolation-by-barrier (the Teotônio Falls) and isolation-by-environment using variables that describe floodplain and water characteristics. The population genetics analyses revealed an unusually strong structure with three geographical groups: Negro/Tapajós rivers, Lower Madeira/Central Amazon, and Upper Madeira. Distance-based redundancy analyses showed that the optimal model for explaining the extreme genetic structure contains all proposed structuring factors and accounts for up to 70% of the genetic structure. We further quantified the contribution of each factor via a variance-partitioning analysis. Our results demonstrate that multiple factors, often proposed as individual drivers of population divergence, have acted in conjunction to divide T. albus into three genetic lineages. Because the conjunction of multiple long-standing population-structuring processes may lead to population reproductive isolation, that is, the onset of speciation, we suggest that the multifactorial population-structuring processes highlighted in this study could account for the high speciation rate characterising the Amazon Basin.

The role of the Andean uplift as an asymmetrical barrier to gene flow in the Neotropical leaf-cutting antAtta cephalotes

“…Despite the strong evidence for the Andes mountains as driver of regional differentiation in A. cephalotes’ populations, we also found evidence for isolation by distance, which makes the interpretation of underlying mechanisms of isolation more difficult to interpret (Crispo, Bentzen, Reznick, Kinnison, & Hendry, 2006; Edwards, Keogh, & Knowles, 2012; Wang et al, 2013). We further investigated both alternative mechanisms of genetic isolation through a db-RDA and model selection approaches (De Queiroz et al, 2017; James et al, 2011; McGaughran, Morgan, & Sommer, 2014; Meirmans, 2015), indicating that both isolating mechanisms have significantly restricted gene flow in A. cephalotes populations. The IBB model remains significant after accounting for IBD, which strongly suggest a substantial role of this isolating mechanism in A. cephalotes .…”

“…The IBB model remains significant after accounting for IBD, which strongly suggest a substantial role of this isolating mechanism in A. cephalotes . However, a combined multifactorial effect of both mechanisms was observed, which seems to be a common pattern for heterogenic landscapes (De Queiroz et al, 2017; Guarnizo & Cannatella, 2014; McGaughran et al, 2014; Noguerales et al, 2016), where multiple factors can affect different sections of the species’ range, making it difficult to disentangle their contributions (Crispo et al, 2006; Wang et al, 2013). The Andes ranges in Colombia seem to drive a North-South genetic differentiation in A. cephalotes , but geographical distance still has a similar impact within regions on both sides of these mountains.…”

“…To test for isolation by distance (IBD), pairwise geographical distances expressed as a distance matrix were transformed into a vector format (De Queiroz, Torrente-Vilara, Quilodran, da Costa Doria, & Montoya-Burgos, 2017; Noguerales, Cordero, & Ortego, 2016) using the ‘ pcnm’ function in the R package VEGAN v.2.2.0 (Oksanen et al, 2019). Then, spatial explanatory components were tested through a db-RDA analysis and only the significant explanatory PCNM components were retained.…”

Osmoregulation in freshwaters: Gene expression in the gills of a Neotropical cichlid in contrasting pH and ionic environments

“…An RNA-seq study of an Amazonian characin, Triportheus albus , from rivers of different water types observed differential expression in a number of these same transporters [72]. While this study is not directly comparable because experimental subjects were surveyed in situ , and it is unclear whether observed expression differences result from plasticity or population-specific, constitutive expression [i.e., 14], these similarities suggest that acclimation to physicochemical challenges, and potentially also adaptation, utilize many of the same mechanisms to cope with ionic gradients of significant magnitude largely regardless of the relative tonicity of environment to body fluids [73]. In addition, our observations of several examples of contrasting expression of fish-specific paralogs of genes with known importance in human osmoregulation indicates the importance of functional diversification of these gene families in fishes for transitions among habitats with distinct physicochemistry [39].…”

“…Despite the ionoregulatory challenges posed by blackwaters, over a thousand species are known to inhabit the Negro sub-basin of the Amazon [11], the largest blackwater drainage basin in the world (Supplemental Figure 1). Approximately two thirds of Amazon species seem to be found in only a single water type [12,13], but many closely related species show complementary distributions across water types, indicating that adaptation to water type may be an important driver of fish diversity [14]. Most research on osmoregulation in Neotropical fishes has focused on broadly or seasonally eurytopic fishes (those that occur in both water types) or contrasts among species endemic to a single water type (stenotopic).…”