Phylogeography of a Typical Forest Heliothermic Lizard Reveals the Combined Influence of Rivers and Climate Dynamics on Diversification in Eastern Amazonia

Abstract

The formation of the Amazon drainage basin has been considered an important driver of speciation of several taxa, promoting vicariant events or reinforcement of barriers that restrict gene flow between opposite river margins. Several recent studies reported a set of miscellaneous events involving climatic fluctuations, geomorphological changes, and dispersal mechanisms as propellers of diversification of Amazonian rainforest taxa. Here, we show the results of dated phylogenetic, biogeographic, and populational analyses to investigate which events could better explain the current distribution of a heliothermic, active foraging lizard in the central and eastern portions of the Amazonian rainforest (besides a disjunct distribution in part of the Atlantic Forest). We sampled Kentropyx calcarata from most of its area of occurrence in Amazonia and used mitochondrial and nuclear markers to evaluate if the genetic structure agrees with evolutionary scenarios previously proposed for Amazonia. We performed phylogenetic and populational analyses to better understand the dynamics of this species in the Amazonia rainforest over time. Phylogenetic inference recovered ten K. calcarata structured lineages in eastern Amazonia, some of them limited by the Amazon River and its southern tributaries (Tapajós, Xingu, and Tocantins), although we detected occasional haplotype sharing across some of the river banks. According to molecular dating, K. calcarata diversified since Miocene–Pliocene, and some of the lineages presented signs of demographic expansion during the Pleistocene, supposedly triggered by climatic dynamics. The putative ancestral lineage of K. calcarata was distributed on the Guiana Shield, later spreading south and southeastward by dispersion. Our results indicate that Amazonian rivers acted as barriers to the dispersal of Kentropyx calcarata, but they were not the sole drivers of diversification.

Deforestation limits evolutionary rescue under climate change in Amazonian lizards

“…Like previous studies using mtDNA data 50,51 , our genomic-level data indicates that K. calcarata presents geographically structured populations, associated to major inter uves in the transition zones between Amazonia and the Cerrado, as well as an isolated population in the Atlantic Forest (Fig. 1).…”

“…The distribution of K. calcarata mostly in eastern Amazonia may explain the dominance of the dry/seasonal genotype relative to the wet/non-seasonal one. Previous studies integrating mtDNA phylogeographic structure, thermal physiology, and mechanistic distribution modelling of K. calcarata have shown a degree of thermal tolerance at the Amazonia-Cerrado ecotone, suggesting adaptation to intense climatic selective pressures 30,50,51 , coincident with the distribution of the dominant dry/seasonal genotype. Although the current rate of environmental changes may require species to adapt or speciate faster than documented in evolutionary studies 52 , our results indicate that, at least for some species, the presence of standing genetic variation and local adaptation related to such climate gradient that could facilitate adaptation processes.…”

Whole genomes show contrasting trends of population size changes and genomic diversity for an Amazonian endemic passerine over the late quaternary

“…According to this model, older lineages in the wetter western and northern parts of the basin gave rise to younger lineages in the drier southern and eastern parts over the past 2 million years, likely owing to greater climatic instability in the southeastern part of the basin (Silva et al., 2019 ). This and other studies concluded that although Amazonian rivers do represent important barriers to gene flow and contribute to speciation, historical oscillations in the steep regional moisture gradient have played a key role in directing the spatio‐temporal sequence of splits across different lineages and rivers (Cronemberger et al., 2022 ; Dornas et al., 2022 ; Silva et al., 2019 ; Weir et al., 2015 ). Therefore, climate and the physical landscape interacted at a continental scale to generate the current species richness and distribution patterns in the Amazon (Godinho & da Silva, 2018 ; Oberdorff et al., 2019 ; Ritter et al., 2019 ; Silva et al., 2019 ; Tuomisto et al., 2019 ; Weir et al., 2015 ).…”