Genomic Basis of Adaptive Evolution: The Survival of Amur Ide (Leuciscuswaleckii) in an Extremely Alkaline Environment

Abstract

The Amur ide (Leuciscus waleckii) is a cyprinid fish that is widely distributed in Northeast Asia. The Lake Dali Nur population inhabits one of the most extreme aquatic environments on Earth, with an alkalinity up to 50 mmol/L (pH 9.6), thus providing an exceptional model with which to characterize the mechanisms of genomic evolution underlying adaptation to extreme environments. Here, we developed the reference genome assembly for L. waleckii from Lake Dali Nur. Intriguingly, we identified unusual expanded long terminal repeats (LTRs) with higher nucleotide substitution rates than in many other teleosts, suggesting their more recent insertion into the L. waleckii genome. We also identified expansions in genes encoding egg coat proteins and natriuretic peptide receptors, possibly underlying the adaptation to extreme environmental stress. We further sequenced the genomes of 10 additional individuals from freshwater and 18 from Lake Dali Nur populations, and we detected a total of 7.6 million SNPs from both populations. In a genome scan and comparison of these two populations, we identified a set of genomic regions under selective sweeps that harbor genes involved in ion homoeostasis, acid-base regulation, unfolded protein response, reactive oxygen species elimination, and urea excretion. Our findings provide comprehensive insight into the genomic mechanisms of teleost fish that underlie their adaptation to extreme alkaline environments.

Genomic signature of ongoing alkaline adaptation in a Schizothoracine fish (Cyprinidae) inhabiting soda lake on the Tibetan Plateau

“…In this study, we identified a bunch of both REGs and PSGs repertoires involved in ion transport process in G. p. kelukehuensis, including the members from solute carrier (SLC) family and transmembrane protein (TMEM) family. This finding is similar to the recent studies of species dwelt in alkaline environment (Xu et al 2017;Tong, Fei, et al 2017). SLC is a super family that encoded transmembrane transporters for inorganic ions, amino acids, neurotransmitters, sugars, purines and fatty acids, and other solute substrates (Dorwart et al 2008).…”

“…We identified a large number of lineage-specific genes associated with ion transport processes in G. p. kelukehuensis, such as water transport, response to pH and monovalent inorganic cation transport, indicating this set of genes showed the putative signature of gene family expansion. This result was consistent with findings in Amur ide that dwelt in an alkaline environment in Lake Dali Nur (Xu et al 2017) and another Schizothoracine fish living in saline lake Qinghai (Tong, Fei, et al 2017), indicating that the alkaline environment of Lake Keluku, Lake Dali Nur and Lake Qinghai spurred evolution and expansion of genes in ion transport function. In this study, we identified a bunch of both REGs and PSGs repertoires involved in ion transport process in G. p. kelukehuensis, including the members from solute carrier (SLC) family and transmembrane protein (TMEM) family.…”

“…SLC is a super family that encoded transmembrane transporters for inorganic ions, amino acids, neurotransmitters, sugars, purines and fatty acids, and other solute substrates (Dorwart et al 2008). Recent studies suggested that the adaptive evolution of SLC genes could contribute to saline and alkaline tolerance in fishes (Xu et al 2017;Dorwart et al 2008;Kavembe et al 2015). Such as SLC4 subfamily, it encodes bicarbonate-transporter and regulated of Cl − -HCO 3 − exchange and plays significant roles in maintenance of intracellular pH equilibrium (Pushkin & Kurtz 2006;Alper 2006).…”

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

“…Water pH is another factor that has been shown to influence several physiological aspects of fish, either at gene expression and other biochemical levels (e.g. Jesus et al 2017;Xu et al 2017;Jesus et al 2018). Thus, water pH my act as a selective pressure, specifically an increased alkalinity (i.e.…”

Comparative genomics identifies putative signatures of sociality in spiders

“…A major goal of evolutionary biology is to elucidate the genomic underpinnings of phenotypic innovations across the tree of life. Over the past decade, comparative genomics has been used as a powerful tool to begin to elucidate the genetic basis of phenotypic innovations and adaptation in a wide range of organisms (Xu et al 2017;Gou et al 2014;Zhang et al 2014;Chen et al 2019;Exposito-Alonso et al 2018;Gaither et al 2018;Goodman et al 2009;Wang et al 2019;Wu et al 2014). These studies have often identified changes in gene repertoire (e.g., expansions of certain gene families) or genomic signatures of molecular evolution at orthologous genes, by comparing the genomes of species with and without a phenotype of interest (Xu et al 2017;Gou et al 2014;Gaither et al 2018;Goodman et al 2009;Wang et al 2019;Wu et al 2014).…”