Genomic insights into the adaptive and convergent evolution of Leuciscus waleckii inhabiting extremely alkaline environments

Abstract

Leuciscus waleckii is widely distributed in Northeast Asia and has high economic value. Different from its freshwater counterparts, the population in Lake Dali Nur has a strong alkalinity tolerance and can adapt to extremely alkaline-saline water with bicarbonate over 50 mmol/L (pH 9.6), thus providing an exceptional model with which to explore the mechanisms of adaptive evolution under extreme alkaline environments. Here, we assembled a high quilty chromosome-level reference genome for L. waleckii from Lake Dali Nur, which provides an important genomic resource for the exploitation of alkaline water fishery resources and adaptive evolution research across teleost fish. Notably, we identified significantly expanded long terminal repeats (LTRs) and long interspersed nuclear elements (LINEs) in L. waleckii compared to other Cypriniformes fish, suggesting their more recent insertion into the L. waleckii genome. We also identified expansions in genes encoding gamma-glutamyltransferase, which possibly underlie the adaptation to extreme environmental stress. Based on the resequencing of 85 L.waleckii individuals from divergent populations, the historical population size of L.waleckii in Lake Dali Nur dramatically expanded in a thousand years approximately 13,000 years ago, and experienced a cliff recession in the process of adapting to the alkaline environment of Lake Dali Nur approximately 6,000 years ago. Genome scans further revealed the significant selective sweep regions from Lake Dali Nur, which harbour a set of candidate genes involved in hypoxia tolerance, ion transport, acid-base regulation and nitrogen metabolism. In particular, 5 alkali population specific nonsynonymous mutations were identified in CA15 gene copies. In addition, two sites with convergent amino acid mutation were detected in the RHCG-a gene among several alkali environment adapted Cypriniformes fish, this mutation may increase the NH3 excretion rate of the RHCG channel. Our findings provide comprehensive insight into the genomic mechanisms of L. waleckii and reveal their adaptative evolution under extreme alkaline environments.