Genomic signature of shifts in selection and alkaline adaptation in highland fish

Abstract

Understanding how organisms adapt to aquatic life at high altitude is fundamental in evolutionary biology. This objective has been addressed mainly related to hypoxia adaptation by recent comparative studies, whereas highland fish has also long suffered extreme alkaline environment, insight into the genomic basis of alkaline adaptation has rarely been provided. Here, we compared the genomes or transcriptomes of 15 fish species, including two alkaline tolerant highland fish species and their six alkaline intolerant relatives, three alkaline tolerant lowland fish species and four alkaline intolerant relatives. We found putatively consistent patterns of molecular evolution in alkaline tolerant species in a large number of shared orthologs within highland and lowland fish taxa. Remarkably, we identified consistent signatures of accelerated evolution and positive selection in a set of core shared genes associated with ion transport, apoptosis, immune response and energy metabolisms in alkaline tolerant species within both highland and lowland fish taxa. This is one of the first comparative studies that began to elucidate the consistent genomic signature of alkaline adaptation shared by highland and lowland fish. This finding also highlights the adaptive molecular evolution changes that support fish adapting to extreme environments at high altitude.Significance StatementLittle is known about how wild fish responds to extreme alkaline stress besides hypoxia at high altitude. Comparative genomics has begun to elucidate the genomic basis of alkaline adaptation in lowland fish, such as killifish, but insight from highland fish has lagged behind. The common role of adaptive molecular evolution during alkaline adaptation in highland and lowland fish has rarely been discussed. We address this question by comparing 15 fish omics data. We find numbers of shared orthologs exhibited consistent patterns of molecular evolution in alkaline tolerant species relative to intolerant species. We further identify remarkably consistent signatures of rapidly evolving and positive selection in a substantial shared core of genes in both highland and lowland alkaline tolerant species.

Convergent genomic signatures of adaptation to an extreme environment in cyprinoid fishes

“…Extreme environments have disruptive effects on endocrine system of fish, can interfer their reproductive functions (Wang and Guo 2019). Notably, extremophile fish G. przwalskii and L. waleckii are both anadromous and migrate to spawn in rivers (freshwater) (Tong et al 2017; Xu et al 2017; Tong et al 2021). Reproduction in most anadromous fishes is a seasonal phenomenon to ensure the survival of their offsprings, which fish experienced the transition from saline or alkaline water to freshwater (Tian et al 2019).…”

“…Thus, extremophile fish require enhanced physiological abilities including ion transport, osmoregulation, and acid-base balance to respond the increase in salinity and alkalinity of freshwater (Evans et al 2005; Marshall 2005). Past studies, including ours, have identified key genes associated with osmoregulation and ion transport in G. przwalskii and L. waleckii under rapid evolving (aka., acceleration) and positive selection (Tong et al 2017; Xu et al 2017; Tong and Li 2020; Tong et al 2021). Consistently, we identified a substantial set of ion transport, osmoregulation, and acid-base balancerelated genes are under convergent selection in both extremophile fish lineages.…”

“…Extremely saline and alkaline stress may cause extensive damage to fish immune system (Bowden 2008; Sridhar et al 2020). In G. przwalskii , our previous genome-wide studies had identified a set of immune-related genes that experienced rapidly evolving or positive selection (Tong et al 2017; Tong and Li 2019; Tong et al 2021), while there is no signal of selections on immune-related genes in L. waleckii (Xu et al 2017). Although previous studies seem to suggest inconsistent patterns of molecular evolution on immune-related genes in extremophile fish adaptation to extreme environment, our present study provide the evidence of molecular convergence on immune-related genes in both fish lineages relative to other freshwater cyprinoid fishes.…”

“…Notably, both extremophile fish survive in freshwater of connective rivers during the spawning migration (Tong et al 2017; Xu et al 2017). For this, several recent genome-wide studies, including ours, have reported the evolutionary changes associated with hypersaline or hyperalkaline adaptations in a single extremophile fish relative to other phylogenetically distant teleost fish species (Tong et al 2017; Xu et al 2017; Tong and Li 2020; Tong et al 2021). However, how phylogenetic background contributes to convergent adaptation to extremely saline or alkaline environments is largely unclear, in particular in a group of cyprinoid fishes.…”

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

“…Although the effects of these extreme environmental factors on the reproduction and growth of freshwater fish are lethal, several fish can naturally survive in alkaline-saline lakes. Therefore, the adaptive evolutionary mechanism of these recurring alkaline-adaptive fish has long been of interest to evolutionary biologists [9][10][11] . Generally, to avoid elevated blood pH due to respiratory alkalosis in alkaline-saline lakes, teleosts regulate the blood pH through reversible CO 2 hydration/dehydration reactions catalysed by carbonic anhydrase (CAs) 12 .…”