Comparative transcriptome analysis of wild and lab populations of Astyanax mexicanus uncovers differential effects of environment and morphotype on gene expression

Abstract

Studying how different genotypes respond to environmental variation is essential to understand the genetic basis of adaptation. The Mexican tetra, Astyanax mexicanus, has cave and surface-dwelling morphotypes that have adapted to entirely different environments in the wild, and are now successfully maintained in lab conditions. While this has enabled the identification of genetic adaptations underlying a variety of physiological processes, few studies have directly compared morphotypes between labreared and natural populations. Such comparative approaches could help dissect the varying effects of environment and morphotype, and determine the extent to which phenomena observed in the lab are generalizable to conditions in the field. To this end, we take a transcriptomic approach to compare the Pachón cavefish and their surface fish counterparts in their natural habitats and the lab environment. We identify key changes in expression of genes implicated in metabolism and physiology between groups of fish, suggesting that morphotype (surface or cave) and environment (natural or lab) both alter gene expression. We find gene expression differences between cave and surface fish in their natural habitats are much larger than differences in expression between morphotypes in the lab environment. However, lab-raised cave and surface fish still exhibit numerous gene expression changes, supporting genetically encoded changes in livers of this species. From this, we conclude that a controlled laboratory environment may serve as an ideal setting to study the genetic underpinnings of metabolic and physiological differences between the cavefish and surface fish.

Genome-wide analysis ofcis-regulatory changes in the metabolic adaptation of cavefish

“…This was in line with our published data wherein the expression of hpdb from wild Pachón was higher than wild surface fish (Fig. 5g) (Krishnan et al, 2020). To extend this analysis we also genotyped other cavefish populations (Tinaja, Yerbaniz, Piedras, and Japonés) and found the same deletion to be fixed in all populations, except for the Japonés individual, which was heterozygous.…”

“…A decreased demand for melanin in cavefish could in principle lead to increased availability of tyrosine for other pathways. (g) hpdb RNA levels in wild-caught surface fish and Pachón cavefish livers (RNA-seq data fromKrishnan et al, 2020).…”

Resilience in a Natural Model of Metabolic Dysfunction Through Changes in Longevity and Ageing-Related Metabolites

“…Adaptation to the cave environment may have led to changes in glutathione metabolism in cavefish to protect against oxidative stress under prolonged fasting. Indeed, in an earlier study we were able to demonstrate that cavefish show an increased expression of genes that are involved in the metabolism of glutathione, which is indicative of an increased stress level compared to surface fish in their natural habitat (59). Here we can confirm the ability of cavefish to respond towards fasting mediated oxidative stress by elevation of reduced glutathione in the liver and brain (Fig 5, Table S2).…”

Astyanax surface and cave fish morphs

“…The relationship between traits expressed in the laboratory and field [ 43 ], interactions between cavefish and other cave fauna, including trophic interactions and parasitism, and the physical differences in cave ecosystems leading to adaptation are ripe for investigation. How surface fish first colonized the challenging cave environment, including the roles of standing and cryptic genetic diversity [ 44 ], phenotypic plasticity and genetic assimilation [ 45 ], and adaptive and neutral evolution [ 46 ], are also worthwhile pursuits.…”