Dark‐rearing uncovers novel gene expression patterns in an obligate cave‐dwelling fish

Abstract

Extreme environments often result in the evolution of dramatic adaptive features. The Mexican tetra, Astyanax mexicanus, includes 30 different populations of cavedwelling forms that live in perpetual darkness. As a consequence, many populations have evolved eye loss, reduced pigmentation, and amplification of nonvisual sensory systems. Closely-related surface-dwelling morphs demonstrate typical vision, pigmentation, and sensation. Transcriptomic assessments in this system have revealed important developmental changes associated with the cave morph, however, they have not accounted for photic rearing conditions. Prior studies reared individuals under a 12:12 hr light/dark (LD) cycle. Here, we reared cavefish under constant darkness (DD) for 5+ years. From these experimental individuals, we performed mRNA sequencing and compared gene expression of surface fish reared under LD conditions to cavefish reared under DD conditions to identify photic-dependent gene expression differences. Gene Ontology enrichment analyses revealed a number of previously underappreciated cave-associated changes impacting blood physiology and olfaction. We further evaluated the position of differentially expressed genes relative to QTL positions from prior studies and found several candidate genes associated with these ecologically relevant lighting conditions. In sum, this work highlights photic conditions as a key environmental factor impacting gene expression patterns in blind cave-dwelling fish.

Cavefish cope with environmental hypoxia by developing more erythrocytes and overexpression of hypoxia-inducible genes

“…Nevertheless, we also found stronger expression of erythropoietic marker genes in the AGM and caudal hematopoietic tissue, which are involved in definitive hematopoiesis, implying that the second wave may also be expanded in cavefish. Further investigation will be required to determine whether erythrocytes are also increased in adults, although this possibility seems likely because adult cavefish have increased levels of hemoglobin transcripts ( Sears et al, 2020 ) and more erythrocytes in their head kidneys compared to surface fish ( Peuß et al, 2020 ). We conclude that cavefish have evolved a permanent enhancement in red blood cells as a potential adaptation for survival in hypoxic cave waters.…”

Adaptations to Subterranean Environments

“…The investigation of genes responsible for phenotypic adaptations in obligate cavefishes (A. mexicanus, S. typhlops, and S. anshuiensis) has revealed that different genetic mechanisms can lead to "many ways to build a cavefish, " as suggested in previous studies (Sears et al, 2020;Policarpo et al, 2021;Van der Weele and Jeffery, 2022). However, the identification of 73 shared genes between S. typhlops and other cavefishes suggests that molecular convergence also plays a significant role in cave adaptation, as previously observed in the Oca2 gene associated with the albinism phenotype in vertebrates (Protas et al, 2006); note that we were unable to retrieve Oca2 from S. typhlops.…”

Transcriptomic analysis of the Brazilian blind characid, Stygichthys typhlops, reveals convergent selection with Astyanax mexicanus and other cavefishes

“…The investigation of genes responsible for phenotypic adaptations in obligate cavefishes (A. mexicanus, S. typhlops, and S. anshuiensis) has revealed that different genetic mechanisms can lead to "many ways to build a cavefish, " as suggested in previous studies (Sears et al, 2020;Policarpo et al, 2021;Van der Weele and Jeffery, 2022). However, the identification of 73 shared genes between S. typhlops and other cavefishes suggests that molecular convergence also plays a significant role in cave adaptation, as previously observed in the Oca2 gene associated with the albinism phenotype in vertebrates (Protas et al, 2006); note that we were unable to retrieve Oca2 from S. typhlops.…”