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

Corine M Van Der Weele,William R Jeffery

doi:10.7554/elife.69109

Abstract

Dark caves lacking primary productivity can expose subterranean animals to hypoxia. We used the surface-dwelling (surface fish) and cave-dwelling (cavefish) morphs of Astyanax mexicanus as a model for understanding the mechanisms of hypoxia tolerance in the cave environment. Primitive hematopoiesis, which is restricted to the posterior lateral mesoderm in other teleosts, also occurs in the anterior lateral mesoderm in Astyanax, potentially pre-adapting surface fish for hypoxic cave colonization. Cavefish have enlarged both hematopoietic domains and develop more erythrocytes than surface fish, which are required for normal development in both morphs. Laboratory-induced hypoxia suppresses growth in surface fish but not in cavefish. Both morphs respond to hypoxia by overexpressing hypoxia-inducible factor 1 (hif1) pathway genes, and some hif1 genes are constitutively upregulated in normoxic cavefish to similar levels as in hypoxic surface fish. We conclude that cavefish cope with hypoxia by increasing erythrocyte development and constitutive hif1 gene overexpression.

Highlights

A unifying theme of cave habitats is complete darkness (Culver and Pipan, 2009) and the absence of primary productivity can subject cave-dwelling animals to oxygen deficiency (Malard and Hervant, 1999)
Astyanax mexicanus cavefish cope with hypoxic environments by expanding embryonic hematopoietic domains, increasing the capacity for erythrocyte development, and constitutive overexpression of hypoxia-inducible genes
Primitive hematopoiesis, which is restricted to the posterior lateral mesoderm in other teleosts, occurs in the anterior lateral mesoderm in Astyanax, potentially pre-adapting surface fish for hypoxic cave colonization

Summary

Introduction

A unifying theme of cave habitats is complete darkness (Culver and Pipan, 2009) and the absence of primary productivity can subject cave-dwelling animals to oxygen deficiency (Malard and Hervant, 1999). We have used the teleost Astyanax mexicanus, which consists of surfacedwelling (surface fish) and cave-dwelling (cavefish) morphs, as a model to study adaptation to hypoxia in caves. Surface fish colonized subterranean waters in the Sierra de El Abra region of Mexico (Mitchell et al, 1977; Gross, 2012) during the late Pleistocene (Fumey et al, 2018; Herman et al, 2018), and their cavefish descendants evolved numerous traits for adaptation to perpetual darkness. Hypoxia may be a deterrent to the survival of colonizing teleosts in the Sierra de El Abra, where oxygen reductions of 50% or more have been measured in cave waters (Boggs and Gross, 2021; Rohner et al, 2013, Ornelas-Garcia et al, 2018). Astyanax cavefish thrive under these conditions, but little is known about how they have adapted to hypo-oxygenated waters

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