Subterranean life: Behavior, metabolic, and some other adaptations of Astyanax cavefish

Abstract

The ability of fishes to adapt to any aquatic environment seems limitless. It is enthralling how new species keep appearing at the deep sea or in subterranean environments. There are close to 230 known species of cavefishes, still today the best-known cavefish is Astyanax mexicanus, a Characid that has become a model organism, and has been studied and scrutinized since 1936. There are two morphotypes for A. mexicanus, a surface fish and a cavefish. The surface fish lives in central and northeastern Mexico and south of the United States, while the cavefish is endemic to the "Sierra del Abra-Tanchipa region" in northeast Mexico. The extensive genetic and genomic analysis depicts a complex origin for Astyanax cavefish, with multiple cave invasions and persistent gene flow among cave populations. The surface founder population prevails in the same region where the caves are. In this review, we focus on both morphotype's main morphological and physiological differences, but mainly in recent discoveries about behavioral and metabolic adaptations for subterranean life. These traits may not be as obvious as the troglomorphic characteristics, but are key to understand how Astyanax cavefish thrives in this environment of perpetual darkness.

Odor-gated oviposition behavior in an ecological specialist

“…Divergence of many traits can potentially lead to reproductive isolation and ultimately speciation, making niche specialization a likely driver of biodiversity (Caillaud and Via, 2000;Rundle and Nosil, 2005; Seehausen, 2006). Many striking examples of adaptations to new niches are known, from the rapid evolution of beak morphology of Darwin's finches as they radiated across the Galápagos archipelago (Grant and Grant, 2005) to visual system loss in Mexican tetra (Astyanax mexicanus, blind cave fish) in cave dwellings in the Gulf of Mexico and Rio Grande (Maldonado et al, 2020). While candidate genomic regions and genes have been implicated in some of these adaptations (e.g., (Abzhanov et al, 2004;Lamichhaney et al, 2015)), the restricted genetic tractability of these speciesand most other examples in naturelimits our understanding of the mechanistic basis of evolutionary adaptations.The fly Drosophila sechellia provides an exceptional model to investigate the genetic and cellular basis of niche adaptation (Auer et al, 2021;Jones, 2005;Stensmyr, 2009).…”

White epaxial muscle aerobic and anaerobic potential and muscle fiber structure in surface and cave morphotypes of the Mexican cavefish (Astyanax mexicanus)

“…Others have found a significant increase in muscle fiber cross‐sectional area in lab‐reared cave morphotypes compared with surface morphotypes (Olsen et al, 2023), however, our methods for determining muscle fiber size and Olsen et al (2023) are different. For cave morphotypes, a selective advantage for decreasing metabolic costs may be associated with their low O 2 and nutrient environment (Boggs & Gross, 2021; Maldonado et al, 2020), and increased concentration of glycogen (Olsen et al, 2023).…”

“…A powerful model system for exploring physiological adaptations to extreme environments is the Mexican cavefish, Astyanax mexicanus (Tabin et al, 2018). This species has two morphotypes: a surface form that lives in a more thermally variable river environment, and an obligate cave‐dwelling form that lives in thermally insulated caves (Boggs & Gross, 2021; Jeffery, 2001; Maldonado et al, 2020; Protas & Jeffery, 2012). Additionally, the two morphotypes of Astyanax mexicanus colonize vastly different O 2 environments, with cave morphotypes having evolved in lower‐O 2 subterranean environments, and surface morphotypes living in higher‐O 2 environments (Boggs & Gross, 2021; Maldonado et al, 2020).…”

“…This species has two morphotypes: a surface form that lives in a more thermally variable river environment, and an obligate cave‐dwelling form that lives in thermally insulated caves (Boggs & Gross, 2021; Jeffery, 2001; Maldonado et al, 2020; Protas & Jeffery, 2012). Additionally, the two morphotypes of Astyanax mexicanus colonize vastly different O 2 environments, with cave morphotypes having evolved in lower‐O 2 subterranean environments, and surface morphotypes living in higher‐O 2 environments (Boggs & Gross, 2021; Maldonado et al, 2020). As environment can determine physiological adaptations, it is of interest to compare the aerobic and anaerobic metabolic profiles of white muscle metabolism in this species.…”

A chromosome level genome ofAstyanax mexicanussurface fish for comparing population-specific genetic differences contributing to trait evolution

“…The ecology of surface and cave environments differ dramatically, allowing for functional and genomic comparisons between populations that have evolved in distinct environments. Dozens of evolved trait differences have been identified in cavefish including changes in morphology, physiology, and behavior 4, 6 . It is also worth noting that comparing cavefish to surface fish reveals substantial differences in many traits of possible relevance to human disease, including sleep duration, circadian rhythmicity, anxiety, aggression, heart regeneration, eye and retina development, craniofacial structure, insulin resistance, appetite, and obesity 7–17 .…”