A Comparative Transcriptomic Analysis of Development in Two Astyanax Cavefish Populations. Issue 6 (14th June 2017)

• Record Type: Journal Article
• Authors: Stahl, Bethany A.; Gross, Joshua B.
• Is Part Of: Journal of experimental zoology. Volume 328:Issue 6(2017)
• Page Start: 515
• Page End: 532
• Publication Date: 2017-06-14
• Subjects: Developmental biology -- Periodicals; Evolution (Biology) -- Periodicals; Molecular evolution -- Periodicals; Zoology -- Periodicals; Evolution, Molecular -- Periodicals; Developmental Biology -- Periodicals; Zoology -- Periodicals; 591
• DOI: 10.1002/jez.b.22749
• Languages: English
• ISSNs: 1552-5007

Abstract

GRAPHICAL ABSTRACT: The expansion of an ecological niche often exposes organisms to intense evolutionary pressures. Over 20 populations of the blind Mexican cavefish, Astyanax mexicanus, have adapted to very severe pressures, including the complete absence of sunlight and near absence of food. Despite this unwelcoming environment, these animals have repeatedly invaded the subterranean environment, providing a powerful opportunity to evaluate how and why certain gene expression patterns evolve following colonization of the dark cave environment. We discovered both shared and unique changes in expression by evaluating two ancient, but distinct, cavefish populations. This work provides insight to both the precise genes involved in cave adaptation and how genetic mechanisms operate during adaptation to extreme environments. ABSTRACT: Organisms that are isolated into extreme environments often evolve extreme phenotypes. However, global patterns of dynamic gene expression changes that accompany dramatic environmental changes remain largely unknown. The blind Mexican cavefish, Astyanax mexicanus, has evolved a number of severe cave‐associated phenotypes including loss of vision and pigmentation, craniofacial bone fusions, increased fat storage, reduced sleep, and amplified nonvisual sensory systems. Interestingly, surface‐dwelling forms have repeatedly entered different caves throughout Mexico, providing a natural set of "replicate" instances of cave isolation. These surrogate "ancestral" surface‐dwelling forms persist in nearby rivers, enabling direct comparisons to the "derived" cave‐dwelling form. We evaluated changes associated with subterranean isolation by measuring differential gene expression in two geographically distinct cave‐dwelling populations (Pachón and Tinaja). To understand the impact of these expression changes on development, we performed RNA‐sequencing across four critical stages during which troglomorphic traits first appear in cavefish embryos. Gene ontology (GO) studies revealed similar functional profiles evolved in both independent cave lineages. However, enrichment studies indicated that similar GO profiles were occasionally mediated by different genes. Certain "master" regulators, such as Otx2 and Mitf, appear to be important loci for cave adaptation, as remarkably similar patterns of expression were identified in both independent cave lineages. This work reveals that adaptation to an extreme environment, in two distinct cavefish lineages, evolves through a combination of unique and shared gene expression patterns. Shared expression profiles reflect common environmental pressures, while unique expression likely reflects the fact that similar adaptive traits evolve through diverse genetic mechanisms.