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Adaptive responses to hypoxia are likely accompanied by highly diverse changes in gene expression. Here, we examined the transcriptomic regulation in blood samples derived from independently-derived captive cave-dwelling fish. These fish are members of the speciesAstyanax mexicanus, which comprises two morphs: an obligate subterranean form, and a “surface-dwelling” form that lives in rivers and streams located near cave localities. These morphs diverged ∼20,000–200,000 years ago, and cavefish derived from multiple, distinct cave localities have adapted to life in hypoxic waters. Here, we focused on captive-rearedAstyanaxmorphs since elevated hemoglobin levels persist in cavefish despite rearing in the normoxic conditions of a laboratory. A GO enrichment analysis revealed several instances of convergent gene regulation between some, but not all, cavefish populations. This finding suggests that different gene expression patterns have evolved in response to hypoxia across geologically-distinct cave localities. Additionally, we identified differential regulation of numerous genes of the canonical hypoxic response pathway. Interestingly, some genes activating this pathway were expressed lower in captive-reared cavefish. These patterns of gene expression may have evolved in cavefish as a consequence of negative pleiotropic consequences associated with prolongedhifgene expression. At present, it is unknown whether this finding is a function of captivity, or whether these expression patterns are also present in wild populations. Collectively, this work provides new insights to the transcriptomic regulation of hypoxia tolerance using a cavefish model evolving in distinct oxygenated environments. 

ABSTRACT Cave‐dwelling animals thrive in isolated caves despite the pressures of darkness, starvation, and reduced oxygen. Prior work revealed thatAstyanaxcave‐dwelling morphs derived from different cave localities express significantly higher levels of blood hemoglobin compared to surface‐dwelling fish. Interestingly, this elevation is maintained in different populations of cavefish, despite captive rearing in normal oxygen conditions. We capitalized on the consistent response of elevated hemoglobin in captive cavefish, which were derived from geographically distinct regions, to determine if this elevation is underpinned by expression of the sameHbgenes. Blood hemoglobin proteins are encoded by a large family ofhemoglobin(Hb) gene family members, which demonstrate coordinated expression patterns, subject to various organismal (e.g., period of life history) and environmental influences (e.g., oxygen availability). Surprisingly, we found that geographically distinct populations showed mostly divergent patterns ofHbgene expression. Cavefish from two cave localities, Pachón and Tinaja, have a more recent shared origin, and show more similarHbexpression patterns as adults. However, during embryonic phases, Pachón and Tinaja show significant variability in timing of peak expression ofHbfamily members. In sum, the transcriptomic underpinnings ofHbgene expression represents a complex composite of shared and divergent expression patterns across three captive cavefish populations. We conclude that these differential patterns are likely influenced by life history, and the unique cave conditions in which these animals evolved. 

ABSTRACT The regulation of bone size is a poorly understood and complex developmental process. Evolutionary models can enable insight through interrogation of the developmental and molecular underpinnings of natural variation in bone size and shape. Here, we examine the Mexican tetra (Astyanax mexicanus), a species of teleost fish comprising of an extant river‐dwelling surface fish and obligate cave‐dwelling fish. These divergent morphs have evolved for thousands of years in drastically different habitats, which have led to diverse phenotypic differences. Among many craniofacial aberrations, cavefish harbor a wider gape, an underbite, and larger jaws compared to surface‐dwelling morphs. Morphotypes are inter‐fertile, allowing quantitative genetic analyses in F₂pedigrees derived from surface × cavefish crosses. Here, we used quantitative trait locus (QTL) analysis to determine the genetic basis of jaw size. Strikingly, we discovered a single genomic region associated with several jaw size metrics. Future work identifying genetic lesions that explain differences in jaw development will provide new insight to the mechanisms driving bone size differences across vertebrate taxa. 

Abstract Identifying the genetic factors that underlie complex traits is central to understanding the mechanistic underpinnings of evolution. Cave-dwelling Astyanax mexicanus populations are well adapted to subterranean life and many populations appear to have evolved troglomorphic traits independently, while the surface-dwelling populations can be used as a proxy for the ancestral form. Here we present a high-resolution, chromosome-level surface fish genome, enabling the first genome-wide comparison between surface fish and cavefish populations. Using this resource, we performed quantitative trait locus (QTL) mapping analyses and found new candidate genes for eye loss such as dusp26 . We used CRISPR gene editing in A. mexicanus to confirm the essential role of a gene within an eye size QTL, rx3 , in eye formation. We also generated the first genome-wide evaluation of deletion variability across cavefish populations to gain insight into this potential source of cave adaptation. The surface fish genome reference now provides a more complete resource for comparative, functional and genetic studies of drastic trait differences within a species.