Elevated Blood Hemoglobin in Different Cavefish Populations Evolves Through Diverse Hemoglobin Gene Expression Patterns

Cave-dwelling animals thrive in isolated caves despite the pressures of darkness, starvation, and reduced oxygen. Prior work revealed that Astyanax cave-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 same Hb genes. Blood hemoglobin proteins are encoded by a large family of hemoglobin (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 of Hb gene expression. Cavefish from two cave localities, Pachón and Tinaja, have a more recent shared origin, and show more similar Hb expression patterns as adults. However, during embryonic phases, Pachón and Tinaja show significant variability in timing of peak expression of Hb family members. In sum, the transcriptomic underpinnings of Hb gene 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.