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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. 

Animals inhabiting subterranean environments tend to evolve a constellation of ‘regressive’ and ‘constructive’ features. Regressive traits like vision and pigmentation are reduced or lost in derived organisms. In contrast, constructive traits like non-visual sensation, are commonly augmented and evolving under strong selection. Numerous studies have examined the genetic, developmental and molecular bases for regressive traits, while constructive traits have received less attention. A key constructive sensory feature in cave animals is the gustatory system which is likely useful for animals living in complete darkness, given the need to secure food for survival. Interestingly, despite having been studied for decades in the Mexican tetra, Astyanax mexicanus , much remains unknown regarding the biological basis, and adaptive relevance, of taste system evolution in cave morphs. Here, we present a brief review of taste system research in this system, conducted over the past ~90  years. We underscore key differences in gustation between cave and surface fish that reside at the levels of anatomy, perception and behavior. From this review, we sought to identify key knowledge gaps in our understanding of constructive taste system evolution. Future studies will provide further insights to the nature of constructive trait evolution by determining if constructive and regressive traits evolve through similar or different genetic and developmental mechanisms, and provide an essential case study for examining convergence of constructive traits across geographically distinct populations. 

The biological basis of lateralized cranial aberrations can be rooted in early asymmetric patterning of developmental tissues. However, precisely how development impacts natural cranial asymmetries remains incompletely understood. Here, we examined embryonic patterning of the cranial neural crest at two phases of embryonic development in a natural animal system with two morphotypes: cave-dwelling and surface-dwelling fish. Surface fish are highly symmetric with respect to cranial form at adulthood, however adult cavefish harbor diverse cranial asymmetries. To examine if lateralized aberrations of the developing neural crest underpin these asymmetries, we used an automated technique to quantify the area and expression level of cranial neural crest markers on the left and right sides of the embryonic head. We examined the expression of marker genes encoding both structural proteins and transcription factors at two key stages of development: 36 hpf (∼mid-migration of the neural crest) and 72 hpf (∼early differentiation of neural crest derivatives). Interestingly, our results revealed asymmetric biases at both phases of development in both morphotypes, however consistent lateral biases were less common in surface fish as development progressed. Additionally, this work provides the information on neural crest development, based on whole-mount expression patterns of 19 genes, between stage-matched cave and surface morphs. Further, this study revealed ‘asymmetric’ noise as a likely normative component of early neural crest development in natural Astyanax fish. Mature cranial asymmetries in cave morphs may arise from persistence of asymmetric processes during development, or as a function of asymmetric processes occurring later in the life history. 

Abstract Laboratory studies have demonstrated that a single phenotype can be produced by many different genotypes; however, in natural systems, it is frequently found that phenotypic convergence is due to parallel genetic changes. This suggests a substantial role for constraint and determinism in evolution and indicates that certain mutations are more likely to contribute to phenotypic evolution. Here we use whole genome resequencing in the Mexican tetra,Astyanax mexicanus, to investigate how selection has shaped the repeated evolution of both trait loss and enhancement across independent cavefish lineages. We show that selection on standing genetic variation and de novo mutations both contribute substantially to repeated adaptation. Our findings provide empirical support for the hypothesis that genes with larger mutational targets are more likely to be the substrate of repeated evolution and indicate that features of the cave environment may impact the rate at which mutations occur. 

The genus Sinocyclocheilus , comprising a large radiation of freshwater cavefishes, are well known for their presence of regressive features (e.g. variable eye reduction). Fewer constructive features are known, such as the expansion of the lateral line system (LLS), which is involved in detecting water movements. The precise relationship between LLS expansion and cave adaptation is not well understood. Here, we examine morphology and LLS-mediated behaviour in Sinocyclocheilus species characterized by broad variation in eye size, habitat and geographical distribution. Using live-staining techniques and automated behavioural analyses, we examined 26 Sinocyclocheilus species and quantified neuromast organ number, density and asymmetry within a phylogenetic context. We then examined how these morphological features may relate to wall-following, an established cave-associated behaviour mediated by the lateral line. We show that most species demonstrated laterality (i.e. asymmetry) in neuromast organs on the head, often biased to the right. We also found that wall-following behaviour was distinctive, particularly among eyeless species. Patterns of variation in LLS appear to correlate with the degree of eye loss, as well as geographical distribution. This work reveals that constructive LLS evolution is convergent across distant cavefish taxa and may mediate asymmetric behavioural features that enable survival in stark subterranean microenvironments. 

Cave animals are a fascinating group of species often demonstrating characteristics including reduced eyes and pigmentation, metabolic efficiency, and enhanced sensory systems. Asellus aquaticus, an isopod crustacean, is an emerging model for cave biology. Cave and surface forms of this species differ in many characteristics, including eye size, pigmentation, and antennal length. Existing resources for this species include a linkage map, mapped regions responsible for eye and pigmentation traits, sequenced adult transcriptomes, and comparative embryological descriptions of the surface and cave forms. Our ultimate goal is to identify genes and mutations responsible for the differences between the cave and surface forms. To advance this goal, we decided to use a transcriptomic approach. Because many of these changes first appear during embryonic development, we sequenced embryonic transcriptomes of cave, surface, and hybrid individuals at the stage when eyes and pigment become evident in the surface form. We generated a cave, a surface, a hybrid, and an integrated transcriptome to identify differentially expressed genes in the cave and surface forms. Additionally, we identified genes with allele-specific expression in hybrid individuals. These embryonic transcriptomes are an important resource to assist in our ultimate goal of determining the genetic underpinnings of the divergence between the cave and surface forms.