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The ability of organisms to adapt to sudden extreme environmental changes produces some of the most drastic examples of rapid phenotypic evolution. The Mexican Tetra, Astyanax mexicanus, is abundant in the surface waters of northeastern Mexico, but repeated colonizations of cave environments have resulted in the independent evolution of troglomorphic phenotypes in several populations. Here, we present three chromosome-scale assemblies of this species, for one surface and two cave populations, enabling the first whole-genome comparisons between independently evolved cave populations to evaluate the genetic basis for the evolution of adaptation to the cave environment. Our assemblies represent the highest quality of sequence completeness with predicted protein-coding and noncoding gene metrics far surpassing prior resources and, to our knowledge, all long-read assembled teleost genomes, including zebrafish. Whole-genome synteny alignments show highly conserved gene order among cave forms in contrast to a higher number of chromosomal rearrangements when compared with other phylogenetically close or distant teleost species. By phylogenetically assessing gene orthology across distant branches of amniotes, we discover gene orthogroups unique to A. mexicanus. When compared with a representative surface fish genome, we find a rich amount of structural sequence diversity, defined here as the number and size of insertions and deletions as well as expanding and contracting repeats across cave forms. These new more complete genomic resources ensure higher trait resolution for comparative, functional, developmental, and genetic studies of drastic trait differences within a species., Competing Interests: Conflicts of interest The author(s) declare no conflicts of interest., (© The Author(s) 2024. Published by Oxford University Press on behalf of The Genetics Society of America.)

Intense environmental pressures can yield both regressive and constructive traits through complex evolutionary mechanisms. Although regression is well-studied, the biological bases of constructive features are less well understood. Cave-dwelling Astyanax fish harbor prolific extraoral taste buds on their heads, which are absent in conspecific surface-dwellers. Here, we present novel ontogenetic data demonstrating extraoral taste buds appear gradually and late in life history. This appearance is similar but non-identical in different cavefish populations, where patterning has evolved to permit taste bud re-specification across the endoderm-ectoderm germ layer boundary. Quantitative genetic analyses revealed that spatially distinct taste buds on the head are primarily mediated by two different cave-dominant loci. While the precise function of this late expansion on to the head is unknown, the appearance of extraoral taste buds coincides with a dietary shift from live-foods to bat guano, suggesting an adaptive mechanism to detect nutrition in food-starved caves. This work provides fundamental insight to a constructive evolutionary feature, arising late in life history, promising a new window into unresolved features of vertebrate sensory organ development., (© 2024. The Author(s).)

Copy number variation is a common contributor to phenotypic diversity, yet its involvement in ecological adaptation is not easily discerned. Instances of parallelly evolving populations of the same species in a similar environment marked by strong selective pressures present opportunities to study the role of copy number variants (CNVs) in adaptation. By identifying CNVs that repeatedly occur in multiple populations of the derived ecotype and are not (or are rarely) present in the populations of the ancestral ecotype, the association of such CNVs with adaptation to the novel environment can be inferred. We used this paradigm to identify CNVs associated with recurrent adaptation of the Mexican tetra (Astyanax mexicanus) to cave environment. Using a read-depth approach, we detected CNVs from previously re-sequenced genomes of 44 individuals belonging to two ancestral surfaces and three derived cave populations. We identified 102 genes and 292 genomic regions that repeatedly diverge in copy number between the two ecotypes and occupy 0.8% of the reference genome. Functional analysis revealed their association with processes previously recognized to be relevant for adaptation, such as vision, immunity, oxygen consumption, metabolism, and neural function and we propose that these variants have been selected for in the cave or surface waters. The majority of the ecotype-divergent CNVs are multiallelic and display copy number increases in cavefish compared to surface fish. Our findings suggest that multiallelic CNVs - including gene duplications - and divergence in copy number provide a fast route to produce novel phenotypes associated with adaptation to subterranean life., (© 2024 John Wiley & Sons Ltd.)

How genotype determines phenotype is a well-explored question, but genotype-environment interactions and their heritable impact on phenotype over the course of evolution are not as thoroughly investigated. The fish Astyanax mexicanus , consisting of surface and cave ecotypes, is an ideal emerging model to study the genetic basis of adaptation to new environments. This model has permitted quantitative trait locus mapping and whole-genome comparisons to identify the genetic bases of traits such as albinism and insulin resistance and has helped to better understand fundamental evolutionary mechanisms. In this review, we summarize recent advances in A. mexicanus genetics and discuss their broader impact on the fields of adaptation and evolutionary genetics., Competing Interests: Declaration of Interests The authors declare no competing interests.

Complex patterns of acoustic communication exist throughout the animal kingdom, including underwater. The river-dwelling and the Pachón cave-adapted morphotypes of the fish Astyanax mexicanus are soniferous and share a repertoire of sounds. Their function and significance is mostly unknown. Here, we explored whether and how sounds produced by blind cavefishes inhabiting different Mexican caves may vary. We compared "Clicks" and "Serial Clicks" produced by cavefish in six different caves distributed in three mountain ranges in Mexico. We also sampled laboratory-bred cavefish lines originating from four of these caves. Sounds were extracted and analyzed using both a manual method and a machine learning-based automation tool developed in-house. Multi-parametric analyses suggest wild cave-specific acoustic signatures, or "accents". An acoustic code also existed in laboratory cavefish lines, suggesting a genetic basis for the evolution of this trait. The variations in acoustic parameters between caves of origin did not seem related to fish phenotypes, phylogeography or ecological conditions. We propose that the evolution of such acoustic signatures would progressively lead to the differentiation of local accents that may prevent interbreeding and thus contribute to speciation., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2023 Hyacinthe et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Dark caves lacking primary productivity can expose subterranean animals to hypoxia. We used the surface-dwelling (surface fish) and cave-dwelling (cavefish) morphs of Astyanax mexicanus as a model for understanding the mechanisms of hypoxia tolerance in the cave environment. Primitive hematopoiesis, which is restricted to the posterior lateral mesoderm in other teleosts, also occurs in the anterior lateral mesoderm in Astyanax , potentially pre-adapting surface fish for hypoxic cave colonization. Cavefish have enlarged both hematopoietic domains and develop more erythrocytes than surface fish, which are required for normal development in both morphs. Laboratory-induced hypoxia suppresses growth in surface fish but not in cavefish. Both morphs respond to hypoxia by overexpressing hypoxia-inducible factor 1 ( hif1 ) pathway genes, and some hif1 genes are constitutively upregulated in normoxic cavefish to similar levels as in hypoxic surface fish. We conclude that cavefish cope with hypoxia by increasing erythrocyte development and constitutive hif1 gene overexpression., Competing Interests: Cv, WJ No competing interests declared, (© 2022, van der Weele and Jeffery.)

The fish Astyanax mexicanus comes in two very different forms: a "normal" river morph, and a blind, depigmented cave morph, living in the total and permanent darkness of Mexican caves. This species is on the way to becoming a model of choice in evolutionary and comparative biology, both for the study of the evolution of behavior, physiology or morphology, and for molecular genetics or population genetics. Here, I present the advancement of knowledge in the field of the developmental evolution of the eye of the cave morph. By rewinding back in time its development from the eye of the larva to the retinal field at the end of gastrulation, the cave-dwelling Astyanax embryo reveals mechanisms and processes likely to contribute to evolutionary variations between species, but also to pathological variations in the morphogenesis of the optic region., (© Société de Biologie, 2022.)

Understanding the molecular basis of repeatedly evolved phenotypes can yield key insights into the evolutionary process. Quantifying gene flow between populations is especially important in interpreting mechanisms of repeated phenotypic evolution, and genomic analyses have revealed that admixture occurs more frequently between diverging lineages than previously thought. In this study, we resequenced 47 whole genomes of the Mexican tetra from three cave populations, two surface populations and outgroup samples. We confirmed that cave populations are polyphyletic and two Astyanax mexicanus lineages are present in our data set. The two lineages likely diverged much more recently than previous mitochondrial estimates of 5-7 mya. Divergence of cave populations from their phylogenetically closest surface population likely occurred between ~161 and 191 k generations ago. The favoured demographic model for most population pairs accounts for divergence with secondary contact and heterogeneous gene flow across the genome, and we rigorously identified gene flow among all lineages sampled. Therefore, the evolution of cave-related traits occurred more rapidly than previously thought, and trogolomorphic traits are maintained despite gene flow with surface populations. The recency of these estimated divergence events suggests that selection may drive the evolution of cave-derived traits, as opposed to disuse and drift. Finally, we show that a key trogolomorphic phenotype QTL is enriched for genomic regions with low divergence between caves, suggesting that regions important for cave phenotypes may be transferred between caves via gene flow. Our study shows that gene flow must be considered in studies of independent, repeated trait evolution., (© 2018 John Wiley & Sons Ltd.)

Background: Cavefish populations belonging to the Mexican tetra species Astyanax mexicanus are outstanding models to study the tempo and mode of adaptation to a radical environmental change. They are currently assigned to two main groups, the so-called "old" and "new" lineages, which would have populated several caves independently and at different times. However, we do not have yet accurate estimations of the time frames of evolution of these populations., Results: We reanalyzed the geographic distribution of mitochondrial and nuclear DNA polymorphisms and we found that these data do not support the existence of two cavefish lineages. Using IMa2, a program that allows dating population divergence in addition to demographic parameters, we found that microsatellite polymorphism strongly supports a very recent origin of cave populations (< 20,000 years). We identified a large number of single-nucleotide polymorphisms (SNPs) in transcript sequences of pools of embryos (Pool-seq) belonging to Pachón cave population and a surface population from Texas. Based on summary statistics that can be computed with this SNP data set together with simulations of evolution of SNP polymorphisms in two recently isolated populations, we looked for sets of demographic parameters that allow the computation of summary statistics with simulated populations that are similar to the ones with the sampled populations. In most simulations for which we could find a good fit between the summary statistics of observed and simulated data, the best fit occurred when the divergence between simulated populations was less than 30,000 years., Conclusions: Although it is often assumed that some cave populations have a very ancient origin, a recent origin of these populations is strongly supported by our analyses of independent sets of nuclear DNA polymorphism. Moreover, the observation of two divergent haplogroups of mitochondrial and nuclear genes with different geographic distributions support a recent admixture of two divergent surface populations, before the isolation of cave populations. If cave populations are indeed only several thousand years old, many phenotypic changes observed in cavefish would thus have mainly involved the fixation of genetic variants present in surface fish populations and within a very short period of time.

Despite recent advances in the understanding of morphological evolution, the genetic underpinnings of behavioral and physiological evolution remain largely unknown. Here, we study the metabolic changes that evolved in independently derived populations of the Mexican cavefish, Astyanax mexicanus. A hallmark of cave environments is scarcity of food. Cavefish populations rely almost entirely on sporadic food input from outside of the caves. To survive under these conditions, cavefish have evolved a range of adaptations, including starvation resistance and binge eating when food becomes available. The use of these adaptive strategies differs among independently derived cave populations. Although all cavefish populations tested lose weight more slowly than their surface conspecifics during restricted rations, only a subset of cavefish populations consume more food than their surface counterparts. A candidate gene-based screen led to the identification of coding mutations in conserved residues of the melanocortin 4 receptor (MC4R) gene, contributing to the insatiable appetite found in some populations of cavefish. Intriguingly, one of the mutated residues has been shown to be linked to obesity in humans. We demonstrate that the allele results in both reduced maximal response and reduced basal activity of the receptor in vitro. We further validate in vivo that the mutated allele contributes to elevated appetite, growth, and starvation resistance. The allele appears to be fixed in cave populations in which the overeating phenotype is present. The presence of the same allele in multiple caves appears to be due to selection from standing genetic variation present in surface populations.

Background: Sleep is characterized by extended periods of quiescence and reduced responsiveness to sensory stimuli. Animals ranging from insects to mammals adapt to environments with limited food by suppressing sleep and enhancing their response to food cues, yet little is known about the genetic and evolutionary relationship between these processes. The blind Mexican cavefish, Astyanax mexicanus is a powerful model for elucidating the genetic mechanisms underlying behavioral evolution. A. mexicanus comprises an extant ancestral-type surface dwelling morph and at least five independently evolved cave populations. Evolutionary convergence on sleep loss and vibration attraction behavior, which is involved in prey seeking, have been documented in cavefish raising the possibility that enhanced sensory responsiveness underlies changes in sleep., Results: We established a system to study sleep and vibration attraction behavior in adult A. mexicanus and used high coverage quantitative trait loci (QTL) mapping to investigate the functional and evolutionary relationship between these traits. Analysis of surface-cave F2 hybrid fish and an outbred cave population indicates that independent genetic factors underlie changes in sleep/locomotor activity and vibration attraction behavior. High-coverage QTL mapping with genotyping-by-sequencing technology identify two novel QTL intervals that associate with locomotor activity and include the narcolepsy-associated tp53 regulating kinase. These QTLs represent the first genomic localization of locomotor activity in cavefish and are distinct from two QTLs previously identified as associating with vibration attraction behavior., Conclusions: Taken together, these results localize genomic regions underlying sleep/locomotor and sensory changes in cavefish populations and provide evidence that sleep loss evolved independently from enhanced sensory responsiveness.

The loss of traits is a commonly observed evolutionary pattern in cave organisms, but due to extensive morphological convergence, inferring relationships between cave and surface populations can be difficult. For instance, Astyanax mexicanus (the blind Mexican cavefish) is thought to have repeatedly lost its eyes following colonization of cave environments, but the number of evolutionarily independent invasions of this species into caves remains unclear. Because of these repeated losses, it has become a model organism for studying the genetic basis of phenotypic trait loss. Here we reconstruct a high-resolution phylogeography for A. mexicanus inferred from both mitochondrial DNA and several thousand single nucleotide polymorphisms. We provide novel insight into the origin of cave populations from the Sabinos and Río Subterráneo caves and present evidence that the Sabinos cave population is part of a unique cave lineage unrelated to other A. mexicanus cave populations. Our results indicate A. mexicanus cave populations have at least four independent origins., (Copyright © 2014 Elsevier Inc. All rights reserved.)