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Life in complete darkness has driven the evolution of a suite of troglobitic features in the blind Mexican cavefish Astyanax mexicanus, such as eye and pigmentation loss. While regressive evolution is a hallmark of obligate cave‐dwelling organisms, constructive (or augmented) traits commonly arise as well. The cavefish cranium has undergone extensive changes compared with closely‐related surface fish. These alterations are rooted in both cranial bones and surrounding sensory tissues such as enhancements in the gustatory and lateral line systems. Cavefish also harbor numerous cranial bone asymmetries: fluctuating asymmetry of individual bones and directional asymmetry in a dorsal bend of the skull. This asymmetry is mirrored by the asymmetrical patterning of mechanosensory neuromasts. We explored the relationship between facial bones and neuromasts using in vivo fluorescent colabeling and microcomputed tomography. We found an increase in neuromast density within dermal bone boundaries across three distinct populations of cavefish compared to surface‐dwelling fish. We also show that eye loss disrupts early neuromast patterning, which in turn impacts the development of dermal bones. While cavefish exhibit alterations in cranial bone and neuromast patterning, each population varied in the severity. This variation may reflect observed differences in behavior across populations. For instance, a bend in the dorsal region of the skull may expose neuromasts to water flow on the opposite side of the face, enhancing sensory input and spatial mapping in the dark. Research Highlights: We characterized facial traits that evolved across multiple populations of cavefish. Changes to the lateral line mirror alterations to dermal bones, suggesting that sensory‐skeletal integration may have evolved to mediate cave‐adapted behaviors. [ABSTRACT FROM AUTHOR]

Together, the complex geological history and climatic diversity of Mesoamerica create a rich source of biodiversity from which evolutionary processes can be studied. Here, we discuss highly divergent morphs of lake‐dwelling fishes distributed across Mexico and Central America, originally recognized as members of different genera (Astyanax and "Bramocharax"). Recent phylogenetic studies, however, suggest these morphs group within the same genus and readily hybridize. Despite genetic similarities, Bramocharax morphs exhibit stark differences in cranial shape and dentition. We investigated the evolution of several cranial traits that vary across morphs collected from four lakes in Mexico and Nicaragua and discovered an ecomorphological cline from northern to southern lakes. Northern populations of sympatric morphs exhibit a similar cranial shape and tooth morphology. Southern populations of Bramocharax morphs, however, showed a larger disparity in maxillary teeth, length and frequency of unicuspid teeth, an elongated snout, and a streamlined cranium compared to Astyanax morphs. This divergence of craniofacial morphology likely evolved in association with differences in trophic niches. We discuss the morphological differences across the four lake systems in terms of geological history and trophic dynamics. In summary, our study suggests that Bramocharax morphs are likely locally adapted members derived from independent Astyanax lineages, highlighting an interesting parallel evolutionary pattern within the Astyanax genus. Research Highlights: We characterized the evolution of cranial traits in two divergent lacustrine morphs in Astyanax genus from four lakes in Mesoamerica.We recovered an ecomorphological disparity cline from northern to southern lakes.Bramocharax morphs showed a convergent cranial traits in Mesoamerican lakes. [ABSTRACT FROM AUTHOR]

SUMMARY Animals that colonize dark and nutrient-poor subterranean environments evolve numerous extreme phenotypes. These include dramatic changes to the craniofacial complex, many of which are under genetic control. These phenotypes can demonstrate asymmetric genetic signals wherein a QTL is detected on one side of the face but not the other. The causative gene(s) underlying QTL are difficult to identify with limited genomic resources. We approached this task by searching for candidate genes mediating fragmentation of the third suborbital bone (SO3) directly inferior to the orbit of the eye. We integrated positional genomic information using emerging Astyanax resources, and linked these intervals to homologous (syntenic) regions of the Danio rerio genome. We identified a discrete, approximately 6 Mb, conserved region wherein the gene causing SO3 fragmentation likely resides. We interrogated this interval for genes demonstrating significant differential expression using mRNA-seq analysis of cave and surface morphs across life history. We then assessed genes with known roles in craniofacial evolution and development based on GO term annotation. Finally, we screened coding sequence alterations in this region, identifying two key genes: transforming growth factor β3 ( tgfb3) and bone morphogenetic protein 4 ( bmp4). Of these candidates, tgfb3 is most promising as it demonstrates significant differential expression across multiple stages of development, maps close (<1 Mb) to the fragmentation critical locus, and is implicated in a variety of other animal systems (including humans) in non-syndromic clefting and malformations of the cranial sutures. Both abnormalities are analogous to the failure-to-fuse phenotype that we observe in SO3 fragmentation. This integrative approach will enable discovery of the causative genetic lesions leading to complex craniofacial features analogous to human craniofacial disorders. This work underscores the value of cave-dwelling fish as a powerful evolutionary model of craniofacial disease, and demonstrates the power of integrative system-level studies for informing the genetic basis of craniofacial aberrations in nature. [ABSTRACT FROM AUTHOR]