In the process of morphological evolution, the extent to which cryptic, preexisting variation provides a substrate for natural selection has been controversial. We provide evidence that HSP90 phenotypically masks standing eye size variation in surface populations of the cavefish Astyanax mexicanus. This variation is exposed by HSP90 inhibition, and can be selected for, ultimately yielding a reduced-eye phenotype even in the presence of full HSP90 activity. Raising surface fish under conditions found in caves taxes the HSP90 system, unmasking the same phenotypic variation as direct inhibition of HSP90. These results suggest that cryptic variation played a role in the evolution of eye loss in cavefish and provide the first evidence for HSP90 as a capacitor for morphological evolution in a natural setting.

Background Surface populations of A. mexicanus, living in rivers like their common ancestors, school, while several, independent derived cave populations of the same species have lost schooling behavior. Results We quantify schooling behavior in individual A. mexicanus and identify quantitative trait loci (QTL) for this trait. We find that the evolutionary modulation of schooling has both vision-dependent and independent components. We also quantify differences in the lateral line and vision between cavefish and surface fish and relate these differences to the evolutionary loss of schooling behavior. We provide evidence that a monoamine may have played a role in the evolution of schooling behavior. Conclusions We find that vision is essential for schooling tendency in A. mexicanus, while the lateral line has a small effect on this behavior. Schooling behavior in A. mexicanus has evolved both through changes in sensory systems and through changes in genetic loci that likely act downstream of sensory inputs.

When an organism colonizes a new environment, it needs to adapt both morphologically and behaviorally to survive and thrive. Although recent progress has been made in understanding the genetic architecture underlying morphological evolution, behavioral evolution is poorly understood. Here, we use the Mexican cavefish, Astyanax mexicanus, to study the genetic basis for convergent evolution of feeding posture. When river-dwelling surface fish became entrapped in the caves, they were confronted with dramatic changes in the availability and type of food source and in their ability to perceive it. In this setting, multiple independent populations of cavefish exhibit an altered feeding posture compared with their ancestral surface forms. We determined that this behavioral change in feeding posture is not due to changes in cranial facial morphology, body depth, or to take advantage of the expansion in the number of taste buds. Quantitative genetic analysis demonstrates that two different cave populations have evolved similar feeding postures through a small number of genetic changes, some of which appear to be distinct. This work indicates that independently evolved populations of cavefish can evolve the same behavioral traits to adapt to similar environmental challenges by modifying different sets of genes.T he colonization of caves is an extreme example of a species entering a new environment. Unique attributes of caves relative to the surface environment include darkness, high humidity, relatively constant temperature, absence of predators, and scarcity of food. Under these circumstances, many species of cave animals have evolved a suite of similar traits, including constructive traits such as heightened sensory systems and regressive traits such as loss of pigmentation and reduction in eye morphology (1). To study the evolution of cave-specific traits, we have focused on Astyanax mexicanus, the Mexican cavefish. A. mexicanus exists in two forms, a cave-dwelling form and a river-dwelling surface form. Importantly, these forms are still interfertile (2), allowing one to take a genetic approach using quantitative trait loci (QTL) analysis for the mapping of cave traits. Furthermore, there are multiple, independently evolved cave populations (3-7) that in many cases have evolved similar traits, allowing for the study of convergent evolution.Populations of cave organisms have often been the subjects of studies on convergence. For example, loss of pigmentation evolved via disruptions in the first step of the melanin synthesis pathway in multiple species of cave organisms (8). Similarly, a decrease in the levels of melanin synthesis arose in multiple cave populations of A. mexicanus through different mutations in the same genes (9, 10). In contrast, crosses between multiple cave populations of A. mexicanus result in embryonic hybrid fish with larger, functional eyes, indicating that evolution of this trait is controlled by different genetic loci in different cave populations (2, 11).Among the most intriguing and least und...

No abstract

Five decades ago, a landmark paper in Science titled The Cave Environment heralded caves as ideal natural experimental laboratories in which to develop and address general questions in geology, ecology, biogeography, and evolutionary biology. Although the ‘caves as laboratory’ paradigm has since been advocated by subterranean biologists, there are few examples of studies that successfully translated their results into general principles. The contemporary era of big data, modelling tools, and revolutionary advances in genetics and (meta)genomics provides an opportunity to revisit unresolved questions and challenges, as well as examine promising new avenues of research in subterranean biology. Accordingly, we have developed a roadmap to guide future research endeavours in subterranean biology by adapting a well‐established methodology of ‘horizon scanning’ to identify the highest priority research questions across six subject areas. Based on the expert opinion of 30 scientists from around the globe with complementary expertise and of different academic ages, we assembled an initial list of 258 fundamental questions concentrating on macroecology and microbial ecology, adaptation, evolution, and conservation. Subsequently, through online surveys, 130 subterranean biologists with various backgrounds assisted us in reducing our list to 50 top‐priority questions. These research questions are broad in scope and ready to be addressed in the next decade. We believe this exercise will stimulate research towards a deeper understanding of subterranean biology and foster hypothesis‐driven studies likely to resonate broadly from the traditional boundaries of this field.