Subterranean Fishes of the World

3376

2013

Proceedings of the National Academy of Sciences, USA

16933–16938

110

Relatively little is known about the genetic basis of behavioral evolution, in particular for behaviors without any obvious related morphological changes. We have focused on changes in feeding posture that evolved in the small tetra Astyanax mexicanus as it adapted from life in the rivers to the very different ecological conditions found in caves. Using comparative quantitative genetics/genomics, we find that behavioral differences in feeding posture between surface and cave populations arose independently, through different polygenic genetic mechanisms in multiple, independent cave populations. This work provides insights into the genetic architecture of this behavioral trait and shows that this hard-wired behavior can arise through multiple genetic routes. 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. The 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 understood adaptations to caves are behavioral traits. Cave populations of A. mexicanus have evolved an enhanced attraction to a vibration source, loss of schooling behavior, reduction in time spent sleeping, and a loss of aggression (2, 12⇓⇓⇓–16). Little is known about how these behaviors evolve and whether each behavior has evolved through the same or different genes or pathways as an adaptation to cave life. Here we focus on a convergent aspect of feeding behavior and its potentially related morphological traits found in cave populations of A. mexicanus. Surface fish feed at a steep angle relative to the substrate when feeding in the dark. In contrast, multiple cave populations feed at a much lower angle (17). We examined feeding orientation in three independently evolved cave populations to determine the underlying genetic architecture, including the extent to which this behavior depended on correlated morphological changes, and to determine whether multiple cave populations evolved this alternative feeding posture through changes in the same or different genetic loci.

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