Convergence and Parallelism in Astyanax Cave-Dwelling Fish

Abstract

The blind Mexican cavefish, Astyanax mexicanus, has emerged as a powerful model system for informing evolutionary and biomedical problems. A number of fascinating features evolve in cave-dwelling lineages, irrespective of phylogeny, or geography. For instance, cave-dwelling animals frequently lose vision and pigmentation, but evolve substantial gains in non-visual sensation. Astyanax cavefish are interesting models for cave evolution because they do not exist as a solitary group or population. Rather, there are 29 different Astyanax cave populations distributed across the Sierra de El Abra region of Mexico. Until recently, our understanding of how different cave populations relate to one another, and to surface-dwelling forms, was limited. We now know that there were two principal invasions over the past several millions of years—an ‘older’ stock invaded ~2–5 My ago and seeded the southern El Abra caves. The descendants of the surface-dwelling fish from this older stock have gone locally extinct. A second, ‘younger’ stock invaded the region ~1–2 My ago and seeded the northern Guatemala caves and the western Micos cave network. Descendants of the second invasion persist as extant surface-dwelling fish in the surrounding rivers. Recent population genetic evidence indicates that substantial ‘mixing’ has occurred between many caves populations, as well as between cave and surface-dwelling forms. This highly complex biogeography has raised many questions about the nature of cave-associated traits. Do these traits evolve once and spread throughout multiple cave systems? Or, alternatively, do cave-related traits evolve repeatedly in different cave complexes? This chapter discusses experimental approaches that have shed light on this question—complementation crosses and candidate gene analyses. Interestingly, complementation analyses show that vision loss and pigmentation loss evolve through similar and different genomic regions, respectively. Vision loss occurs throughout the Sierra de El Abra, but the extent to which the same genes are implicated in different eyeless caves decreases with geographic distance between caves. In contrast, pigmentation changes affecting two Mendelian traits (albinism and brown) appear to evolve through the same genes, via distinct mutations. Standing genetic variation, present in local surface-dwelling forms, also plays a key role in the evolution of reduced eye sizes, albinism, and appetite control. Thus, evolution of cave-associated phenotypes proceeds through a complex mosaic of both convergent and parallel processes. These patterns reflect the complex evolutionary and geographic origins of cavefish in this region of Mexico. Future studies based on genome-level analyses will provide new insight to the pace and mechanism(s) of cave evolution in this emerging model system.