Genes, modules and the evolution of cave fish

Abstract

Cave fish provide a model system for exploring the genetic basis of regressive evolution. A proposal that regressive evolution (for example, eye loss) may result from pleiotropy, by selection on constructive traits (for example, improved taste) has received considerable recent interest as it contradicts the theory that regressive evolution results from neutral evolution. In this study, these theories are reviewed by placing the classical and molecular genetic studies of cave fish in a common framework. Sequence data and the wide range of intermediate sized eyes in hybrids between surface and cave fish suggest that currently there is no strong evidence supporting the notion that structural eye genes have been afflicted by destructive mutations. The hedgehog genes, which are suggested to reduce the primordial eye cup size in cavefish by expanded expression, are also not mutated. The as yet unidentified 'eye genes' revealed by crossing experiments seem primarily responsible for eye regression and determine eye development through hedgehog. Hybrids between different eye-reduced cave populations developing large 'back to surface eyes' support this. In such eyes, hh expression is restored by complementary restitution because of the recombination of 'eye genes', which were subjected to different destructive mutations in separately evolving cave fish populations. All regressive and constructive cave fish traits can be considered to result from genetic modules, each showing a comparable pattern of expression. The constructive and regressive modules are shown to inherit independently from each other, which does not support the view that eye regression is a spin off effect of the improvement of beneficial traits through pleiotropy.

Pleiotropy and eye degeneration in cavefish

“…As shown by Strickler et al (2007), the lens is necessary to prevent cell death in the retina, including its photoreceptor cells, which gradually turn over and are replaced in the normal and degenerating retina. The recovery of photoreceptor cells in cavefish hosts containing a transplanted surface fish lens, observed by Yamamoto and Jeffery (2000) and Strickler et al (2007), cannot be explained by variability in eye phenotypes within the cavefish population, as also claimed by Wilkens (2010), because replaced photoreceptor cells are not seen in the opposite (degenerating) eye of the same host, which did not receive a lens transplant. In summary, the genetic and developmental data are not conflicting on this point.…”

“…However, no such claim is made in this or subsequent lens transplantation studies, which instead conclude that at least two processes govern eye regression, one centered in the lens and another in the optic cup (possibly the pigment epithelium; Strickler et al, 2007). The lens transplantation studies demonstrate that retinal development is not completely independent of the lens, as contended by Wilkens (2010). As shown by Strickler et al (2007), the lens is necessary to prevent cell death in the retina, including its photoreceptor cells, which gradually turn over and are replaced in the normal and degenerating retina.…”

“…The first idea was favored until about the turn of this century (Culver and Wilkens, 2000), but since then new genetic and developmental evidence has tipped the scale toward the third idea-pleiotropy (Jeffery, 2005;Protas et al, 2008). In this review, Wilkens (2010) re-evaluates the genetic and developmental data and concludes that there is no validity for the second or third (selectionist) theories, reverting to neutral mutation as the most plausible explanation for eye degeneration. Here, I contest some of the facts and interpretations presented in the Wilkens (2010) review and call attention to published developmental data implicating pleiotropy in A. mexicanus eye regression (Yamamoto et al, 2009) that were apparently not considered in drawing its conclusions.…”

“…A major finding of the Yamamoto et al (2009) study was that A. mexicanus surface fish overexpressing a shh transgene showed coupled eye degeneration and enhancement of oral and taste bud development, revealing a developmental trade-off between these regressive and constructive traits mediated by pleiotropy. Quantitative trait loci mapping results suggest that neither of the two A. mexicanus shh genes are mutated in cavefish (Protas et al, 2007), prompting Wilkens (2010) to propose that eye regression is possibly mediated by disruptive mutations in modifier genes (called 'eye genes') acting upstream of shh. If this proposal is correct, the 'eye genes' would regulate the pleiotropic shh system described above and therefore would not be effectively neutral.…”

“…In an article recently published in Heredity, Wilkens (2010) reviews the mechanisms of regressive evolution in the cavefish, Astyanax mexicanus. A. mexicanus consists of a surface-dwelling morph with eyes and pigmentation, and many cave-dwelling morphs that have lost or have a reduced form of both traits.…”