Regressive Evolution in the Mexican Cave Tetra, Astyanax mexicanus

Abstract

The evolutionary forces driving the reduction of eyes and pigmentation in cave-adapted animals are unknown; Darwin famously questioned the role of natural selection in eye loss in cave fishes: "As it is difficult to imagine that eyes, although useless, could be in any way injurious to animals living in darkness, I attribute their loss wholly to disuse"[1]. We studied the genetics of eye and pigmentation regression in the Mexican cave tetra, Astyanax mexicanus, by mapping and quantitative trait loci (QTL) analysis. We also mapped QTL for the putatively constructive traits of jaw size, tooth number, and numbers of taste buds. The data suggest that eyes and pigmentation regressed through different mechanisms. Cave alleles at every eye or lens QTL we detected caused size reductions, consistent with evolution by natural selection but not with drift. QTL polarities for melanophore number were mixed, however, consistent with genetic drift. Arguments against a role for selection in the regression of cave-fish eyes cited the insignificant cost of their development [2, 3], but we argue that the energetic cost of their maintenance is sufficiently high for eyes to be detrimental in the cave environment. Regression can be caused either by selection or drift.

Genes, modules and the evolution of cave fish

“…In addition, mapping of candidate genes shh, twhh and Pax6 revealed that no eye quantitative trait loci (QTLs) are located near these loci. This result makes it unlikely that mutations in any of these genes are directly responsible for eye regression (Protas et al, 2007). This finding is also supported by the observation that all the different-sized eyes developed in hybrids between cave and surface forms show all the structures characteristic of an eye such as lens, lens muscle, pupil and retinal layers (Wilkens, 1988(Wilkens, , 2007.…”

“…This second peak or the skewness is interpreted as being caused by an unproportional increase of phenotypic manifestation. This increase is not due to monofactorial inheritance, because at least eight eye polygenes were calculated to be responsible for the eye size difference between cave and surface fish (Lande, 1981;Wilkens, 1988;Culver and Wilkens, 2000;Protas et al, 2007). Multiple polygeny is also found in other complex regressive and constructive cave fish traits and the false assumption of apparent monofactorial inheritance was studied in detail for feeding behaviour (Schemmel, 1980).…”

“…In addition to the hypothesis that an exposed eye may be a deleterious risk in darkness (Barr, 1968;Strickler et al, 2007), it has recently been suggested that the same genes, which are responsible for eye or pigment regression, would simultaneously improve specific constructive traits. Thus, selection would indirectly influence the reduction of the eye by pleiotropy through a constructive trait such as taste or energy economy (Barr, 1968;Jeffery, 2005;Protas et al, 2007).…”

Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox genelabial

“…Often, however, new bodyplans also emerge by the loss of features and organs. Examples of this so-called regressive evolution include eye loss in cavefish [1], wing loss in ants [2] or the loss of limbs in the snake bodyplan [3]. Another textbook example for regressive evolution is limb loss on the intercalary segment in insects [4].…”

Pleiotropy and eye degeneration in cavefish

“…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.…”