Abstract
BackgroundHow and why animals lose eyesight during adaptation to the dark and food-limited cave environment has puzzled biologists since the time of Darwin. More recently, several different adaptive hypotheses have been proposed to explain eye degeneration based on studies in the teleost Astyanax mexicanus, which consists of blind cave-dwelling (cavefish) and sighted surface-dwelling (surface fish) forms. One of these hypotheses is that eye regression is the result of indirect selection for constructive characters that are negatively linked to eye development through the pleiotropic effects of Sonic Hedgehog (SHH) signaling. However, subsequent genetic analyses suggested that other mechanisms also contribute to eye regression in Astyanax cavefish. Here, we introduce a new approach to this problem by investigating the phenotypic and genetic relationships between a suite of non-visual constructive traits and eye regression.ResultsUsing quantitative genetic analysis of crosses between surface fish, the Pachón cavefish population and their hybrid progeny, we show that the adaptive vibration attraction behavior (VAB) and its sensory receptors, superficial neuromasts (SN) specifically found within the cavefish eye orbit (EO), are genetically correlated with reduced eye size. The quantitative trait loci (QTL) for these three traits form two clusters of congruent or overlapping QTL on Astyanax linkage groups (LG) 2 and 17, but not at the shh locus on LG 13. Ablation of EO SN in cavefish demonstrated a major role for these sensory receptors in VAB expression. Furthermore, experimental induction of eye regression in surface fish via shh overexpression showed that the absence of eyes was insufficient to promote the appearance of VAB or EO SN.ConclusionsWe conclude that natural selection for the enhancement of VAB and EO SN indirectly promotes eye regression in the Pachón cavefish population through an antagonistic relationship involving genetic linkage or pleiotropy among the genetic factors underlying these traits. This study demonstrates a trade-off between the evolution of a non-visual sensory system and eye regression during the adaptive evolution of Astyanax to the cave environment.
Highlights
How and why animals lose eyesight during adaptation to the dark and food-limited cave environment has puzzled biologists since the time of Darwin
We discovered that the quantitative trait loci (QTL) underlying vibration attraction behavior (VAB), a specific class of superficial neuromasts (SN) located within the cavefish eye orbit (EO), and reduced eyes form two distinct clusters of overlapping QTL that together explain a significant portion of the genetic variation underlying these traits
By shh overexpression, we showed that induction of eye degeneration in surface fish did not induce VAB or increase EO SN, suggesting that these traits are part of an antagonistic system impacting eye formation that is independent of Sonic Hedgehog (SHH) signaling, and that the extra space opened by eye regression is insufficient to promote the appearance of these constructive traits
Summary
Three competing hypotheses have been proposed for the adaptive evolution of eye regression: (1) direct natural selection against eyes to conserve energy in the resource poor cave environment [7]; (2) indirect selection against eyes to open sufficient space for the elaboration of constructive characters [2,8,9,10]; and (3) indirect selection against eyes due to the enhancement of traits that are negatively linked to optic development by antagonistic pleiotropy [11,12] Distinguishing among these hypotheses has been difficult since the genetic basis of eye reduction is unknown in cavedwelling animals
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