Evolution of an adaptive behavior and its sensory receptors promotes eye regression in blind cavefish

How 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. Using 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. We 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.https://doi.org/10.1186/1741-7007-10-108https://doi.org/10.1186/1741-7007-11-8

Distinct genetic architecture underlies the emergence of sleep loss and prey-seeking behavior in the Mexican cavefish

Sleep is characterized by extended periods of quiescence and reduced responsiveness to sensory stimuli. Animals ranging from insects to mammals adapt to environments with limited food by suppressing sleep and enhancing their response to food cues, yet little is known about the genetic and evolutionary relationship between these processes. The blind Mexican cavefish, Astyanax mexicanus is a powerful model for elucidating the genetic mechanisms underlying behavioral evolution. A. mexicanus comprises an extant ancestral-type surface dwelling morph and at least five independently evolved cave populations. Evolutionary convergence on sleep loss and vibration attraction behavior, which is involved in prey seeking, have been documented in cavefish raising the possibility that enhanced sensory responsiveness underlies changes in sleep. We established a system to study sleep and vibration attraction behavior in adult A. mexicanus and used high coverage quantitative trait loci (QTL) mapping to investigate the functional and evolutionary relationship between these traits. Analysis of surface-cave F2 hybrid fish and an outbred cave population indicates that independent genetic factors underlie changes in sleep/locomotor activity and vibration attraction behavior. High-coverage QTL mapping with genotyping-by-sequencing technology identify two novel QTL intervals that associate with locomotor activity and include the narcolepsy-associated tp53 regulating kinase. These QTLs represent the first genomic localization of locomotor activity in cavefish and are distinct from two QTLs previously identified as associating with vibration attraction behavior. Taken together, these results localize genomic regions underlying sleep/locomotor and sensory changes in cavefish populations and provide evidence that sleep loss evolved independently from enhanced sensory responsiveness.https://doi.org/10.1186/s12915-015-0119-

Summary statistics of all quantitative trait loci (QTL) for scleral ossification detected in this study.

<p>LOD = logarithm of the odds. PVE = percent variance explained.</p

Recessive inheritance of scleral ossicles at all QTL positions.

<p>Effect plots displaying average scleral ossicle number for each genotypic class observed in the CF x SF F2 hybrids from all three analyses. In each case, F2 hybrids with two cavefish alleles have fewer scleral ossicles on average than those with either one or two surface fish alleles. This pattern is consistent with the recessive inheritance of scleral ossicle loss in CF [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0171061#pone.0171061.ref013" target="_blank">13</a>].</p

Chi-square (χ²) analysis of observed and expected ratios of the combined CF(Pa) x SF(Mx) F2 progeny from Gross <i>et al</i>. [15] and the CF(Pa) x SF(Tx) F2 progeny from O’Quin <i>et al</i>. [13] with and without scleral ossicles due to a genotypic threshold at 1–4 loci.

<p>Chi-square (χ²) analysis of observed and expected ratios of the combined CF(Pa) x SF(Mx) F2 progeny from Gross <i>et al</i>. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0171061#pone.0171061.ref015" target="_blank">15</a>] and the CF(Pa) x SF(Tx) F2 progeny from O’Quin <i>et al</i>. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0171061#pone.0171061.ref013" target="_blank">13</a>] with and without scleral ossicles due to a genotypic threshold at 1–4 loci.</p

Skewed distribution of scleral ossicles in CF x SF F2 hybrids.

<p>(<b>A</b>) Example CF(Pa) x SF(Mx) F2 progeny from Gross <i>et al</i>. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0171061#pone.0171061.ref015" target="_blank">15</a>] with 0, 1, and 2 scleral ossicles. (<b>B</b>) Distribution of scleral ossicles among CF(Pa) x SF(Tx) F2 originally published in O'Quin <i>et al</i>. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0171061#pone.0171061.ref013" target="_blank">13</a>], from CF(Pa) x SF(Mx) F2 from Gross <i>et al</i>. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0171061#pone.0171061.ref015" target="_blank">15</a>], and the combined F2 from both analyses. In each case, the skewed distributions of F2 progeny with two scleral ossicles is consistent with hypothesis that multiple genes control scleral ossicle formation through an epistatic threshold model of inheritance.</p

Evolution of cichlid vision via <it>trans</it>-regulatory divergence

<p>Abstract</p> <p>Background</p> <p>Phenotypic evolution may occur through mutations that affect either the structure or expression of protein-coding genes<b>.</b> Although the evolution of color vision has historically been attributed to structural mutations within the opsin genes, recent research has shown that opsin regulatory mutations can also tune photoreceptor sensitivity and color vision. Visual sensitivity in African cichlid fishes varies as a result of the differential expression of seven opsin genes<b>.</b> We crossed cichlid species that express different opsin gene sets and scanned their genome for expression Quantitative Trait Loci (eQTL) responsible for these differences. Our results shed light on the role that different structural, <it>cis</it>-, and <it>trans</it>-regulatory mutations play in the evolution of color vision.</p> <p>Results</p> <p>We identified 11 eQTL that contribute to the divergent expression of five opsin genes. On three linkage groups, several eQTL formed regulatory “hotspots” associated with the expression of multiple opsins. Importantly, however, the majority of the eQTL we identified (8/11 or 73%) occur on linkage groups located <it>trans</it> to the opsin genes, suggesting that cichlid color vision has evolved primarily via <it>trans</it>-regulatory divergence. By modeling the impact of just two of these <it>trans</it>-regulatory eQTL, we show that opsin regulatory mutations can alter cichlid photoreceptor sensitivity and color vision at least as much as opsin structural mutations can.</p> <p>Conclusions</p> <p>Combined with previous work, we demonstrate that the evolution of cichlid color vision results from the interplay of structural, <it>cis</it>-, and especially <it>trans</it>-regulatory loci. Although there are numerous examples of structural and <it>cis</it>-regulatory mutations that contribute to phenotypic evolution, our results suggest that <it>trans</it>-regulatory mutations could contribute to phenotypic divergence more commonly than previously expected, especially in systems like color vision, where compensatory changes in the expression of multiple genes are required in order to produce functional phenotypes.</p