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.2012 Dec 27:10:108.
doi: 10.1186/1741-7007-10-108.

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

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

Masato Yoshizawa et al. BMC Biol..

Abstract

Background: 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.

Results: 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.

Conclusions: 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.

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Figures

Figure 1
Figure 1
Genetic analysis of VAB, SN and eye regression. (A-E) Histograms showing (A) VAB level (square-rooted number of approaches, or NOA), (B) SO-3 SN number, (C) EO SN number, (D) SO-3 SN diameter, and (E) eye diameter in surface fish, cavefish and their F1progeny (upper frames), and the F2and F3generations (lower frames). The F1and F2phenotypes are intermediate between surface fish and cavefish, and the sum of F2and F3phenotypes covered most of the range of phenotypes for each trait between surface fish and cavefish, although the distributions of SO-3 and EO SN numbers remain somewhat restricted towards the surface fish phenotype. (F-G) Regression analysis showing the relationships between VAB and (F) EO SN number, (G) SO-3 SN number, (H) SO-3 SN diameter, and (I) eye diameter/SL. (J) The relationship of SN number at EO and eye diameter/SL. EO SN number and SO-3 SN diameter were both positively correlated with VAB level, which was negatively correlated with eye size. EO SN number was also negatively correlated with eye size. Linear regression lines are shown in red. (K-N) Bright field images (upper) and DASPEI-stained neuromasts (lower) compared among (K) surface fish, (L-M) two examples of F3hybrids, and (N) cavefish. Scale bar in (N) is equal to 1.0 mm. In K-N, circles outlined by white dashed lines indicate the edges of the eye, red dashed lines indicate the lines of suborbital canal neuromasts in the head lateral line, the areas enclosed by the blue dotted lines indicate the approximate outline of the SO-3 region, and the areas shown by the yellow dotted lines and indicated by yellow arrows show the EO regions.
Figure 2
Figure 2
Astyanax mexicanusgenetic linkage map from a Texas surface fish × Pachón cavefish cross. The names of the genomic markers are indicated at the right of each linkage group. LG ids for this cross are shown at the top with LG ids corresponding to the numbering scheme of Protaset al.[23] made from the F2 progeny of Mexican surface fish × Pachón cavefish cross shown in parentheses. NA indicates that there is no homologous linkage group in Protaset al.[23]. The bars denote Bayesian credible intervals with probability coverage as 0.95. New genes placed on the map in this study were the 5-hydroxytryptamine (serotonin) receptors (5ht1A, 5ht2A, 5ht2B, 5ht2C, 5ht2C_like), dopamine receptor D1 (drd1), eyes absent homolog 1 (eya1), monoamine oxidase (mao); melanin-concentrating hormone receptor 2 (mchr2), neurogenin 1 (ngn1), neuregulin 2 (nrg2); pro-melanin concentrating hormone (pmch); profilin 2 (pfn2); serotonin transporter (sert); tyrosine hydroxylase 1 and 2 (th, th2); and tryptophan hydroxylase 2 (tph2). Other genes (cryaa, hsp90a, igfbp5, mc1r, mc2r, mch1r, oca2, pax6, shhA, shroom2, tfe3) were genotyped and mapped as in previous studies [7,22,34].
Figure 3
Figure 3
QTL mapping of VAB, SN number and size, and eye size. (A) LOD scores computed with single-QTL model genome-scan are plotted against the distance across each linkage group (LG). Red solid lines indicate LOD scores for VAB-level at 35 Hz vibration stimulus, yellow dotted lines for VAB at 50 Hz stimulus, and lime green dotted lines for VAB at 10 Hz stimulus. Significant VAB QTL were detected at LG2 and 17 only at 35 Hz stimulus. The horizontal line indicates the genome-wide significance thresholds atP< 0.05. (B, C) LOD scores computed following multiple QTL mapping. Nine QTL were found across five different LG (see also Table 1). Six overlapping Bayesian credible intervals of QTL for VAB, EO SN number and eye size were found on LG 2 and 17. The X-axis indicates genetic distance in centimorgans (cM), and colored bars denote Bayesian credible intervals with probability coverage as 0.95 for each significant QTL. Insets with gray background show effect plots of phenotypic values against each genotype (mean ± s.e.m.) at the peak locus denoted by the black triangle. Sf/Sf, surface fish homozygote, Sf/Cf, heterozygote, and Cf/Cf, cavefish homozygote. Horizontal dotted lines are genome-wide significant thresholds (P< 0.05) calculated from the single-QTL model (see Methods).
Figure 4
Figure 4
Effects of bilateral SN ablation on VAB in cavefish. (A) Comparison of DASPEI-stained EO SN and SO-3 SN in the ablated areas. The SN present before but absent after ablation within the two ablated regions (outlined by dashed white lines) are pseudo-colored in red. The red dashes indicate the line of suborbital canal neuromasts in the head lateral line and the areas enclosed by the blue dashed lines indicate the SO-3 region; the areas between the suborbital canal lateral line (red dashes) and dashed yellow lines represent the region containing EO SN. Scale bar in (lower panel of A) is 1.0 mm. (B) Schematic drawing of the ablated areas of 10 cavefish in the EO SN ablation experiment. Each experiment was color-coded. The snout is shown at the left. The ablated area included both the EO region and a part of the SO-3 region. The suborbital canal lateral line is indicated with red line. (C) The EO SN number of cavefish prior to ablation of EO or SO-3 SN. There was no difference in EO SN number between these two groups (Z= -0.54,P= 0.614; n = 10 for EO SN ablation; n = 7 for SO-3 SN ablation). (D) VAB in cavefish before SN ablation and four to six days after SN ablation. Values are means ± s.e.m. **:P< 0.01. n.s.: not significant. Number of cavefish used were: n = 10 for EO, n = 7 for SO-3. Rod vibration at 35 Hz was used to measure VAB.
Figure 5
Figure 5
Effects ofshhinduced eye degeneration on VAB and SN number. (A) Bright field image (upper) and DASPEI-stained neuromasts (lower) in two-year-old adults that developed fromshhA-mRNA injected surface fish embryos. The red dashes indicate the line of suborbital canal neuromasts in the head lateral line and the areas enclosed by the blue dashed lines indicate the SO-3 region. Scale bar in (lower panel of A) is 1.0 mm. (B-D) Regression analysis showing the relationship between eye diameter and (B) VAB level, (C) EO SN number and (D) SO-3 SN number inshhA-mRNA injected surface fish (gray dots) compared to uninjected surface fish (black dots). Linear regression line is shown in red. Eye degeneration did not result in the appearance of SN in the EO or increase VAB level inshh-overexpressed surface fish.
Figure 6
Figure 6
Schematic diagram showing correlations among four traits examined in this study. Yellow and green dots represent EO SN and SO-3 SN, respectively. Red arrows indicate significant positive correlations (denoted by "+"), shown in this study and previous studies [27]. The statistics of positive correlation between EO SN and SO-3 SN werer= 0.24,P< 0.001,n= 247. Black arrows with dotted lines indicate significant negative correlations (denoted by "-") determined in the present study.
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