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Cryptic Variation in Morphological Evolution: HSP90 as a Capacitor for Loss of Eyes in Cavefish

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Science  13 Dec 2013:
Vol. 342, Issue 6164, pp. 1372-1375
DOI: 10.1126/science.1240276

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  1. Fig. 1 Reduction of HSP90 levels in A. mexicanus using the chemical inhibitor Radicicol.

    (A) Inhibition of HSP90 using 500 nM Radicicol leads to activation of BAG3 and HSPB1 (two-tailed t test, **P < 0.005, ***P < 0.0005). Time scale refers to hours of treatment. (B) Variable eye sizes in surface A. mexicanus larvae after treatment. (C) Quantification of eye size in adult F2 hybrids after larval treatment of Radicicol reveals a significant increase in SD of eye size, whereas average eye size is not affected (two-sided F test: P = 0.0004; Bartlett’s test, P = 0.001; Levene’s test, P = 0.03). Raising the fish in the dark alone does not affect eye size. Values were corrected for body size by using standard length of the fish. (D) Examples of eye size variation in F2 population of hybrid A. mexicanus.

  2. Fig. 2 HSP90 inhibition in natural populations of A. mexicanus.

    (A and B) HSP90 inhibition in natural populations of surface A. mexicanus leads to an increase of variation in (A) eye size and (B) orbit size. Eye size SD, +83%; two-sided F test, P = 8.1 × 10–6; Bartlett’s test, P < 0.001; Levene’s test, P < 0.001; orbit size SD, +108%; two-sided F test: P = 3.4 × 10–6; Bartlett’s test, P < 0.001; Levene’s test, P < 0.001. (C) Orbit size decreases after Radicicol treatment in Tinaja cave populations (t test, P = 0.02), while change in variation is observed (SD, –12%; two-sided F test, P = 0.239). Control is DMSO. Asterisks in (A) and (B) compare SDs, whereas in (C), asterisks compare averages.

  3. Fig. 3 Genetic assimilation.

    (A and B) Selection for small eye size in surface fish generated by Radicicol treatment resulted in offspring with significantly smaller (A) orbit size and (B) eye size in the absence of treatment (two-tailed t test, P = 6.5 × 10–13 for orbit size; P = 7.2 × 10–16 for eye size). The resultant range exceeded the range seen in any cross of untreated surface fish.

  4. Fig. 4 Low-conductivity conditions in the cave natural habitat have a similar effect to Radicicol treatment on surface populations.

    (A) Quantitative reverse transcription polymerase chain reaction of BAG3 and HSPB1 for surface fish reared under low-conducitivity (230 μS) conditions compared with control conductivity conditions (two-tailed t test, *P < 0.05; **P < 0.005; ***P < 0.0005). Time scale refers to hours of treatment. (B and C) Lower-conductivity conditions reveal an increase in variation of (B) orbit size and (C) eye size (eye size SD, +50%; two-sided F test, P = 0.0018; Bartlett’s test, P = 0.006; Levene’s test, P = 0.005; orbit size SD, +58%; two-sided F test: P = 5.9 × 10–4; Bartlett’s test, P = 0.001; Levene’s test, P = 0.01).