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Nat Commun
2011 Dec 20;2:592. doi: 10.1038/ncomms1603.
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Rapid adaptation to food availability by a dopamine-mediated morphogenetic response.
Adams DK
,
Sewell MA
,
Angerer RC
,
Angerer LM
.
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Food can act as a powerful stimulus, eliciting metabolic, behavioural and developmental responses. These phenotypic changes can alter ecological and evolutionary processes; yet, the molecular mechanisms underlying many plastic phenotypic responses remain unknown. Here we show that dopamine signalling through a type-D(2) receptor mediates developmental plasticity by regulating arm length in pre-feeding sea urchin larvae in response to food availability. Although prey-induced traits are often thought to improve food acquisition, the mechanism underlying this plastic response acts to reduce feeding structure size and subsequent feeding rate. Consequently, the developmental programme and/or maternal provisioning predetermine the maximum possible feeding rate, and food-induced dopamine signalling reduces food acquisition potential during periods of abundant resources to preserve maternal energetic reserves. Sea urchin larvae may have co-opted the widespread use of food-induced dopamine signalling from behavioural responses to instead alter their development.
Figure 2. Dopamine signaling through type-D2 receptors mediates inhibition of skeletal growth by algal sensation(a) Change in post-oral arm and body rod length for 5-day larvae treated with DRD2 agonist, quinpirole, at the indicated concentrations vs. control. One-way ANOVA for post-oral arm length, F3,463 = 30.586, P < 0.0001. Bonferroni-corrected comparisons vs. control; *** P < 0.001. The decrease in arm length was not due to a global response or sick embryos as body rod length and other aspects of larval morphology did not change with treatment. (b) Change in post-oral arm and body rod length for 5-day larvae cultured with vs. without algae for control (blue) and DRD2 antagonist amisulpride 25 μM (light gray) treatments. ANOVA (Supplementary Table S1), treatment×algae for post-oral arms, F1,363 = 7.005, P = 0.008 and for body rods, F1,345 = 1.584, P = 0.209; Bonferroni-corrected comparisons without vs. with algae (i.e. algae-induced change), *** P < 0.001. Error bars ± SEM. DRD2, dopamine receptor type-D2.
Figure 3. Dopamine biosynthesis is necessary for the response to algae(a) Change in post-oral arm and body rod length for 4-day larvae cultured with vs. without algae for control (blue) and a translation-blocking MASO at 0.4 mM (TH MASO1, light gray) treatments. ANOVA (Supplementary Table S2), treatment×algae for post-oral arms, F1,286 = 19.604, P < 0.001 and for body rods, F1,285 = 0.359, P = 0.550. Bonferroni-corrected comparisons without vs. with algae (i.e. algae-induced change), *** P < 0.001. (b) TH protein was not detectible in TH MASO1 injected embryos 4 days post-fertilization (right panel, n = 22/22 TH negative) as compared to controls (white arrow in left panel, n = 3/26 TH negative). Nuclei stained with DAPI (blue). Scale bars, 50 μm. (c) Change in post-oral arm and body rod length for 4-day larvae cultured with vs. without algae for control (blue) and a splice-blocking MASO at 0.15 mM (TH MASO2, light gray) treatments. Student's two-tailed t-test without vs. with algae, *** P < 0.001. (d) Change in post-oral arm and body rod length for 5-day larvae cultured with vs. without algae in control (blue) and TH inhibitor (light gray) treatments. ANOVA (Supplementary Table S3), treatment×algae for post-oral arms, F1,300 = 13.708, P < 0.001 and for body rods, F1,262 = 0.060, P = 0.807. Bonferroni-corrected comparisons without vs. with algae, *** P < 0.001. Error bars ± SEM. TH, tyrosine hydroxylase; MASO, morpholino anti-sense oligonucleotide.
Figure 4. Dopamine and dopamine biosynthesis enzymes are spatially and temporally expressed correctly to mediate the response to algaeFluorescent immunohistochemical detection of the rate-limiting dopamine biosynthesis enzyme, TH, and a PMC marker (SM30) for reference, at 54 hours post-fertilization (hpf) (a) and 60 hpf (b). White arrows in these and subsequent panels indicate the post-oral arm tip. (c) Post-oral arm length vs. hpf showing coincident initiation of arm elongation and first detection of TH-positive cells (black arrow). Gray dashed line indicates approximate length of an initial triradiate spicule. Error bars ± SEM. Fluorescent immunohistochemical detection of dopamine (d) and TH (e), and PMC markers, Msp130 (d) and SM30 (e), at pluteus stage (92 hpf). Fluorescent whole-mount in situ hybridization detecting ddc mRNA (f) in the post-oral arm tip and in the serotonergic ganglia (at the top of the image) at early pluteus (72 hpf, oral view). (g-j) Higher-magnification images of dopamine and PMC (Msp130) immunostains at the arm tip. Nuclei stained with DAPI (blue). DA, dopamine; TH, tyrosine hydroxylase; PMC, primary mesenchymal cell; ddc, dopa decarboxylase. Scale bars, (a-f) 50 μm, (g-j) 10 μm.
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