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. 2017 Dec;14(6):517-525.
doi: 10.1089/zeb.2017.1453. Epub 2017 Sep 21.

Thyroid Hormone Stimulates the Onset of Adult Feeding Kinematics in Zebrafish

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Free PMC article

Thyroid Hormone Stimulates the Onset of Adult Feeding Kinematics in Zebrafish

Sarah McMenamin et al. Zebrafish. .
Free PMC article

Abstract

The physical demands for swimming and feeding change dramatically over the course of development for many aquatic animals. Indeed, in teleosts, the transition from larva to adult involves major shifts in both trophic morphology and feeding behavior. A spike in thyroid hormone (TH) coordinates many developmental processes that occur during this adult transition in numerous vertebrate species. Using mutant and transgenic zebrafish, we tested the hypothesis that TH is essential for the transition from larval to adult feeding kinematic profiles. We found that every measured kinematic variable that distinguished larvae from adults also differentiated hypothyroid from wild-type (WT) euthyroid adults, suggesting that TH is indeed necessary for the onset of mature feeding behaviors. In contrast, feeding kinematics in hyperthyroid adults were extremely similar to those measured in euthyroid adults. Altered TH signaling underlies pedomorphosis in some amphibian species, and Danionella is a pedomorphic danionin genus. We therefore tested whether feeding kinematics of adult Danionella would more closely match larval zebrafish (and hypothyroid adults) than WT adult zebrafish. We found Danionella feeding kinematics resemble those of larval (and hypothyroid) zebrafish in multiple respects. Overall, we conclude that TH is essential in stimulating the onset of adult feeding kinematics in zebrafish, and that some of the underlying developmental pathways may have been lost in Danionella.

Keywords: behavior; developmental biology; other aquatic model species; zebrafish.

Conflict of interest statement

No competing financial interests exist.

Figures

<b>FIG. 1.</b>
FIG. 1.
Kinematic movements in different backgrounds. (A, A') Two angles and three distances were ultimately recorded from each strike; see text for measurement details. Note that these two images represent different frames and do not necessarily reflect the maximum measurement for any variable. (B–G) Example strikes from six groups of analyzed fish. Leftmost panels show the frames as the fish starts to open its mouth; next is the panel immediately before food is enveloped; next is the frame at which the fish shows maximum hyoid depression; rightmost panel shows the fish after the mouth completely closes. Arrowheads indicate prey item before envelopment. Asterisk in (B) indicates the high degree of cranial elevation in young larvae. Arrows in (D, E) indicate large amount of jaw protrusion in WT and hyperthyroid adults. Numbers in bottom left corners indicate the milliseconds from the frame at which prey item is enveloped. Scale bar = 1 mm. WT, wild type.
<b>FIG. 2.</b>
FIG. 2.
Kinematics change as fish grow, and these relationships are affected by thyroid hormone. Scatter plots show the relationships between fish size and maximum (A) gape distance, (B) gape angle, (C) cranial elevation angle, (D) jaw protrusion, and (E) hyoid depression. Measurement details in text. All WT groups shown as black dots; dashed lines show best fit lines for WT samples only. Asterisks of corresponding colors indicate that a group differs significantly from values predicted by regression (paired t test, p < 0.01).
<b>FIG. 3.</b>
FIG. 3.
Maximum kinematic excursions show that strikes of hypothyroid and Danionella adults resemble strikes of larvae. Box plots show the relative amount of maximum (A) gape distance, (B) gape angle, (C) cranial elevation angle, (D) jaw protrusion, and (E) hyoid depression. Measurement details in text. For most factors, the groups Larval and WT contain pooled samples of 8 dpf (light orange) with 30 dpf (dark orange), and AB (dark green) and DMSO (light green), respectively. Points are jittered for clarity. Letters indicate significance groups. DMSO, dimethyl sulfoxide; dpf, days postfertilization.
<b>FIG. 4.</b>
FIG. 4.
PCA separates larval from adult strike kinematics. PCA performed on the maximum excursion for each variable for every strike. The groups larval and WT contain pooled samples of 8 dpf (light-orange plus signs) with 30 dpf (dark-orange plus signs), and AB (dark-green triangles) and DMSO (light-green triangles), respectively. Shaded ovals show regions of 90% coverage for each group. PCA, principle components analysis.
<b>FIG. 5.</b>
FIG. 5.
Timing measurements show that strikes of hypothyroid and Danionella adults resemble strikes of larvae. Box plots show the time in milliseconds from food envelopment to different kinematic events: (A) opening of the mouth, (B) maximum gape distance, (C) maximum gape angle, (D) maximum cranial elevation, (E) maximum premaxillary protrusion, and (F) maximum hyoid depression. Colors as in Figure 3. Letters indicate significance groups.
<b>FIG. 6.</b>
FIG. 6.
PCA of strike timing. PCA includes all measured times of events, zeroed to the time at which the food is enveloped. The groups larval and WT contain pooled samples of 8 dpf (light-orange plus signs) with 30 dpf (dark-orange plus signs), and AB (dark-green triangles) and DMSO (light-green triangles), respectively. Transparent ovals show regions of 90% coverage for each group.

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