Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics

Abstract

Protrusile jaws are a highly useful innovation that has been linked to extensive diversification in fish feeding ecology. Jaw protrusion can enhance the performance of multiple functions, such as suction production and capturing elusive prey. Identifying the developmental factors that alter protrusion ability will improve our understanding of fish diversification. In the zebrafish protrusion arises postmetamorphosis. Fish metamorphosis typically includes significant changes in trophic morphology, accompanies a shift in feeding niche and coincides with increased thyroid hormone production. We tested whether thyroid hormone affects the development of zebrafish feeding mechanics. We found that it affected all developmental stages examined, but that effects were most pronounced after metamorphosis. Thyroid hormone levels affected the development of jaw morphology, feeding mechanics, shape variation, and cranial ossification. Adult zebrafish utilize protrusile jaws, but an absence of thyroid hormone impaired development of the premaxillary bone, which is critical to jaw protrusion. Premaxillae from early juvenile zebrafish and hypothyroid adult zebrafish resemble those from adults in the genera Danionella, Devario, and Microdevario that show little to no jaw protrusion. Our findings suggest that evolutionary changes in how the developing skulls of danionin minnows respond to thyroid hormone may have promoted diversification into different feeding niches.

Functional morphogenesis from embryos to adults: Late development shapes trophic niche in coral reef damselfishes

“…They experience water as a “sticky” fluid that can reduce the effectiveness of many adult feeding strategies (Hernandez, ). Jaw protrusion, for example, facilitates zooplankton capture by pelagic‐feeding adult damselfishes (Cooper et al, ; Coughlin & Strickler, ), but jaw protrusion would likely interfere with zooplanktivory in a viscous fluid by pushing prey away from a larval fish (Galindo et al, ). Zebrafish ( Danio rerio ) use protrusile jaws to capture zooplankton as adults, but employ little or no jaw protrusion when feeding on zooplankton as larvae (Galindo et al, ; McMenamin, Carter, & Cooper, ).…”

“…Jaw protrusion, for example, facilitates zooplankton capture by pelagic‐feeding adult damselfishes (Cooper et al, ; Coughlin & Strickler, ), but jaw protrusion would likely interfere with zooplanktivory in a viscous fluid by pushing prey away from a larval fish (Galindo et al, ). Zebrafish ( Danio rerio ) use protrusile jaws to capture zooplankton as adults, but employ little or no jaw protrusion when feeding on zooplankton as larvae (Galindo et al, ; McMenamin, Carter, & Cooper, ). The extent and speed of other cranial motions are also significantly different in larval and adult zebrafish during zooplankton capture (Galindo et al, ; McMenamin et al, ).…”

“…Zebrafish ( Danio rerio ) use protrusile jaws to capture zooplankton as adults, but employ little or no jaw protrusion when feeding on zooplankton as larvae (Galindo et al, ; McMenamin, Carter, & Cooper, ). The extent and speed of other cranial motions are also significantly different in larval and adult zebrafish during zooplankton capture (Galindo et al, ; McMenamin et al, ). Because the biomechanical requirements for zooplanktivory are different for adult and larval fishes, pelagic‐feeding damselfishes are also likely to require postlarval cranial remodeling.…”

“…TH is also known to play an important role in skull morphogenesis throughout development and to have large effects on the growth and remodeling of both endochondral and intramembranous bone (Bassett & Williams, ; Hanken & Hall, ; Harvey et al, ; Hirano, Akita, & Fujii, ; Waung, Bassett, & Williams, ; Wojcicka et al, ). Experimental work with genetically modified zebrafish ( D. rerio ; Cyprinidae) has shown that individuals which cannot manufacture TH will retain many aspects of larval feeding mechanics into adulthood (Galindo et al, ; McMenamin et al, ). There is also evidence that changes in TH signaling have played an important role in the evolution of skull mechanics within the cypriniform lineage to which the zebrafish belongs (Galindo et al, ; McMenamin et al, ; Shkil & Smirnov, ; Shkil et al, ; Shkil, Kapitanova, Borisov, Abdissa, & Smirnov, ).…”

“…Experimental work with genetically modified zebrafish ( D. rerio ; Cyprinidae) has shown that individuals which cannot manufacture TH will retain many aspects of larval feeding mechanics into adulthood (Galindo et al, ; McMenamin et al, ). There is also evidence that changes in TH signaling have played an important role in the evolution of skull mechanics within the cypriniform lineage to which the zebrafish belongs (Galindo et al, ; McMenamin et al, ; Shkil & Smirnov, ; Shkil et al, ; Shkil, Kapitanova, Borisov, Abdissa, & Smirnov, ). Further investigation into the mechanisms through which TH affects larval skull reorganization is likely to inform our understanding of trophic evolution in fishes.…”