BACKGROUND: Caudal fin symmetry characterizes teleosts and likely contributes to their evolutionary success. However, the coordinated development and patterning of skeletal elements establishing external symmetry remains incompletely understood. We explore the spatiotemporal emergence of caudal skeletal elements in zebrafish to consider evolutionary and developmental origins of caudal fin symmetry. RESULTS: Transgenic reporters and skeletal staining reveal that the hypural diastema-defining gap between hypurals 2 and 3 forms early and separates progenitors of two plates of connective tissue. Two sets of central principal rays (CPRs) synchronously, sequentially, and symmetrically emerge around the diastema. The two dorsal- and ventral-most rays (peripheral principal rays, PPRs) arise independently and earlier than adjacent CPRs. Muscle and tendon markers reveal that different muscles attach to CPR and PPR sets. CONCLUSIONS: We propose that caudal fin symmetry originates from a central organizer that establishes the hypural diastema and bidirectionally patterns surrounding tissue into two plates of connective tissue and two mirrored sets of CPRs. Further, two peripheral organizers unidirectionally specify PPRs, forming a symmetric "composite" fin derived from three fields. Distinct CPR and PPR ontogenies may represent developmental modules conferring ray identities, muscle connections, and biomechanical properties. Our model contextualizes mechanistic studies of teleost fin morphological variation.
BACKGROUND: Caudal fin symmetry characterizes teleosts and likely contributes to their evolutionary success. However, the coordinated development and patterning of skeletal elements establishing external symmetry remains incompletely understood. We explore the spatiotemporal emergence of caudal skeletal elements in zebrafish to consider evolutionary and developmental origins of caudal fin symmetry. RESULTS: Transgenic reporters and skeletal staining reveal that the hypural diastema-defining gap between hypurals 2 and 3 forms early and separates progenitors of two plates of connective tissue. Two sets of central principal rays (CPRs) synchronously, sequentially, and symmetrically emerge around the diastema. The two dorsal- and ventral-most rays (peripheral principal rays, PPRs) arise independently and earlier than adjacent CPRs. Muscle and tendon markers reveal that different muscles attach to CPR and PPR sets. CONCLUSIONS: We propose that caudal fin symmetry originates from a central organizer that establishes the hypural diastema and bidirectionally patterns surrounding tissue into two plates of connective tissue and two mirrored sets of CPRs. Further, two peripheral organizers unidirectionally specify PPRs, forming a symmetric "composite" fin derived from three fields. Distinct CPR and PPR ontogenies may represent developmental modules conferring ray identities, muscle connections, and biomechanical properties. Our model contextualizes mechanistic studies of teleost fin morphological variation.
Authors: Jacob M Daane; Nicola Blum; Jennifer Lanni; Helena Boldt; M Kathryn Iovine; Charles W Higdon; Stephen L Johnson; Nathan R Lovejoy; Matthew P Harris Journal: Curr Biol Date: 2021-09-16 Impact factor: 10.900
Authors: Lindsey Barske; Peter Fabian; Christine Hirschberger; David Jandzik; Tyler Square; Pengfei Xu; Nellie Nelson; Haoze Vincent Yu; Daniel M Medeiros; J Andrew Gillis; J Gage Crump Journal: Proc Natl Acad Sci U S A Date: 2020-09-21 Impact factor: 11.205
Authors: Erika Kague; Simon M Hughes; Elizabeth A Lawrence; Stephen Cross; Elizabeth Martin-Silverstone; Chrissy L Hammond; Yaniv Hinits Journal: FASEB J Date: 2019-05-17 Impact factor: 5.834
Authors: Hyo Sik Jang; Yujie Chen; Jiaxin Ge; Alicia N Wilkening; Yiran Hou; Hyung Joo Lee; You Rim Choi; Rebecca F Lowdon; Xiaoyun Xing; Daofeng Li; Charles K Kaufman; Stephen L Johnson; Ting Wang Journal: Genome Biol Date: 2021-10-04 Impact factor: 13.583