The Caudal Skeleton of the Zebrafish, Danio rerio, from a Phylogenetic Perspective: A Polyural Interpretation of Homologous Structures

Abstract

The structure of the caudal skeleton of extant teleost fishes has been interpreted in two different ways. In a diural interpretation, a caudal skeleton is composed of two centra articulated with one to six hypurals. Most subsequent authors have followed this interpretation. In contrast, a polyural interpretation considers the teleost fin to be derived from a fully metameristic ancestral bauplan originally composed of a one-to-one relationship between neural arches, centra (when present), and hypurals. Three different interpretations of the identity and homology of skeletal components of the caudal skeleton of the teleost fish Danio rerio have been proposed, two from a diural perspective and one from a polyural perspective. We examine each caudal skeletal component of Danio rerio from both a developmental and phylogenetic perspective. We propose that a polyural interpretation of structures is consistent with the current interpretation of the basal neopterygian caudal fin for this model organism rather than the older diural interpretation that does not take into account the metamerism observed in caudal structures during development. The polyural interpretation suggests several shared evolutionary innovations of major clades that would remain undiscovered under the older diural naming paradigm and makes the terminology of the parts of the caudal fin of Danio rerio strictly comparable to more basal fishes.

Fig. 1

Caudal fin ossifications and terminology. Lateral view of (A) Danio rerio (28 mm SL) drawn from University of Kansas specimen KU 29144 and (B) Moxostoma hubbsi (29.1 mm SL) redrawn from Grünbaum et al. (2003). ANs, accessory neural spine; E-?H3, putative epural of hypural 3; E-H3, epural of hypural 3; H1–H6, hypurals 1–6; ?H4, ?H5, ?H6, putative hypurals 5–6; HaPu2–3, haemal arches of Pu2 and Pu3; HD, hypural diastema; HsPu2–3, haemal spines of Pu2 and Pu3; mNa, membranous neural arch; NaPu1–3, neural arches of urostyle, Pu2, and Pu3; NsPu2–3, neural spines of Pu2 and Pu3 (double spine on Pu2 in Moxostoma hubbsi); Pu2–3, preural centra 2 and 3; Ph, parhypural; Un-U4, uroneurals of ural neural arch 4; Us, urostyle (U1+U2+U3+U4+pleurostyle+membrane ural neural arch).

Fig. 2

Immunostained caudal fins in early developmental stage. Lateral view of (A) Danio rerio (5.4 mm SL) and (B) Gasterosteus aculeatus (7.1 mm SL). Danio is stained with Collagen II (green) and DAPI (purple). Gasterosteus is stained with WGA (red) and DAPI (purple). EH-1, EH-2, epurals above hypurals 1 and 2; E-?H4, putative epural of H4; HD, hypural diastema; H1, H2, H4–6, hypurals 1, 2, 4, 5, and 6; H1–2, compound anterior hypural; H3–5, compound posterior hypural; Mc, mesenchyme field; NaPu1–2, neural arches of preural centra 1 and 2; Nc, notochord; Ph, parhypural. Scale bar is 0.1 mm.

Fig. 3

Early parhypural development in Danio. Lateral view of caudal region of Danio rerio (3.4 mm SL). Collagen II (green) and DAPI (blue) stain. Anterior left, dorsal up, axis inclined CCW about 45 degrees. Act, actinotrichia; MCN, mesenchyme cell nuclei; Nc, notochord; Ph, parhypural.

Fig. 4

Neural arch development in Danio. Lateral view of caudal region showing formation of the neural arch of preural centrum 1 of Danio rerio (5.3 mm SL) stained with Collagen II (green) and DAPI (blue). H1, H2, hypurals 1 and 2; HD, hypural diastema; HsPu2, haemal spine of Pu2; NaPu1, NaPu2, neural arches of preural centra 1 and 2; Nc, notochord; Ph, parhypural. Anterior is left; dorsal is up.

Fig. 5

Hypural development in Gasterosteus. Lateral view of the caudal region of Gasterosteus aculeatus (5.9 mm SL) stained with Collagen II (green) and DAPI (blue). H1–2, anterior compound hypural comprising chondrocytes that would normally form H1 and H2 in acanthomorphs with two anterior hypurals; H3–5, posterior compound hypural formed by chondrocytes normally forming H3–H5 in acanthomorph fishes; HD, hypural diastema; Nc, notochord; Ph, parhypural. Anterior is left; dorsal is up, specimen inclined.

Fig. 6

Development of the caudal fin. Caudal structures in young specimens of (A) Danio rerio redrawn and modified from Bensimon-Brito et al. (2012) and (B) Moxostoma hubbsi redrawn and modified from Grünbaum et al. (2003). Bone is lightly shaded, cartilage heavily shaded. E-H3, epural above H3; H1–H6, hypurals 1–6; HD, hypural diastema; HaPu2–3, haemal arches of Pu2–3; HsPu2–3, haemal spines of Pu2–3; mNa, membranous neural arches; NaPu1–3, neural arches of urostyle, Pu2, and Pu3; Nc, notochord; NsPu2–3, neural spines of Pu2–3; Opc, opisthural cartilage; Ph, parhypural; Pl, pleurostyle; Pu2–3, preural centra 2–3; U1–3, uroneurals 1–3; U1+U2, fused ural centrum 1 and ural centrum 2; U3+U4, fused ural centrum 3 and ural centrum 4; Un-U4, uroneural of ural neural arch 4. Note that the neural arch of preural centrum 1 is not show on this rendering of Danio rerio.