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Skeletal development in the heterocercal caudal fin of spotted gar (lepisosteus oculatus) and other lepisosteiformes - PubMed

Skeletal development in the heterocercal caudal fin of spotted gar (lepisosteus oculatus) and other lepisosteiformes

Thomas Desvignes et al. Dev Dyn. 2018 May.

Abstract

Background: The caudal fin of actinopterygians experienced substantial morphological changes during evolution. In basal actinopterygians, the caudal fin skeleton supports an asymmetrical heterocercal caudal fin, while most teleosts have a symmetrical homocercal caudal fin. The transition from the ancestral heterocercal form to the derived homocercal caudal fin remains poorly understood. Few developmental studies provide an understanding of derived and ancestral characters among basal actinopterygians. To fill this gap, we examined the development of the caudal fin of spotted gar Lepisosteus oculatus, one of only eight living species of Holostei, the sister group to the teleosts.

Results: Our observations of animals from fertilization to more than a year old provide the most detailed description of the development of caudal fin skeletal elements in any Holostean species. We observed two different types of distal caudal radials replacing two transient plates of connective tissue, identifying two hypaxial ensembles separated by a space between hypurals 2 and 3. These features have not been described in any gar species, but can be observed in other gar species, and thus represent anatomical structures common to lepisosteiformes.

Conclusions: The present work highlights the power and importance of ontogenic studies and provides bases for future evolutionary and morphological investigations on actinopterygians fins. Developmental Dynamics 247:724-740, 2018. © 2018 Wiley Periodicals, Inc.

Keywords: Holostei; actinopterygian; morphology; ontogeny; skeletogenesis; tail.

© 2018 Wiley Periodicals, Inc.

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Figures

Figure 1
Figure 1

Spotted gar caudal fin organization and development. (A) Caudal portion of a skeletonized adult spotted gar (471 mm SL), left view. (B) Schematic representation of the spotted gar caudal fin skeleton, left view. (C) Sample distribution by 5 mm size classes (Standard Length (SL) in mm) and by type of staining: green, Alcian Blue + Alizarin Red; blue, Alcian Blue only; red, Alizarin Red only. (D) Age-length relationship of developing spotted gars from 7 days post fertilization (dpf) and 121 dpf. The black solid line represents the average total length (TL, in mm) and the dashed blue lines represent ± one standard deviation (SD) from the average TL. Abbreviations: c, centrum; cfr, caudal fin rays; darc, dorsal arcualia; dcr, distal radials; ep, epural; fub, basal fulcra; fufr, fringing fulcra; ha, haemal arch; hs, haemal spine; hyp, hypural; na, neural arch; nsp, paired neural spines; phy, parhypural; pp, parapophysis; pu, preural centra; u, ural centra.

Figure 2
Figure 2

Sequence of development and ossification of individual caudal fin skeletal elements based on median values. Diamonds indicate earliest appearance of elements by cell condensation. Blue indicates Alcian Blue uptake and development of cartilage. The blue-to-red transition represents the progression of ossification. Red represents fully mineralized structures. Less opaque bars refer to elements found in less than 25% of the studied specimens.

Figure 3
Figure 3

External view of spotted gar caudal fin development. (A) 7.5 mm TL, equivalent Stage 25 (Braasch et al., 2015; Long and Ballard, 2001). (B) 13 mm TL, equivalent Stage 31. (C) 22.5 SL, 30.5 mm TL. (D) 147 mm SL, 174 mm TL. (E) 200 mm SL, 252 mm TL. The dotted line in (B) denotes the margin of the larval fin fold. The dotted line in (E) highlights the almost symmetrical shape of the adult spotted gar caudal fin. The dashed line demarcates the oblique delimitation of the boundary between the scaled caudal peduncle and the caudal fin rays, which contribute to most of perceived asymmetry. Abbreviations: af, anal fin; av, anal vent; df, dorsal fin; el, epichordal lobe of the caudal fin; ff, fin fold; fub, basal fulcra; hl, hypochordal lobe of the caudal fin; int, intestine; ol, opisthural lobe; nc, notochord; y, yolk.

Figure 4
Figure 4

Developmental sequence of the spotted gar caudal fin skeleton. (A) 12 mm SL. (B) 13 mm SL. (C) 15 mm SL. (D) 21 mm SL. (E) 62 mm SL. (F) 416 mm SL. The white elongated triangle indicates hypural 1 as a reference point. Scale bars indicate 1 mm. Abbreviations: bv, basiventral arcualia; cfr, caudal fin rays; darc, dorsal arcualia; ep, epural; fub, basal fulcra; fufr, fringing fulcra; hs, haemal spine; hyp, hypural; nc, notochord; pu1, preural centrum 1; u, ural centra; u1, ural centrum 1.

Figure 5
Figure 5

Detailed development of major caudal fin skeletal elements in spotted gar. (A) 16 mm SL, sagittal section. (B) 13 mm SL. (C) 61 mm SL. (D) 12 mm SL. (E) 10 mm SL. (F) 14 mm SL. (G) 60 mm SL. (H) 61 mm SL. (I) 79 mm SL. (J) 17 mm SL. (K) 23 mm SL. (L) 37 mm SL. (M) Schematic representation of developmental dynamics of caudal fin skeletal elements. The origin of the arrow marks the first element to form and the arrowhead indicates the direction of developmental progression. The white elongated triangle indicates hypural 1 as a reference point, and the black arrow points at the gap between the two plates of connective tissue and the change of size and shape in hypurals. Small equilateral white triangles indicate haemal elements supporting caudal fin rays. Small black equilateral triangles indicate haemal elements not supporting caudal fin rays. Scale bar in (A) indicates 100 μm; other scale bars indicate 1 mm. Abbreviations: bv, basiventral arcualia; darc, dorsal arcualia; dcr, distal caudal radials; ep, epural; fub, basal fulcra; ha, haemal arch; hs, haemal spine; hyp, hypural; hyp1, hypural 1; na, neural arch; nc, notochord; ns, neural spine; phy, parhypural; pp, parapophysis; pu1, preural centrum 1; u1, ural centrum 1.

Figure 6
Figure 6

Variation in hypurals and epurals among gar individuals. (A) 165 mm SL. (B) 58 mm SL. (C) 219 mm SL. (D) 75 mm SL. (E) Regression of the number of epurals against the number of hypurals in individuals having all skeletal elements formed. The size of each circle denotes the number of specimens displaying indicated number of hypurals and epurals. (F) 103 mm SL. In (A), (B) and (F), the white elongated triangle indicates hypural 1; in (A) and (B), the grey elongated triangle points at hypural 2 and more posterior hypurals. Scale bars indicate 1 mm. Abbreviations: avp-hyp1, antero-ventral process of hypural 1; ep, epurals; hyp, hypurals.

Figure 7
Figure 7

Caudal fulcra in spotted gar. (A) 90 mm SL. (B & E) 416 mm SL. (C & F) 471 mm SL. (D) 98 mm SL. Alcian Blue Alizarin Red cleared and stained dorsal (A) and ventral (D) basal fulcra dissected and flat mounted; Alcian Blue Alizarin Red cleared and stained dorsal (B) and ventral (E) fulcra; demerstid beetle cleaned dorsal (C) and ventral (F) fulcra. Scale bars indicate 1 mm. Abbreviations: cfr, caudal fin rays; fub, unpaired basal fulcra; fufr, fringing fulcra; or, ornamentation; pfub, paired basal fulcra; sca, scales.

Figure 8
Figure 8

The gar caudal fin is organized around two plates of connective tissue. (A) 43 mm SL. (B) 62 mm SL. (C) 184 mm SL. Animals were stained with Alcian Blue and Alizarin Red. Scale bars indicate 1 mm. (D–E) 17 mm SL, cross section; scale bar is 100 μm; (F) 17 mm SL, sagittal section, scale bar is 100 μm; (F′) 17 mm SL, sagittal section, scale bar is 25 μm. D–F are sections stained with Alcian Blue and counter stained with Nuclear Fast Red. The white elongated triangle indicates hypural 1 and the black arrow points at the hypural diastema. Abbreviations: pdcr, post-element distal caudal radials; idcr, intercalated distal caudal radials; hs, haemal spin; hyp, hypural; nc, notochord; pct, plate of connective tissue; pcta, anterior plate of connective tissue; pctp, posterior plate of connective tissue.

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