XB-ART-54785
BMC Dev Biol
2018 Apr 03;181:8. doi: 10.1186/s12861-018-0166-4.
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The skeletal ontogeny of Astatotilapia burtoni - a direct-developing model system for the evolution and development of the teleost body plan.
Woltering JM
,
Holzem M
,
Schneider RF
,
Nanos V
,
Meyer A
.
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BACKGROUND: The experimental approach to the evolution and development of the vertebrate skeleton has to a large extent relied on "direct-developing" amniote model organisms, such as the mouse and the chicken. These organisms can however only be partially informative where it concerns secondarily lost features or anatomical novelties not present in their lineages. The widely used anamniotes Xenopus and zebrafish are "indirect-developing" organisms that proceed through an extended time as free-living larvae, before adopting many aspects of their adult morphology, complicating experiments at these stages, and increasing the risk for lethal pleiotropic effects using genetic strategies. RESULTS: Here, we provide a detailed description of the development of the osteology of the African mouthbrooding cichlid Astatotilapia burtoni, primarily focusing on the trunk (spinal column, ribs and epicentrals) and the appendicular skeleton (pectoral, pelvic, dorsal, anal, caudal fins and scales), and to a lesser extent on the cranium. We show that this species has an extremely "direct" mode of development, attains an adult body plan within 2 weeks after fertilization while living off its yolk supply only, and does not pass through a prolonged larval period. CONCLUSIONS: As husbandry of this species is easy, generation time is short, and the species is amenable to genetic targeting strategies through microinjection, we suggest that the use of this direct-developing cichlid will provide a valuable model system for the study of the vertebrate body plan, particularly where it concerns the evolution and development of fish or teleost specific traits. Based on our results we comment on the development of the homocercal caudal fin, on shared ontogenetic patterns between pectoral and pelvic girdles, and on the evolution of fin spines as novelty in acanthomorph fishes. We discuss the differences between "direct" and "indirect" developing actinopterygians using a comparison between zebrafish and A. burtoni development.
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293700 European Research Council
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Fig. 1. Astatotilapia burtoni morphology, distribution and husbandry. a A. burtoni shows pronounced sexual dimorphism, with colorful dominant males with their characteristic egg spots on the anal fin (black arrowhead), and plain females. b A. burtoni is native to Lake Tangayika in the East African Rift Valley, with additional, introduced populations western of Lake Victoria (distribution after IUCN 2006, geographical boundaries drawn after Google earth 2017). c Typical tank set up for A. burtoni to house a breeding group of 20–40 adult fish. Aquaria do not need to be planted but are best decorated with gravel and numerous rocks and hiding places, such as upturned half-flowerpots, which the fish will use during their mating rituals. d Mouthbrooding females can be recognized by their expanded lower jaw, leading to a pronounced “chin” in profile view (white arrowhead) | |
Fig. 2. Early embryonic development of A. burtoni. a On the day of fertilization (0 dpf) embryos develop until gastrulation – (shown is a blastula stage embryo, ~ stage 5). As in other teleosts, embryos develop on top of the yolk. b, c At 1 dpf, the neural tube and a head Anlage have formed (stage 10 shown). d, e By 2 dpf (stage 14), the embryos have developed pigmentation on the yolk, and a clear head can be distinguished, with presence of the mid-hindbrain boundary, otic vesicles and unpigmented eyes. At this stage, embryos are still surrounded by their chorion and the embryo shown has been manually dechorionated. f, g By 3 dpf (stage 15), the anterior-posterior axis has elongated further, pectoral fin Anlagen have appeared, and a clearly beating heart is visible. The eyes have developed light pigmentation. Also at this stage, embryos are still surrounded by their chorion, and the embryo shown has been manually dechorionated. h, i By 4 dpf (stage 17), the head has lifted up from the yolk, strong blood circulation through the heart is visible, and extensive vasculature runs across the yolk. All stages are indicated following the staging table for Nile tilapia [41]. Abbreviations: dpf: days post fertilization; st.: stage; BD: blastodisc; NT: neural tube; MHB: mid-hindbrain boundary; E: eye; OV: otic vesicle; PF: pectoral fin; H: heart; HA: Head Anlage | |
Fig. 3. Late embryonic development of A. burtoni. a After hatching, embryos rapidly develop their adult morphology, whereby at 13 dpf essentially all structures of the body plan are present. b Ventral view during 11–13 dpf shows progressive closure of the body wall over the yolk during these stages (white arrowheads). All stages are indicated following the staging table for Nile tilapia [41]. Abbreviations: dpf: days post fertilization; st.: stage | |
Fig. 4. Osteology of the axial and median fin skeleton of A. burtoni. a, b Alizarin red/Alcian blue stained and cleared skeleton of an adult fish shows a typical teleost skeleton, consisting of a spinal column with associated elements, and pectoral, pelvic, dorsal, anal and caudal fins. The axial skeleton consists of pre-caudal, caudal and ural regions. Vertebral centra and associated arches and spines are drawn as fused units. Two anterior ribless vertebrae followed by around 10 rib-bearing vertebrae form the pre-caudal region. The caudal region consists of around 12 ribless vertebrae. The vertebral column terminates posteriorly in the ural region, which consists of highly modified vertebral elements and arches supporting the caudal fin rays. Other accessory elements present to the vertebrae are the epicentrals, also known as dorsal ribs (see main text), which are membrane bones without homologs in tetrapods. In panel a note the presence of the pelvic fins on the anterior abdomen at the same anterior-posterior level as he pectoral fins. Dorsal and anal fins consist of an anterior domain containing fin spines and a posterior domain with soft fin rays, each shown for the dorsal fin in a zoom-box in panel a | |
Fig. 5. Development of the axial skeleton of A. burtoni. a Neural and haemal arches develop between 102 hpf and 126 hpf, as shown by Alcian blue staining. In teleost fish, vertebral centra do not form through a cartilaginous intermediate, and ossified centra become first visible by Alizarin red staining (fluorescent microscopy image) at 138 hpf. Blue asterisk in 126 hpf indicates absence of mineralized centra. b Visualization of somites, using the muscle sarcomere specific antibody MF20 together with Alcian blue staining, shows that the basioccipital (yellow arrowhead) has formed by 100 hpf within somites 1 and 2, and extends up to the somite 2–3 boundary. The first developing neural arch is present in somite 4. This shows that, as in other anamniotes, the basioccipital develops from the first three somites. The horizontal dotted line indicates the somite 2–3 boundary. c Ribs develop around 138 hpf (red arrowhead). Interestingly, we observe what appear to be rib Anlagen associated with pre-caudal vertebrae 1 and 2 (indicated with a red asterisk), which in the adult skeleton are not rib-bearing. At 156 hpf, these “cryptic” ribs are however no longer present (indicated with a red asterisk). Epicentrals develop much later and only start developing around 9 dpf as membrane bones (black arrowhead indicates epicentral on pre-caudal vertebra 1; the black asterisk indicates the forming epicentral on pre-caudal vertebra 2; the blue arrowhead indicates a transversal process on pre-caudal vertebra 4, which is not further discussed here). d The axial skeleton forms in the following sequence: the first element to appear is the basioccipital (stage I, before 100 hpf), followed by the formation of neural and haemal arches dorsal and ventral of the notochord (stage II and III). Further elements to appear are the vertebral centra and the ribs (stage IV), followed by the epicentrals (stage V). Abbreviations: dpf: days post fertilization; hpf: hours post fertilization; AZR: Alizarin red | |
Fig. 6. Development of the anal and dorsal fins of A. burtoni. a The first dorsal and anal fin Anlagen are visible at hatching day (4 dpf) as a fin fold that is continuous with the caudal fin. In the anal fin fold, the domain of the final anal fin is recognizable by the lack of vascularization (black arrowhead in lower panel), which is restricted to the part of the fin fold that will degenerate. b At 6 dpf, mesenchymal condensations become visible proximally in the posterior dorsal and anal fins (indicated with a black arrowhead for the dorsal fin). These condensations correspond to tissue surrounding the forming fin radials (see transition from 138 hpf to 156 hpf in panel c). c Alcian blue staining shows the progression of dorsal and anal fin formation. At 138 hpf, a fin fold is present without detectable skeletal structures (asterisk). By 156 hpf, fin radials have formed (blue arrowhead), but no ray structures are apparent yet in the fin fold (asterisk). By 172 hpf, fin rays start forming (black arrowhead). The last elements to appear are the distal radials in between the proximal radials and the fin rays, and these appear around 198 hpf. d Initially, fin spines and soft-rays look very similar. By 10 dpf, their differentiation has progressed and clearly shows diverging developmental trajectories. Fin spines have developed a pointy ending, and segmentation is apparent in the soft-rays (black arrowheads). e At 13 dpf, ossification in the soft-rays and spines in dorsal and anal fins has progressed, and clearly demonstrates stronger ossification of the spines compared to soft rays. Upper panel shows bright-field view, lower panel shows fluorescent imaging for Alizarin red staining in the same specimen. Abbreviations: dpf: days post fertilization; hpf: hours post fertilization; AZR: Alizarin red; S: spines, SR: soft-rays | |
Fig. 7. Development of the pectoral fins and girdles of A. burtoni. a, b The pectoral girdles and fins of A. burtoni show the typical teleost anatomy. The girdle consists of two dermal bones, the cleithrum and the post-cleithrum, and two endochondral bones, the scapula and coracoid (indicated S and C in panel b). The pectoral fins consist of proximal radials that articulate via distal radials with the main external fin support, the dermal fin rays. The propterygium (see main text) is present as a separate radial during embryogenesis but is in the adult fused to the scapula. Shown is an Alizarin red/Alcian blue stained pectoral fin/girdle complex of an adult fish. c, d Alcian blue stained sequence of pectoral fin development (see main text for details). The cleithrum is indicated from 84 hpf to 138 hpf. Distal radials appear first at 174 hpf, and are present but not indicated in 180 hpf to 222 hpf. The post-cleithrum, which is only visible through its different contrast, is only indicated in 126 hpf and 192 hpf. Abbreviations: hpf: hours post fertilization; S: scapula; C: coracoid | |
Fig. 8. Development of the pectoral girdle of A. burtoni. a Visualization of ossification by fluorescent imaging of Alizarin red stained embryos. At 6 dpf and 7 dpf, only the cleithrum has ossified, followed by the fin rays and the post-cleithrum at 9 dpf. Embryos shown were also stained for Alcian blue, which in the fluorescent images shows cartilaginous elements as a dark counterstain. In the drawing these unossified endoskeletal girdle and fin elements are indicated in grey. Cb In situ hybridization for collagenX visualizes the ossifying dermal bones in the same sequence but approximately one day in advance of the mineralization process as detected by Alizarin red staining. Abbreviations: dpf: days post fertilization; AZR: Alizarin red | |
Fig. 9. Development of the pelvic fins and girdle of A. burtoni. a Alizarin red/Alcian blue stain of the adult paired pelvic girdle (ventral view, both left and right side elements are present). The pelvic girdle consists of a single element (the basipterygium) that directly articulates with the fin rays, without presence of proximal or distal radials (see zoom in on the dissected left fin). The most anterior fin ray is unbranched and unsegmented, and has the identity of a spine (indicated with “S”), while the other rays have soft-ray morphology. b, c Alcian blue (198 hpf-240 hpf) and Alcian blue/Alizarin red stained (12 dpf − 16 dpf) pelvic girdle/fin complexes. The first elements of the pelvic fin skeleton appear around 198 hpf as a split chondrogenic condensation, which at 240 hpf has elongated and developed a distinct “forked” appearance. Between 240 hpf (10 dpf) and 12 dpf, the forked ends become connected through intermediate occurring cartilaginous growth, possibly homologous to the endoskeletal elements of the pectoral fins (blue arrowhead, indicated “endoskeletal disk”). Fin rays develop from 240 hpf onwards (indicated black arrowhead). Abbreviations: dpf: days post fertilization; hpf: hours post fertilization; S: spine | |
Fig. 10. Development of the caudal fin of A. burtoni. a, b Osteology of the adult caudal fin of A. burtoni as detected by Alizarin red staining (fluorescence image in panel a. A. burtoni has a typical acanthomorph caudal fin consisting of five hypurals (I-V), a parahypural, two epurals (I, II), a urostyle, and two haemal and neural spines, contributing to the support of the dermal fin rays. Note the highly modified neural spine on the second pre-ural centrum (PU-2) that forms a complex articulation with the first epural. c Alcian blue staining shows that the first elements to appear are the hypurals and parahypural aroud 120 hpf. This is followed by the appearance of the haemal and neural arches on pre-ural centra 2 and 3 around 132 hpf. The epurals appear later, between 156 hpf and 180 hpf. By 260 hpf (Alcian blue/Alizarin red double stain), the uroneural has developed as a directly ossifying membrane bone. The developing notochord is indicated using a grey asterisk in the 72 hpf specimen. Abbreviations (except those explained at the bottom of the figure): hpf: hours post fertilization | |
Fig. 11. Scale development in A. burtoni. a Adult scales stained using Alizarin red. Scales are present in an organized arrangement, whereby their proximal-distal axis is aligned anterior-posteriorly along the trunk. Proximally, scales are overlapped by the distal part of their anterior/lateral neighboring scale(s). In the left panel, the outline of one scale is drawn using a dotted line for the proximal part that is covered by the flanking scales. In the right panel, a close up of a single scale is shown. The scales consist of concentric rings of bone, and spike elements distally, the ctenii. The scales attach to the body through their proximal end. b During development, scale Anlagen are first detected at 7 dpf, using in situ hybridization with the ossification marker collagenX, as a single row along the posterior midline (indicated “1” in the drawing to the right). At 8 dpf, one more row dorsally and one more row ventrally have appeared (indicated “2” in the drawing to the right), while the initial row has expanded anteriorly. At 9 dpf, this process has been repeated with the appearance of an additional dorsal and ventral row of scales (indicated “3” in the drawing to the right). c At 13 dpf, bone mineralization in the scales is present along the posterior trunk where they were first formed (zoom-in right panel), while more anteriorly, mineralization is still absent or less pronounced. Shown is a fluorescence image of an Alizarin red stained specimen. Abbreviations: AZR: Alizarin red; dpf: days post fertilization | |
Fig. 12. Chondrification of the cranial skeleton in A. burtoni. Chondrified elements of the cranio-facial skeleton are detected using staining with Alcian blue. At 3 dpf, no chondrogenic differentiation of the craniofacial skeleton is yet detected At 4 dpf, the first elements corresponding to the pharyngeal skeleton become vissible and differentiate rapidly, so that at 5 dpf, the full complement of pharyngeal cartilages has formed. The schematic illustration of the chondrogenic cartilages present is for 6 dpf. Abbreviations: dpf: days post fertilization | |
Fig. 13. Ossification of the cranio-facial skeleton in A. burtoni. At 6 dpf, ongoing ossification can be detected in the craniofacial skeleton using in situ hybridization with collagenX. This clearly visualizes the formation of the branchiostegal rays (red arrowhead), which form without a cartilage intermediate (compare 6 dpf in Fig. 12). At 9 dpf, most of the adult bones of the cranio-facial skeleton have started ossification, as shown by Alizarin red staining (fluorescence microscopy images shown), and the formation of teeth has started (orange arrowhead). Full formation of the complete opercular series (opercle, infraopercle, subopercle and preopercle) is shown for a 13 dpf specimen. Note that many bones in the skull form without a cartilaginous intermediate. Therefore, there is no one to one correspondence between the chondrogenic elements in Fig. 12 and the ossifying elements in Fig. 13. The legend in the figure indicates for which specimen each anatomical element is indicated. Abbreviations: l: lateral view; v: ventral view; f: frontal view; dpf: days post fertilization | |
Fig. 14. Direct- versus indirect-development – A. burtoni versus zebrafish. The direct-development of A. burtoni (blue) is characterized by the completion of the body plan before the onset of feeding (embryo to larva transition at 14 dpf). This is reflected in a very homogenous progression of development, as has been described in this paper, and a very homogenous overall growth with only minor variation in standard length (Y-axis, data points included for 10 embryos/juveniles per day coming from different clutches). In comparison, zebrafish (red) develops only synchronously until the start of the embryo to larva transition, marked by the onset of feeding at 5 dpf. After this point, growth trajectories of individual fish strongly diverge (data range included from Parichi et al. 2009 [22], a very similar range was described in Grandel & Schulte-Merker 1998 [25]). The zebrafish' larva- to juvenile transition is indicated after references [4, 22]. When we consider the development of the pectoral fins for zebrafish (after [25]) and A. burtoni (this article), we see that in both species these follow very similar developmental trajectories (stages indicated after Fig. 7). In A. burtoni, pectoral fin formation is completed before 10 dpf, well before feeding stages, and differentiation occurs at a steady progression, and is predictable amongst individuals from the same clutch (developmental progression indicated along the X-axis in relation to time after fertilization). In zebrafish, pectoral fin formation starts similar with the formation of the endoskeletal disk (stage II). From the embryo to larva transition onward however, overall development slows down and growth becomes heterogeneous amongst similarly aged larvae. Therefore, time is not a good predictor of the progression of pectoral fin development, but standard length has to be used instead (pectoral fin stages indicated along the Y-axis in relation to standard length). Abbreviations: dpf: days post fertilization; SL: standard length | |
Fig. 15. Overview of the sequence of development of the post-cranial skeleton of A. burtoni. Schematic representation of the development of the various morphological aspects described for the axial skeleton as well as the pectoral, pelvic, dorsal/anal and caudal fins, with the anatomical structures aligned along the X-axis and their development shown according to time (dpf) on the Y-axis. No timeline for craniofacial elements is included. Abbreviations: dpf: days post fertilization |
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