The skeletal ontogeny of Astatotilapia burtoni – a direct-developing model system for the evolution and development of the teleost body plan

Abstract

BackgroundThe 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.ResultsHere, 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.ConclusionsAs 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.

Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus

“…In contrast to the zebrafish where adult color pattern develops indirectly during a post-embryonic metamorphic phase (Parichy et al, 2009), the vertical bars in H. latifasciatus develop directly and are already visible at a time when the larvae are still feeding from their yolk. This is in line with previous reports on the direct development of other morphological traits of African cichlid fishes (Woltering et al, 2018).…”

Patterning the spine

“…This would be in agreement with the findings of Lleras-Forero et al, which showed potential interaction between the notochord and somites, reinforcing the pattern of the forming vertebral components. Work in ‘indirect’ developing salamanders and ‘direct’ developing fish give support to this proposition ( Figure 1B ; Slijepčević et al, 2018 ; Woltering et al, 2018 ). By this model, the early formation of the mineralized, segmented notochord in zebrafish may dissociate, or even expose, these two patterning mechanisms.…”

“…(4) Direct development strategies (e.g. Woltering et al, 2018 ), which have a contemporary activation of pattern mechanisms; here a somite signal masks a putative influence of the notochord. (5) In tetrapod vertebrates, in which the influence of the notochord is reduced or masked, the vertebrae arise from somites, and cartilage-derived tissue forms an arcocentrum (light blue).…”

Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris)

“…For example, Parichy et al used the flexion angle as developmental criteria, but, as in goldfish, this criterion seems not obvious to apply for clownfish, as in our conditions it is difficult to measure in late‐stage larvae due to their pigmentation, which covers the notochord. To determine flexion of the notochord, we used the position of the hypural bones, as it is commonly used in descriptions of larval fish development . As in many fish species, hypural bones are the first skeletal structures to appear in the caudal fin .…”