Development and evolution of craniofacial patterning is mediated by eye‐dependent and ‐independent processes in the cavefish Astyanax

Abstract

We studied the development and evolution of craniofacial features in the teleost fish, Astyanax mexicanus. This species has an eyed surface dwelling form (surface fish) and many different cave dwelling forms (cavefish) with various degrees of reduced eyes and pigmentation. The craniofacial features we examined are the tooth-bearing maxillary bones, the nasal and antorbital bones, the circumorbital bones, and the opercular bones, all of which show evolutionary modifications in different cavefish populations. Manipulations of eye formation by transplantation of the embryonic lens, by lentectomy, or by removing the optic vesicle showed that eye-dependent and -independent processes change both the surface fish and cavefish craniofacial skeletons. The size of the olfactory pits, which the nasal and antorbital bones define, and the size and positioning of the circumorbital bones were found to correlate with eye development. For the six suborbital bones (SO1-6), the relationship with the developing eye appears to be due to ossification initiated from foci in the suborbital canal of cranial neuromasts, whose patterning is also highly correlated with the presence or absence of an eye. By contrast, we found that the number of maxillary teeth, the number of SO3 bone elements, the positioning of SO4-6 with respect to the opercular bone, and the shape of the opercular bone are not dependent on eye formation and vary among different cavefish populations. The results suggest that evolution of the cavefish craniofacial skeleton is controlled by multiple developmental events, some a direct consequence of eye degeneration and others unrelated to loss of the eye.

Skeletal elements in the vertebrate eye and adnexa: Morphological and developmental perspectives

“…It is currently unclear whether the RPE of teleosts induces scleral cartilage development. However, given that the scleral cartilage element is restricted to the equatorial region, that the lens influences scleral cartilage ossification (discussed below; Yamamoto et al, 2003) and that some aspects of eye development (i.e., the lens) differs between tetrapods and teleosts (Glass and Dahm, 2004;Cvekl and Tamm, 2004), it is possible that a different inductive mechanism exists in teleosts. What is needed is to determine whether the onset of scleral cartilage formation coincides with RPE differentiation and when the RPE obtains its ability to induce cartilage.…”

“…Although teleosts are used currently as model organisms to study eye development (e.g., Yamamoto and Jeffery, 2002;Vihtelic and Hyde, 2002;Glass and Dahm, 2004), very few have specifically investigated eye development together with the surrounding skeletal element by means of direct larval manipulation. The most recent work is by Jeffery, Yamamoto, and colleagues in Astyanax mexicanus, the Mexican tetra (Yamamoto et al, 2003). This species exists as two morphs-a sighted surface form and a blind cavefish form in which the lens undergoes apoptosis shortly after its development.…”

“…The sighted surface morph has two large scleral ossicles with minimal scleral cartilage joining their ends, whereas the blind cavefish form has the ring of scleral cartilage but no scleral ossicles. By transplanting the embryonic lens from the surface form to the blind cavefish form (and vice versa) and by extirpating the lens, these researchers noted that ossification of the scleral cartilage was affected as well as the size and positioning of the circumorbital bones (Yamamoto et al, 2003). In cavefish that had received a surface fish lens, the cartilaginous sclera ossified, suggesting that, although the cavefish eye appears to have lost the ability to promote scleral ossification, the scleral cartilage is still capable of responding to signals from the restored eye.…”

Contrasting feeding habits of post-larval and adult Astyanax cavefish

“…Direct measurements of the size of the olfactory pits have shown that eyeless cavefish have a wider olfactory pit than eyed surface fish. The width of the olfactory pit is on average 12.9% larger due to the eyedependent developmental processes (Yamamoto et al 2003;Hinaux et al 2016). An enlarged olfactory pit could result in an enhanced sense of smell, which could directly correlate with the feeding skills of eyeless fish (Bibliowicz et al 2013).…”

Kowalevsky, comparative evolutionary embryology, and the intellectual lineage of evo‐devo

“…The results are appearing from a number of contemporary laboratories, including (in hardly an exhaustive list) studies of ascidians (Jeffery et al,'99), amphioxus (Holland, 2002), hemichordates (Takacs et al, 2002;Lowe et al, 2003), a swarm of arthropods (Hughes and Kaufman, 2002), nematodes (Sommer, 2000), fish (Parichy and Johnson, 2001;Yamamoto et al, 2003), frogs (Callery et al, 2001), snakes (Cohn and Tickle, '99), starfish (Hart et al,'97), and sea urchins (Raff, '96;Wray, 2000). All of these systems offer particular advantages in addressing specific problems in the evolution of development, such as the role of Hox genes in the evolution of body form.…”