Early lens ablation causes dramatic long-term effects on the shape of bones in the craniofacial skeleton of Astyanax mexicanus.

Megan Dufton,Brian K Hall,Tamara A Franz-Odendaal,Henry H Roehl

doi:10.1371/journal.pone.0050308

Megan Dufton, Brian K Hall + Show 2 more

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https://doi.org/10.1371/journal.pone.0050308

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Journal: PloS one	Publication Date: Nov 30, 2012
Citations: 70	License type: CC BY 4.0

Affiliation: Dalhousie University, Mount Saint Vincent University

Abstract

The Mexican tetra, Astyanax mexicanus, exists as two morphs of a single species, a sighted surface morph and a blind cavefish. In addition to eye regression, cavefish have an increased number of taste buds, maxillary teeth and have an altered craniofacial skeleton compared to the sighted morph. We investigated the effect the lens has on the development of the surrounding skeleton, by ablating the lens at different time points during ontogeny. This unique long-term study sheds light on how early embryonic manipulations on the eye can affect the shape of the adult skull more than a year later, and the developmental window during which time these effects occur. The effects of lens ablation were analyzed by whole-mount bone staining, immunohistochemisty and landmark based morphometric analyzes. Our results indicate that lens ablation has the greatest impact on the skeleton when it is ablated at one day post fertilisation (dpf) compared to at four dpf. Morphometric analyzes indicate that there is a statistically significant difference in the shape of the supraorbital bone and suborbital bones four through six. These bones expand into the eye orbit exhibiting plasticity in their shape. Interestingly, the number of caudal teeth on the lower jaw is also affected by lens ablation. In contrast, the shape of the calvariae, the length of the mandible, and the number of mandibular taste buds are unaltered by lens removal. We demonstrate the plasticity of some craniofacial elements and the stability of others in the skull. Furthermore, this study highlights interactions present between sensory systems during early development and sheds light on the cavefish phenotype.

Highlights

The eye is an island of soft tissue surrounded by the neural crest derived tissues of the craniofacial skeleton
Lens ablation in the surface Mexican tetra results in eye regression in approximately 50% of juveniles, regardless of the age of the embryo when surgery is performed (n = 51)
The supraorbital bone and suborbital bones four through six are the most dramatically altered in size and shape following lens ablation (Table 1)

Summary

Introduction

The eye is an island of soft tissue surrounded by the neural crest derived tissues of the craniofacial skeleton. Studies investigating interactions between the soft eye tissues and the harder skull tissues have been rare until recently We explore this relationship and demonstrate that some bones are plastic, while others are resistant to manipulation. To do this we use a fish species which is extremely well suited for studying the influence of the eye on craniofacial development, namely the Mexican tetra. The approximately 29 different blind cavefish morphs are thought to have originated from the surface morph in the last few million years [5]. These cavefish populations are found in a small region of limestone caves located in north-eastern Mexico [6]. Less commonly studied are the constructive changes, which include changes in body position while feeding, increased jaw size, increased number of taste buds, increased size and number of neuromasts, larger fat stores and increased number of maxillary teeth [9,10]

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