Sensory-skeletal integration underlies diverse bone fusion patterns in a complex demography of cavefish

Abstract Over the course of development, sensory systems must integrate specialized cells and tissues to generate a functional unit. A robust example of this type of integration is the lateral line, a mechanosensory system in fishes and amphibians that senses changes in water movement. Over the past century, numerous reports noted that the principal organs of the lateral line—neuromasts—co-localize to the position of ossification centers for bones of the facial skeleton. More recent work in the freshwater model system, Astyanax mexicanus, revealed facial bones of the suborbital complex frequently fuse in a manner consistent with approximated neuromasts. In cave dwelling morphs, which lack a structural eye, positioning of the neuromasts encircling the orbit differ from closely related, eyed surface-dwelling morphs. This suggests facial bone fusion patterns are a function of eye regression, which interferes with neuromast positioning early in development. Here, we compared adult bone fusion patterns from individuals derived from three cavefish populations derived from at least two independent cave colonizations—the Pachón, Tinaja and Molino caves. Interestingly, despite established asymmetries impacting the cavefish craniofacial complex, no asymmetric bias was observed in facial bone fusion. Surface fish showed minimal fusion, however cave morphs showed substantial facial bone fusion which varied in severity by cave population. Facial bone fusion is therefore not a simple function of eye regression, since each eyeless cavefish population harbored different patterns of fusion severity. We propose intra-population variation in bone fusion is a function of the timing of eye degeneration. Early and rapid eye degeneration (as in Pachón cavefish) likely has a more profound effect on neuromast positioning, and consequential bone fusion patterns. Tinaja and Molino cavefish have slower and more gradual eye regression, likely interfering less with neuromast positioning. This results in fewer approximated neuromasts, and fusions between neighboring facial bones. This study showcases the integrated nature of sensory-skeletal development, a poorly understood phenomenon. Moreover, aberrations impacting this integration—such as eye loss in cave dwelling fish—can lead to remarkable intraspecific (and intra-population) variation.