Re-make, re-model: evolution and development of vertebrate cranial lateral lines.

Abstract

Lateral lines are placodally derived mechanosensory systems on the heads and trunks of many aquatic vertebrates. There is evidence of lateral lines in the earliest known vertebrate fossils, and they exist in organisms with widely different craniofacial morphologies - including the presence or absence of jaws, external or internal nostrils, and variable positions of the cranial cartilages with respect to eyes and braincase. Consequently, the lateral lines make an ideal study system to understand how morphological variation in a deeply conserved sensory system responds to overall evolution of the head. However, palaeontological and developmental data have not been integrated to elucidate the history of this system in the context of evolving vertebrate crania. The emergence of new imaging techniques and molecular methods to study ontogeny in non-model systems provides unique opportunities for such a study. This review examines open questions in light of new fossil discoveries that have altered our understanding of vertebrate evolution as well as new insights on the development of non-model taxa. We find that the diversity of lateral lines is not the result of simplification from a complex ancestral condition as previously supposed. Rather, the anterior lateral line systems of living gnathostomes result from an evolutionary episode of reduction and reassembly, both preceding and overlapping the origin of jawed vertebrates. This event is coupled to a marked postorbital to orbital-preorbital shift in the territorial elaboration of the lateral line systems, and we argue that this spatial move likely signals functional change, coinciding with a major enhancement of the gnathostome vestibular system.