Developmental origin of a major difference in sensory patterning between zebrafish and bluefin tuna

Alain Ghysen,Christine Dambly‐Chaudière,Fernando De La Gandara,Aurelio Ortega,Denis Coves

doi:10.1111/j.1525-142x.2012.00529.x

Abstract

SUMMARYThe posterior lateral line system (PLL) of teleost fish comprises a number of mechanosensory organs arranged in defined patterns on the body surface. Embryonic patterns are largely conserved among teleosts, yet adult patterns are highly diverse. Although changes in pattern modify the perceptual abilities of the system, their developmental origin remains unknown. Here we compare the processes that underlie the formation of the juvenile PLL pattern in Thunnus thynnus, the bluefin tuna, to the processes that were elucidated in Danio rerio, the zebrafish. In both cases, the embryonic PLL comprises five neuromasts regularly spaced along the horizontal myoseptum, but the juvenile PLL comprises four roughly parallel anteroposterior lines in zebrafish, whereas it is a simple dorsally arched line in tuna fish. We examined whether this difference involves evolutionary novelties, and show that the same mechanisms mediate the transition from embryonic to juvenile patterns in both species. We conclude that the marked difference in juveniles depends on a single change (dorsal vs. ventral migration of neuromasts) in the first days of larval life.

Highlights

The patterning of sense organs has a major influence on their behavioral function, yet in no case have changes in sensory pattern been satisfactorily explained–-except for the drastic change corresponding to eye loss in the blind cavefish, Astyanax (Jeffery, 2008, 2009)
The embryonic posterior lateral line system (PLL) is fully differentiated at 2 dpf
Nearly identical patterns are found in late embryos of Danio rerio and Thunnus thynnus, two highly derived species that belong respectively to the Ostariophysi and Acanthopterygii superorders of teleosts. In both species the embryonic PLL comprises five neuromasts regularly spaced along the horizontal myoseptum, linked by a stripe of interneuromast cells (Fig. 1, Ghysen et al 2010)

Summary

Introduction

The patterning of sense organs has a major influence on their behavioral function, yet in no case have changes in sensory pattern been satisfactorily explained–-except for the drastic change corresponding to eye loss in the blind cavefish, Astyanax (Jeffery, 2008, 2009). Development of the PLL involves the long-distance migration of an embryonic primordium, prim, as originally discovered in amphibians (Stone, 1937), Harrison, 1904 and later confirmed in zebrafish (Metcalfe, 1985) and in tuna fish (Ghysen et al 2010). During this migration, prim deposits five clusters of cells (proneuromasts L1–L5) along the horizontal myoseptum, and a continuous stripe of interneuromast cells (Grant et al 2005, Lopez-Schier and Hudspeth, 2005). The molecular bases of this development have been extensively studied in zebrafish over the past 10 years (reviewed in Ghysen and Dambly-Chaudiere, 2007, Friedl and Gilmour, 2009, Ma and Raible, 2009, Aman and Piotrowski, 2010)

Methods

Results

Discussion

Conclusion