Evolution of posterior lateral line development in fish and amphibians

Abstract

The lateral line is a sensory system present in fish and amphibians. It is composed of discrete sense organs, the neuromasts, arranged on the head and body in species-specific patterns. The neuromasts are deposited by migrating primordia that originate from pre- and postotic placodes and follow defined pathways on the head and body. Here we examine the formation of the posterior lateral line (PLL), which extends rostrocaudally on the trunk and tail. In amphibians, the PLL neuromasts are deposited as a single wave from the head to the tip of the tail. In the zebrafish, however, the first wave of neuromast deposition forms but a rudimentary PLL, and several additional waves are needed to form the adult pattern. We show that the amphibian mode is also present in the sturgeon and therefore probably represents the primitive mode, whereas the zebrafish mode is highly conserved in several teleost species. A third mode is found in a subgroup of teleosts, the protacanthopterygians, and may represent a synapomorphy of this group. Altogether, the mode of formation of the embryonic PLL appears to have undergone remarkably few changes during the long history of anamniote evolution, even though large differences can be observed in the lateral line morphology of adult fishes.

Supernumerary neuromasts in the posterior lateral line of zebrafish lacking peripheral glia

“…The number of neuromasts is highly regulated in wild-type zebrafish larvae (18,24). However, in ngn1 and cls mutants, more than twice the normal complement of neuromasts forms in the posterior lateral line.…”

The lateral line microcosmos

“…This pattern appears extremely conserved among teleosts (Pichon and Ghysen 2004). It is observed not only in the relatively basal ostariophysians (e.g., zebrafish and the blind tetra, Astyanax fasciatus) but also in groups that show many derived characters such as pleuronectids (flatfishes; Pichon and Ghysen 2004) and scombrids (tunafish; Kawamura et al 2003). Fish continue to grow throughout their life, however, and their lateral-line system continues to develop.…”

Estrogen receptor ESR1 controls cell migration by repressing chemokine receptor CXCR4 in the zebrafish posterior lateral line system

“…The control of primordium organization and migration by two self-maintained, connected systems, Wnt/FGF on one hand and CXCR4/CXCR7 on the other hand, would ensure a remarkable stability of the migration process and may explain the extreme conservation of embryonic PLL patterns across all teleosts, from the relatively basal zebrafish to highly derived flatfish embryos (22). This duality may also explain why, whereas the inactivation of SDF1, CXCR4, or CXCR7 prevents migration altogether, interfering with the other components of this control system (Wnt, FGF, ESR1) only leads to reduced migration, which eventually comes to a halt after several hours (11)(12)(13).…”