Evolution of Sensory Development – Lessons from the Lateral Line

Abstract

evolved at least twice independently in various teleosts [Bullock et al., 1983]. Recently published insights into lateral line development [Modrell et al., 2011] now provide important new clues for reconstructing the developmental changes underlying some of these evolutionary modifications. Embryonically, the receptor organs of the lateral line are thought to originate from a group of lateral line placodes, which also give rise to the sensory neurons innervating the receptors. Grafting and ablation experiments in the axolotl (Ambystoma mexicanum) demonstrated that lateral line placodes give rise to both neuromasts and ampullary organs [Northcutt et al., 1995]. However, it has so far remained unresolved whether embryonic development in other vertebrates follows a similar pattern. A new study now describes development of the lateral line system in the paddlefish Polyodon spathula [Modrell et al., 2011]. This chondrostean fish, closely related to sturgeons, has the largest number of ampullary organs among all living vertebrates, covering extensive regions of the head. Combined evidence from histological sections, scanning electron microscopy, Eya and Six family gene expression patterns, and DiI labelling of lateral line placodes strongly suggests that in Polyodon, as With our five senses, we humans and fellow amniotes live in a relatively impoverished sensory world. Most other vertebrates possess two additional senses mediated by their lateral line system. This lateral line consists of multiple receptor organs distributed in lines along the body surface, each comprising a cluster of secondary sensory cells (hair cells) and their supporting cells [Northcutt, 1997; Schlosser, 2002a; Ghysen and Dambly-Chaudiere, 2007]. Mechanoreceptive sensory organs (neuromasts) detect water movements along the body surface, while electroreceptive sensory organs (ampullary organs) allow the perception of electric fields. A lateral line system with both types of receptor organs is found in most vertebrate taxa and, thus, appears to be a primitive character of vertebrates. However, several vertebrate groups such as amniotes and some direct developing amphibians have secondarily lost the entire lateral line system. Other groups retain the lateral line system but have lost some of its components [Northcutt, 1997; Schlosser, 2002b]. Mechanoreceptive lateral line organs were, for example, lost in some caecilians (limbless amphibians), whereas electroreceptive lateral line organs were lost in anurans and in the neopterygian fishes (teleosts, gars and bowfin). Electroreceptors then rePublished online: February 8, 2012