An unusual case of a mutant lobster embryo with double brain and double ventral nerve cord

Abstract

We report the rare finding of a Siamese twin embryo of the American lobster Homarus americanus. Immunohistochemical labeling of this mutant with an antibody directed against Drosophila synaptic proteins revealed that the embryo had a structurally normal visual system with two compound eyes and eyestalk Anlagen but twin brains and twin ventral nerve cords. We have analyzed the patterns of connectivity of the components of the nervous system and have concluded that the wiring pattern in this nervous system provides a logical and elegant way of connecting the parts of the twin system in this unusual mutation.

Introduction

The ontogeny of the arthropod nervous system is initiated by the proliferation of neuronal stem cells (Doe and Skeath, 1996; Campos-Ortega and Hartenstein, 1997; Reichert and Boyan, 1997), their mitotic activity being under strict genetic control as are most other developmental processes (Campos-Ortega, 1995; Hartmann and Reichert, 1998; Tautz and Schmid, 1998). The components of the nervous system are then wired in an ordered species-specific manner that is influenced by cell to cell interactions (Chiba and Keshishian, 1996; Whitington, 1996; Stoeckli and Landmesser, 1998). However, research on arthropod neurogenesis relies heavily on the study of insect model organisms while in crustaceans we are only just beginning to understand possible similarities or variations in the processes which govern nervous system formation (Whitington, 1996).

In the course of recent studies on embryonic neurogenesis in the ventral nerve cord (Harzsch et al., 1998), brain (Harzsch et al., 1999a), and visual system (Harzsch et al., 1999b) of the American lobster Homarus americanus, we screened a large number of embryos from several lobster females and in one case encountered a female with an unusually high number (more than 1 in 20) of malformed embryos (such as embryos with normal optic Anlagen and brain, but without a trunk, or with a malformed trunk, or eggs with no embryo at all). One of these mutant eggs housed a Siamese twin embryo and therefore, we decided to label this specimen with an antibody directed against Drosophila synaptic proteins (Klagges et al., 1996; Harzsch et al., 1997) in order to reveal the structure of the nervous system. The mutant embryo appeared to have a normally developed visual system, which consisted of two compound eyes and two sets of eyestalk ganglia but was equipped with a twin brain, two ventral nerve cords, and duplicated limb Anlagen. The present report describes the structure of this double nervous system and discusses the way in which the components of this twin system resolve the challenge of neuronal wiring. In Drosophila melanogaster, the genetic network which regulates neurogenesis has been studied in depth and several genetic mutations are known which cause an abnormal growth of components of the nervous system (Hartenstein et al., 1992; Hinz, 1997), e.g. mastermind (Brand and Campos-Ortega, 1988) or big brain (Rao et al., 1992). Furthermore, mutation of the twin gene causes a duplication of the wing imaginal discs (Uemura et al., 1993). However, to our knowledge a mutation responsible for the formation of a double nervous system in any arthropod has so far not been described.