Myogenesis of Malacostraca - the egg-nauplius concept revisited

Background: Malacostracan evolutionary history has seen multiple transformations of ontogenetic mode. For example direct development in connection with extensive brood care and development involving planktotrophic nauplius larvae, as well as intermediate forms are found throughout this taxon. This makes the Malacostraca a promising group for study of evolutionary morphological diversification and the role of heterochrony therein. One candidate heterochronic phenomenon is represented by the concept of the 'egg-nauplius', in which the nauplius larva, considered plesiomorphic to all Crustacea, is recapitulated as an embryonic stage. Results: Here we present a comparative investigation of embryonic muscle differentiation in four representatives of Malacostraca: Gonodactylaceus falcatus (Stomatopoda), Neocaridina heteropoda (Decapoda), Neomysis integer (Mysida) and Parhyale hawaiensis (Amphipoda). We describe the patterns of muscle precursors in different embryonic stages to reconstruct the sequence of muscle development, until hatching of the larva or juvenile. Comparison of the developmental sequences between species reveals extensive heterochronic and heteromorphic variation. Clear anticipation of muscle differentiation in the nauplius segments, but also early formation of longitudinal trunk musculature independently of the teloblastic proliferation zone, are found to be characteristic to stomatopods and decapods, all of which share an egg-nauplius stage. Conclusions: Our study provides a strong indication that the concept of nauplius recapitulation in Malacostraca is incomplete, because sequences of muscle tissue differentiation deviate from the chronological patterns observed in the ectoderm, on which the egg nauplius is based. However, comparison of myogenic sequences between taxa supports the hypothesis of a zoea-like larva that was present in the last common ancestor of Eumalacostraca (Malacostraca without Leptostraca). We argue that much of the developmental sequences of larva muscle patterning were retained in the eumalacostracan lineage despite the reduction of free swimming nauplius larvae, but was severely reduced in the peracaridean clade.