Mushroom bodies in Reptantia reflect a major transition in crustacean brain evolution

Brain centers possessing a suite of neuroanatomical characters that define mushroom bodies of dicondylic insects have been identified in mantis shrimps, which are basal malacostracan crustaceans. Recent studies of the caridean shrimp Lebbeus groenlandicus further demonstrate the existence of mushroom bodies in Malacostraca. Nevertheless, received opinion promulgates the hypothesis that domed centers called hemiellipsoid bodies typifying reptantian crustaceans, such as lobsters and crayfish, represent the malacostracan cerebral ground pattern. Here, we provide evidence from the marine hermit crab Pagurus hirsutiusculus that refutes this view. P. hirsutiusculus, which is a member of the infraorder Anomura, reveals a chimeric morphology that incorporates features of a domed hemiellipsoid body and a columnar mushroom body. These attributes indicate that a mushroom body morphology is the ancestral ground pattern, from which the domed hemiellipsoid body derives and that the “standard” reptantian hemiellipsoid bodies that typify Astacidea and Achelata are extreme examples of divergence from this ground pattern. This interpretation is underpinned by comparing the lateral protocerebrum of Pagurus with that of the crayfish Procambarus clarkii and Orconectes immunis, members of the reptantian infraorder Astacidea

Introduction to ‘Homology and convergence in nervous system evolution’

The origin of brains and central nervous systems (CNSs) is thought to have occurred before the Palaeozoic era 540 Ma. Yet in the absence of tangible evidence, there has been continued debate whether today's brains and nervous systems derive from one ancestral origin or whether similarities among them are due to convergent evolution. With the advent of molecular developmental genetics and genomics, it has become clear that homology is a concept that applies not only to morphologies, but also to genes, developmental processes, as well as to behaviours. Comparative studies in phyla ranging from annelids and arthropods to mammals are providing evidence that corresponding developmental genetic mechanisms act not only in dorso–ventral and anterior–posterior axis specification but also in segmentation, neurogenesis, axogenesis and eye/photoreceptor cell formation that appear to be conserved throughout the animal kingdom. These data are supported by recent studies which identified Mid-Cambrian fossils with preserved soft body parts that present segmental arrangements in brains typical of modern arthropods, and similarly organized brain centres and circuits across phyla that may reflect genealogical correspondence and control similar behavioural manifestations. Moreover, congruence between genetic and geological fossil records support the notion that by the ‘Cambrian explosion’ arthropods and chordates shared similarities in brain and nervous system organization. However, these similarities are strikingly absent in several sister- and outgroups of arthropods and chordates which raises several questions, foremost among them: what kind of natural laws and mechanisms underlie the convergent evolution of such similarities? And, vice versa: what are the selection pressures and genetic mechanisms underlying the possible loss or reduction of brains and CNSs in multiple lineages during the course of evolution? These questions were addressed at a Royal Society meeting to discuss homology and convergence in nervous system evolution. By integrating knowledge ranging from evolutionary theory and palaeontology to comparative developmental genetics and phylogenomics, the meeting covered disparities in nervous system origins as well as correspondences of neural circuit organization and behaviours, all of which allow evidence-based debates for and against the proposition that the nervous systems and brains of animals might derive from a common ancestor

Mushroom bodies in crustaceans: Insect‐like organization in the caridid shrimp Lebbeus groenlandicus

Paired centers in the forebrain of insects, called the mushroom bodies, have become the most investigated brain region of any invertebrate due to novel genetic strategies that relate unique morphological attributes of these centers to their functional roles in learning and memory. Mushroom bodies possessing all the morphological attributes of those in dicondylic insects have been identified in mantis shrimps, basal hoplocarid crustaceans that are sister to Eumalacostraca, the most species-rich group of Crustacea. However, unless other examples of mushroom bodies can be identified in Eumalacostraca, the possibility is that mushroom body-like centers may have undergone convergent evolution in Hoplocarida and are unique to this crustacean lineage. Here, we provide evidence that speaks against convergent evolution, describing in detail the paired mushroom bodies in the lateral protocerebrum of a decapod crustacean, Lebbeus groenlandicus, a species belonging to the infraorder Caridea, an ancient lineage of Eumalacostraca