Abstract
Descriptions of crustacean brains have focused mainly on three highly derived lineages of malacostracans: the reptantian infraorders represented by spiny lobsters, lobsters, and crayfish. Those descriptions advocate the view that dome- or cap-like neuropils, referred to as 'hemiellipsoid bodies,' are the ground pattern organization of centers that are comparable to insect mushroom bodies in processing olfactory information. Here we challenge the doctrine that hemiellipsoid bodies are a derived trait of crustaceans, whereas mushroom bodies are a derived trait of hexapods. We demonstrate that mushroom bodies typify lineages that arose before Reptantia and exist in Reptantia thereby indicating that the mushroom body, not the hemiellipsoid body, provides the ground pattern for both crustaceans and hexapods. We show that evolved variations of the mushroom body ground pattern are, in some lineages, defined by extreme diminution or loss and, in others, by the incorporation of mushroom body circuits into lobeless centers. Such transformations are ascribed to modifications of the columnar organization of mushroom body lobes that, as shown in Drosophila and other hexapods, contain networks essential for learning and memory.
Highlights
As demonstrated in Drosophila melanogaster, paired mushroom bodies in the insect brain play manifold roles in learning and memory (Aso et al, 2014a; Aso et al, 2014b; Cognigni et al, 2018)
Species considered here belong to malacostracan lineages whose divergence times are known from fossil-calibrated molecular data (Wolfe et al, 2019), and which are estimated to have originated between the mid-to-late Ordovician and the Carboniferous (Figure 1A)
Our results demonstrate substantial variation of the mushroom body ground pattern in pancrustaceans where it has undergone major transformations in Reptantia (Figure 16), a monophyletic group for which fossil-calibrated molecular phylogenies estimate a time of origin at 400–385 mya (Wolfe et al, 2019; Porter et al, 2005)
Summary
As demonstrated in Drosophila melanogaster, paired mushroom bodies in the insect brain play manifold roles in learning and memory (Aso et al, 2014a; Aso et al, 2014b; Cognigni et al, 2018). Ephemeroptera (mayflies) and Odonata (dragonflies, darters) are calyxless; inputs to their mushroom bodies supply their columnar lobes directly (Strausfeld et al, 2009) Such distinctions demonstrate a general property of all well-defined protocerebral brain centers: retention of ancestral ground patterns despite evolved modifications such as losses of some components and elaborations of others. We show here that crown eumalacostracan species belonging to lineages originating early in evolutionary history share the same expanded set of diagnostic characters that define insect mushroom bodies, including the partitioning of columns into discrete circuit-defined domains These can occur as segment-like partitions of the columnar lobes and as tuberous outswellings, as they do in basal insects belonging to Zygentoma and Pterygota (Farris, 2005a; Farris, 2005b; Strausfeld et al, 2009). In contrast to mushroom bodies in insects, evolved modifications of the mushroom body ground pattern in crustaceans have resulted in highly divergent morphologies including, both within Caridea and in certain lineages of Reptantia, centers lacking defined lobes
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