Strange eyes, stranger brains: exceptional diversity of optic lobe organization in midwater crustaceans

Abstract

Nervous systems across Animalia not only share a common blueprint at the biophysical and molecular level, but even between diverse groups of animals the structure and neuronal organization of several brain regions are strikingly conserved. Despite variation in the morphology and complexity of eyes across malacostracan crustaceans, many studies have shown that the organization of malacostracan optic lobes is highly conserved. Here, we report results of divergent evolution to this ‘neural ground pattern’ discovered in hyperiid amphipods, a relatively small group of holopelagic malacostracan crustaceans that possess an unusually wide diversity of compound eyes. We show that the structure and organization of hyperiid optic lobes has not only diverged from the malacostracan ground pattern, but is also highly variable between closely related genera. Our findings demonstrate a variety of trade-offs between sensory systems of hyperiids and even within the visual system alone, thus providing evidence that selection has modified individual components of the central nervous system to generate distinct combinations of visual centres in the hyperiid optic lobes. Our results provide new insights into the patterns of brain evolution among animals that live under extreme conditions.

Neural organization of the third optic neuropil, the lobula, in the highly visual semiterrestrial crab Neohelice granulata

“…It also became evident that the third neuropil of eumalacostracan crustaceans was usually accompanied by a small lobula satellite that, in allusion to the dipteran structure, was termed lobula plate (Strausfeld, 1998, 2005; Sinakevitch et al., 2003). Since then, the lobula satellite has been described with the name lobula plate in a variety of crustaceans including isopods (Kenning & Harzsch, 2013; Sinakevitch et al., 2003), amphipods (Lin et al., 2021), stomatopods (Thoen et al., 2017), anomuran crabs (Harzsch & Hansson, 2008), stenopodidea shrimps (Krieger et al., 2020), dendrobranchiata shrimps (Meth et al., 2017), and brachyuran crabs (Bengochea et al., 2018; Sinakevitch et al., 2003; Sztarker et al., 2005). Recently, Strausfeld and collaborators have argued that the lobula of crustaceans and insects evolved as a result of convergent evolution and that the lobula plate does not exist in crustaceans (Strausfeld & Olea‐Rowe, 2021; Strausfeld, 2021, but see Bengochea et al., 2018).…”

“…It is important to emphasize that the use of this terminology does not imply a homology statement. In most crustaceans (except in the isopod Ligia ; Strausfeld, 1998), the lobula accounts for a high percentage of the lobula complex mass (e.g., Bengochea et al., 2018; Harzsch & Hansson, 2008; Krieger et al., 2020; Lin et al., 2021; Meth et al., 2017; Sinakevitch et al., 2003; Sztarker et al., 2005; Thoen et al., 2017).…”

Multiple axes of visual system diversity in Ithomiini, an ecologically diverse tribe of mimetic butterflies

“…Allatostatin is a neuropeptide expressed in distinct cell types within the optic lobes of insects and crustaceans (Kreissl et al . 2010; Lin et al . 2021; Sivasubramanian & Sood, 2003) and provides additional anatomical detail of these brain regions.…”

Multiple axes of visual system diversity in Ithomiini, an ecologically diverse tribe of mimetic butterflies

“…Samples were then stained with anti-allatostatin (Antibody 5F10; Developmental Studies Hybridoma Bank, University of Iowa, Iowa City, IA, USA, RRID: AB_528076) at a 1:100 dilution in fresh NGS-PBS-TX and incubated for 24 h at room temperature under agitation. Allatostatin is a neuropeptide expressed in distinct cell types within the optic lobes of insects and crustaceans ( Kreissl et al, 2010 ; Lin et al, 2021 ; Sivasubramanian and Sood, 2003 ) and provides additional anatomical detail of these brain regions. Slices then underwent 6×30 min PBS-TX washes before introducing the secondary Cy2-conjugated anti-mouse antibody (Jackson ImmunoResearch cat.…”