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.

Keywords: brain evolution; compound eyes; hyperiid amphipods; neuroanatomy; optic lobes.

Figure 1.

Four hyperiid amphipod eye morphologies. (a) Cystisoma magna, huge dorsally directed compound eyes with a diffuse retinal sheet. Ventral view of the brain and the retinal sheet (left) and whole animal (right). (b) Lanceola sayana, tiny compound eyes (white arrowhead). (c) Hyperia galba, one pair, large, dome-like compound eyes with dorsally and laterally directed regions. (d) Phronima sedentaria, two pairs compound eyes (dashed line indicates dorsal eye, dotted indicates the lateral eye). Body lengths approximately: 8 cm C. magna (a), 1 cm L. sayana (b), 0.8 cm H. galba (c) and 1.5 cm P. sedentaria (d). (Online version in colour.)

Figure 2.

The brain and optic lobe organization of the near shore, non-hyperiid amphipod, Gammarus mucronatus. (a–c) The animal, its brain and eyes, and three-dimensional reconstruction of the brain with highlighted optic and olfactory lobes. (d–f) Osmium-ethyl gallate-stained optic lobe sections in different planes showing the characteristic optic lobe first and second chiasmata (white and black arrowheads, respectively), uncrossed neural connections between medulla and lobula plate (white arrow in f), and all four optic neuropils. (Online version in colour.)

Figure 3.

Hyperiid optic lobe arrangements and brain morphologies. Cystisoma magna, enlarged optic lobe with all four optic neuropils as seen in other malacostracans. Lanceola sayana, reduced optic lobe with lamina and medulla only and enlarged olfactory lobes. Hyperia galba, enlarged optic lobe comprise lamina, medulla and dorsal and ventral lobula plates. Phronima sedentaria, enlarged optic lobe comprise dorsal and ventral laminas, a fused medulla and dorsal lobula plate receiving inputs solely from the dorsal half of the medulla. Scale bars, 100 µm (black) and 200 µm (white). (Online version in colour.)

Figure 4.

Osmium-ethyl gallate-stained optic lobe sections of various crustaceans at the antero-posterior plane showing the characteristic optic lobe first and second chiasmata (white and black arrowheads, respectively) and optic neuropils, including the structurally simplified medulla found in hyperiids. (a) Alima pacifica (mantis shrimp), (b) Procambarus clarkii (crayfish), (c) Hyperia galba (hyperiid) and (d) Phronima sedentaria (hyperiid). Black arrows indicate the uncrossed neuronal connections between medulla and lobula plate. Scale bars, 50 µm. (Online version in colour.)

Figure 5.

FMRFamide-like (yellow, top row) and allatostatin-like (blue, middle row) immunoreactivity reveals distinct layers of neuronal organization in (a) a stomatopod (mantis shrimp, Neogonodactylus oerstedii) lamina (LA), medulla (ME) and lobula (LO) and in (b) a decapod (crayfish Procambarus clarkii). However, in (c) Hyperia galba and (d) Phronima sedentaria FMRFamide-like immunoreactivity is scattered throughout the entire medulla and lobula plate (LOP). No allatostatin-like immunoreactivity is detected in the hyperiid optic lobes. Scale bars, 100 µm. (Online version in colour.)

Figure 6.

Optic lobe organization in malacostracan crustaceans with compound eyes. Hyperiid amphipods exhibit dramatic variation in the number of optic neuropils unlike all other known malacostracans, including all previously known amphipods [–12]. Phylogeny modified from [27,38]. (Online version in colour.)