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

Abstract

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.

Mushroom Body Homology and Divergence across Pancrustacea

“…Apart from a fundamental misunderstanding of the nomenclature, that viewpoint is incorrect and is in conflict with the demonstration here, and in two recent studies (Wolff et al, 2017;Sayre and Strausfeld, 2019), that mushroom bodies hallmark eumalacostracan lineages that diverged earlier than Reptantia. As will be discussed later, comparisons across Eumalacostraca described here indicate that contrary to received opinion mushroom bodies are ubiquitous across Crustacea.…”

The reniform body: An integrative lateral protocerebral neuropil complex of Eumalacostraca identified in Stomatopoda and Brachyura

“…oerstedii anti‐TH‐immunoreactive zones characterizing the mushroom body's columnar lobes (Wolff et al, ) indicate dendritic territories of mushroom body output neurons, as they do in Drosophila and the cockroach (Cohn, Morantte, & Ruta, ; Hamanaka, Minoura, Nishino, Miura, & Mizunami, ). A second distinguishing feature is that the reniform body's pedestal comprises smooth axons that show none of the synaptic specializations that typify the extended processes of intrinsic neurons comprising the length of a mushroom body's columnar lobe, as observed in Stomatopoda, Caridea, Paguroidea, and insects (Sayre & Strausfeld, ; Strausfeld, Sinakevitch, Brown, & Farris, ; Wolff et al, ). Third, the prominent arrangement of caudally placed adjoining zones that extend from the pedestal share none of the morphological attributes of columnar lobes typifying mushroom bodies.…”

“…groenlandicus , and the marine hermit crab P . hirsutiusculus (Sayre & Strausfeld, ; Strausfeld & Sayre, ), showing that across Eumalacostraca some, if not all, decapod lineages possess two higher centers (the reniform body and the mushroom body) likely to be involved in learning and memory. The implications of this and the functional relevance of the reniform body have yet to be discovered, but could possibly be revealed by studying the behavioral differences as well as the ecological constraints of these species.…”

“…The methods described here are those used in two recent studies on the eumalacostracan brain (Sayre & Strausfeld, ; Wolff et al, ). About four to eight examples of each species were used for each of the applications using the described antibody combinations.…”

“…The caridean Lebbeus groenlandicus , which is equipped with an insect‐like mushroom body (Sayre & Strausfeld, ), possesses paired centers, the Bodian‐stained neuropils of which morphologically correspond to the stomatopod reniform bodies, as do similar centers in some reptantian decapods equipped with lobed mushroom bodies, such as the marine hermit crab Pagurus hirsutiusculus (Strausfeld & Sayre, ). As recognized by Hanström (), many other reptantians have highly modified centers that lack columnar lobes, which he nevertheless recognized as mushroom bodies but referred to as “hemiellipsoid bodies.” Those species also show evidence of reniform bodies (Strausfeld & Sayre, ).…”