Increased complexity of mushroom body Kenyon cell subtypes in the brain is associated with behavioral evolution in hymenopteran insects

Satoyo Oya,Hiroki Kohno,Takeo Kubo,Yooichi Kainoh,Masato Ono

doi:10.1038/s41598-017-14174-6

Satoyo Oya, Hiroki Kohno + Show 3 more

Open Access

https://doi.org/10.1038/s41598-017-14174-6

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Abstract

In insect brains, the mushroom bodies (MBs) are a higher-order center for sensory integration and memory. Honeybee (Apis mellifera L.) MBs comprise four Kenyon cell (KC) subtypes: class I large-, middle-, and small-type, and class II KCs, which are distinguished by the size and location of somata, and gene expression profiles. Although these subtypes have only been reported in the honeybee, the time of their acquisition during evolution remains unknown. Here we performed in situ hybridization of tachykinin-related peptide, which is differentially expressed among KC subtypes in the honeybee MBs, in four hymenopteran species to analyze whether the complexity of KC subtypes is associated with their behavioral traits. Three class I KC subtypes were detected in the MBs of the eusocial hornet Vespa mandarinia and the nidificating scoliid wasp Campsomeris prismatica, like in A. mellifera, whereas only two class I KC subtypes were detected in the parasitic wasp Ascogaster reticulata. In contrast, we were unable to detect class I KC subtype in the primitive and phytophagous sawfly Arge similis. Our findings suggest that the number of class I KC subtypes increased at least twice – first with the evolution of the parasitic lifestyle and then with the evolution of nidification.

Highlights

Hymenoptera comprise many species that exhibit various behavioral traits[1]
Class I small-type Kenyon cell (KC) have small somata (5–7 μm) that occupy the innercore of the calyces, while class I large-type KCs have large somata (7–9 μm) that are located at the inner peripheral region of the calyces, and class I middle-type KCs have middle-sized somata that are located between the lKC and sKC somata[28]
Our results demonstrated that KC subtypes became more diverse with the evolution of Hymenoptera: while a member of the basalmost Hymenoptera, A. similis, has only one class I subtype; parasitic wasp A. reticulata has two; and Aculeata wasps, V. mandarinia, C. prismatica, and A. mellifera have three (Fig. 6)

Summary

Introduction

Hymenoptera comprise many species that exhibit various behavioral traits[1]. Members of the most basal lineages are solitary and phytophagous[2]. Adult female parasitic wasps lay their eggs in the host, and their larvae grow inside the host by feeding on the host body[2,3] From one of their lineages arose Aculeata[2,4,5], the clade to which all of the eusocial Hymenoptera, such as hornets, ants, and honeybees, belong[6]. Class I sKCs express hormone receptor-like 38 (HR38), whose expression varies with the division of labor of the workers, implying their involvement in the regulation of worker behaviors[36] Both class I sKCs and some mKCs are active in the brains of workers engaged in foraging, suggesting their roles in visual information-processing during foraging flights[37,38]. As the honeybee is the only organism known to have such KC subtypes, these subtypes are assumed to contribute to the regulation of the highly advanced behaviors of the honeybee

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