The smallest insects evolve anucleate neurons

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Abstract

The smallest insects are comparable in size to unicellular organisms. Thus, their size affects their structure not only at the organ level, but also at the cellular level. Here we report the first finding of animals with an almost entirely anucleate nervous system. Adults of the smallest flying insects of the parasitic wasp genus Megaphragma (Hymenoptera: Trichogrammatidae) have only 339–372 nuclei in the central nervous system, i.e., their ganglia, including the brain, consist almost exclusively of processes of neurons. In contrast, their pupae have ganglia more typical of other insects, with about 7400 nuclei in the central nervous system. During the final phases of pupal development, most neuronal cell bodies lyse. As adults, these insects have many fewer nucleated neurons, a small number of cell bodies in different stages of lysis, and about 7000 anucleate cells. Although most neurons lack nuclei, these insects exhibit many important behaviors, including flight and searching for hosts.

Highlights

► We report the novel discovery of anucleate neuron cells in a miniature wasp. ► A mostly anucleate CNS is capable of sustaining many functions exhibited by other insects with nucleated neurons. ► Smallest insects have only about 7400 cells in their central nervous system.

Introduction

Miniaturization is an evolutionary decrease in body size, an important trend in the evolution of animals (Hanken and Wake, 1993). Insects are one of the most successful at this evolutionary direction and a lot of them demonstrate extreme miniaturization. Size strongly determines the morphology, physiology, and biology of species (Schmidt-Nielsen, 1984). Structural trends associated with miniaturization have been described in many animals (Hanken and Wake, 1993). For vertebrates, e.g. Amphibia, they affect mainly particular aspects of anatomy of the skeleton (Hanken, 1983, Hanken, 1985, Yeh, 2002). For some invertebrates miniaturization affect whole organs and organ system (Hanken and Wake, 1993). For small insects, considerable modifications have been described affecting almost all the organs (Grebennikov and Beutel, 2002, Polilov, 2005, Polilov, 2008, Polilov and Beutel, 2010). In the smallest insects whose size is comparable to that of unicellular organisms (Fig. 1), miniaturization creates problems not only at the organ, but also at the cellular level (Rensch, 1948, Polilov and Beutel, 2009).

The nervous system of very small insects is of special interest because the neuronal control of behaviors depends in part on neuronal number (Kaas, 2000). In spite of their extremely small size, the smallest beetles of the family Ptiliidae (Coleoptera) have about 40,000 cells in their nervous systems (Polilov, 2008). These beetles have evolved a nervous system with considerably larger relative volume and considerably smaller cell size compared to those in larger members of related taxa. This decrease in cell size is accompanied by a considerable increase in the relative volume of the cytoplasm and an increase in the degree of chromatin compaction (Polilov, 2008). Similar evolutionary changes are observed in other very small insects.

The smallest flying insects belong to the genus Megaphragma (Hymenoptera: Trichogrammatidae). Their adult body length is only 170 μm in Megaphragma caribea and 200 μm in Megaphragma mymaripenne. The anatomy of these insects is of considerable interest for studies of the influence of size on tissue structure. Our initial anatomical study of M. mymaripenne revealed that their adult nervous system contained only a few hundred neuronal nuclei. This finding raised the question of whether the central nervous system of this species actually contains so few neurons, or something happens to their nuclei.

Section snippets

List of taxa examined

M. mymaripenne Timberlake, 1924 (Hymenoptera: Trichogrammatidae), adults and pupae, collected in Blanes, Spain (2008) and Funchal, Madeira, Portugal (2009) were studied. For comparative purposes, specimens of adults and pupae of Trichogramma evanescens Westwood, 1833 were studied. The Trichogramma was obtained from LTD Centre Biotechnique, Khlebodarskoe, Ukraine.

Histology

Adults and pupae were fixed in formaldehyde–ethanol–acetic acid (FAE). They were embedded in Araldite M, cut at 1 μm with a Leica

Results

A detailed study of the nervous system based on serial histological sections using 3D computer modeling and transmission electron microscopy shows that the central nervous system of adult M. mymaripenne displays considerable oligomerisation and concentration of ganglia, with the thoracic ganglia merged into a single synganglion positioned mostly in the metathorax, and the abdominal ganglia merged into a single synganglion. The brain of M. mymaripenne occupies a large part of the space within

Discussion

Estimates of the anatomy of the nervous system and the size of neurons, limited by the volume of chromatin and axon diameter, are conservative, making the volume of the nervous system one of the principal factors limiting the decrease of body size (Kaas, 2000, Polilov, 2008, Polilov and Beutel, 2010). This problem is especially acute for the brain, the largest structure in the CNS. The problem of an excessively large brain is solved in most small insects by a partial or complete shift of its

Acknowledgments

I thank R. Beutel, P. Petrov and E. Gurarie for useful comments and recommendations on the manuscript. This study was supported by the Russian Foundation for Basic Research (10-04-00457 and 11-04-00496), the President of Russia Foundation (MK-558.2010.4) and Alexander von Humboldt Foundation (1128047).

References (19)

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