Insect Antennal Morphology: The Evolution of Diverse Solutions to Odorant Perception

Abstract

Chemical communication involves the production, transmission, and perception of odors. Most adult insects rely on chemical signals and cues to locate food resources, oviposition sites or reproductive partners and, consequently, numerous odors provide a vital source of information. Insects detect these odors with receptors mostly located on the antennae, and the diverse shapes and sizes of these antennae (and sensilla) are both astonishing and puzzling: what selective pressures are responsible for these different solutions to the same problem - to perceive signals and cues? This review describes the selection pressures derived from chemical communication that are responsible for shaping the diversity of insect antennal morphology. In particular, we highlight new technologies and techniques that offer exciting opportunities for addressing this surprisingly neglected and yet crucial component of chemical communication.

Keywords: antennae; chemical communication; insects; receiver morphology; signal perception.

Figure 1

The diversity of insect antennae (by rows, top to bottom, left to right): scarab beetle, Phyllotocus macleaya antenna (Scarabidae, Coleoptera; image: Christopher Freelance); mosquito Anopheles (Culicidae, Diptera; image: Qike Wang); stick insect, Extatosoma tiaratum (Phasmatidae, Phasmatodea; image: Christopher Freelance); Australian longicorn beetle (Cerambycidae, Coleoptera; image: Mark Elgar); moth, Uraba lugens (Nolidae, Lepidoptera; image: Christopher Freelance); ant worker, Oecophilla (Formicidea, Hymenoptera; image Zheng-yan Zhou); butterfly, Jalmenus evagoras (Lycaenidae, Lepidoptera; image: Mark Elgar); bloomed furrow bee, Lasioglossum albipes antenna (Halictidae, Hymenoptera; image: Bernadette Wittwer); shield bug Anaxandra (Acanthosomatidae, Hemiptera; image Zheng-yan Zhou); grasshopper (Orthoptera; image Zheng-yan Zhou); tachinid fly (Tachinidae, Diptera; image Zheng-yan Zhou); paper wasp, Polistes (Vespidae, Hymenoptera; image: Zheng-yan Zhou).

Figure 2

Schematic of the process of chemical communication, from odor production through to odorant perception, highlighting the role of antennae in bringing the odorant to the vicinity of the receptors. (Moth illustration by Sander van der Molen).

Figure 3

Antennae of male and female insects with well-developed olfactory sense: (a) honey bee (Apis mellifera L.); (b) flesh fly (genus Sarcophaga); (c) cariion beetle (genus Necrophorus); (d) scarabid beetle (genus Rhopaea); (e) saturniid moth (genus Antheraea); (f) hawk-moth (sphingidae, genus Pergesa) (g) butterfly (genus Vanessa). Common scale (1 mm) for a-d and e-g. Reproduced from [10].

Figure 4

The number of sensilla qualitatively increases with flagella length across males and females of various insects. Data from [8].

Figure 5

Beetles with different antennal morphology and their representative pheromones. Beetles with relatively larger and more elaborate antennae (bottom three species) use pheromones with lower volatility, while species with relatively more simple, smaller antennae (top three species) use more volatile pheromones. (Data from [35]). (Image credits: A. glabripennis, Dutch Government; C. sordidus, Joachim Rheinheimer; I. typographus, Udo Scmidt; R. ferrugineus, Didier Descouens; O. agamemnon, source unknown, http://www.enature.qa/specie/rhinoceros-beetle/; M. melolontha, Josef Dvorak).

Figure 6

Predicted concentration (red is high) around the surface of the antennae of nano-particles (pheromone molecules) in the (a) parallel and (b) ringed arrangement of antennal scales, and of micro-particles in the (c) parallel and (d) ringed arrangement of antennal scales. Sensilla number increases with the angle of the scales across genera (indicated by different colors) of heliozelid moths (Reproduced from [42]).