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

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.

Anticipatory flexibility: larval population density in moths determines male investment in antennae, wings and testes.

Developmental plasticity provides individuals with a distinct advantage when the reproductive environment changes dramatically. Variation in population density, in particular, can have profound effects on male reproductive success. Females may be easier to locate in dense populations, but there may be a greater risk of sperm competition. Thus, males should invest in traits that enhance fertilization success over traits that enhance mate location. Conversely, males in less dense populations should invest more in structures that will facilitate mate location. In Lepidoptera, this may result in the development of larger antennae to increase the likelihood of detecting female sex pheromones, and larger wings to fly more efficiently. We explored the effects of larval density on adult morphology in the gum-leaf skeletonizer moth, Uraba lugens, by manipulating both the number of larvae and the size of the rearing container. This experimental arrangement allowed us to reveal the cues used by larvae to assess whether absolute number or density influences adult responses. Male investment in testes size depended on the number of individuals, while male investment in wings and antennae depended upon larval density. By contrast, the size of female antennae and wings were influenced by an interaction of larval number and container size. This study demonstrates that male larvae are sensitive to cues that may reveal adult population density, and adjust investment in traits associated with fertilization success and mate detection accordingly.

Sexual selection on receptor organ traits: younger females attract males with longer antennae.

Sexual selection theory predicts that female choice may favour the evolution of elaborate male signals. Darwin also suggested that sexual selection can favour elaborate receiver structures in order to better detect sexual signals, an idea that has been largely ignored. We evaluated this unorthodox perspective by documenting the antennal lengths of male Uraba lugens Walker (Lepidoptera: Nolidae) moths that were attracted to experimentally manipulated emissions of female sex pheromone. Either one or two females were placed in field traps for the duration of their adult lives in order to create differences in the quantity of pheromone emissions from the traps. The mean antennal length of males attracted to field traps baited with a single female was longer than that of males attracted to traps baited with two females, a pattern consistent with Darwin's prediction assuming the latter emits higher pheromone concentrations. Furthermore, younger females attracted males with longer antennae, which may reflect age-specific changes in pheromone emission. These field experiments provide the first direct evidence of an unappreciated role for sexual selection in the evolution of sexual dimorphism in moth antennae and raise the intriguing possibility that females select males with longer antennae through strategic emission of pheromones.

Investment in sensory structures, testis size, and wing coloration in males of a diurnal moth species: trade-offs or correlated growth?

For dioecious animals, reproductive success typically involves an exchange between the sexes of signals that provide information about mate location and quality. Typically, the elaborate, secondary sexual ornaments of males signal their quality, while females may signal their location and receptivity. In theory, the receptor structures that receive the latter signals may also become elaborate or enlarged in a way that ultimately functions to enhance mating success through improved mate location. The large, elaborate antennae of many male moths are one such sensory structure, and eye size may also be important in diurnal moths. Investment in these traits may be costly, resulting in trade-offs among different traits associated with mate location. For polyandrous species, such trade-offs may also include traits associated with paternity success, such as larger testes. Conversely, we would not expect this to be the case for monandrous species, where sperm competition is unlikely. We investigated these ideas by evaluating the relationship between investment in sensory structures (antennae, eye), testis, and a putative warning signal (orange hindwing patch) in field-caught males of the monandrous diurnal painted apple moth Teia anartoides (Lepidoptera: Lymantriidae) in southeastern Australia. As predicted for a monandrous species, we found no evidence that male moths with larger sensory structures had reduced investment in testis size. However, contrary to expectation, investment in sensory structures was correlated: males with relatively larger antennae also had relatively larger eyes. Intriguingly, also, the size of male orange hindwing patches was positively correlated with testis size.

Pheromone production, male abundance, body size, and the evolution of elaborate antennae in moths.

The males of some species of moths possess elaborate feathery antennae. It is widely assumed that these striking morphological features have evolved through selection for males with greater sensitivity to the female sex pheromone, which is typically released in minute quantities. Accordingly, females of species in which males have elaborate (i.e., pectinate, bipectinate, or quadripectinate) antennae should produce the smallest quantities of pheromone. Alternatively, antennal morphology may be associated with the chemical properties of the pheromone components, with elaborate antennae being associated with pheromones that diffuse more quickly (i.e., have lower molecular weights). Finally, antennal morphology may reflect population structure, with low population abundance selecting for higher sensitivity and hence more elaborate antennae. We conducted a phylogenetic comparative analysis to test these explanations using pheromone chemical data and trapping data for 152 moth species. Elaborate antennae are associated with larger body size (longer forewing length), which suggests a biological cost that smaller moth species cannot bear. Body size is also positively correlated with pheromone titre and negatively correlated with population abundance (estimated by male abundance). Removing the effects of body size revealed no association between the shape of antennae and either pheromone titre, male abundance, or mean molecular weight of the pheromone components. However, among species with elaborate antennae, longer antennae were typically associated with lower male abundances and pheromone compounds with lower molecular weight, suggesting that male distribution and a more rapidly diffusing female sex pheromone may influence the size but not the general shape of male antennae.

Spire, an actin nucleation factor, regulates cell division during Drosophila heart development.

The Drosophila dorsal vessel is a beneficial model system for studying the regulation of early heart development. Spire (Spir), an actin-nucleation factor, regulates actin dynamics in many developmental processes, such as cell shape determination, intracellular transport, and locomotion. Through protein expression pattern analysis, we demonstrate that the absence of spir function affects cell division in Myocyte enhancer factor 2-, Tinman (Tin)-, Even-skipped- and Seven up (Svp)-positive heart cells. In addition, genetic interaction analysis shows that spir functionally interacts with Dorsocross, tin, and pannier to properly specify the cardiac fate. Furthermore, through visualization of double heterozygous embryos, we determines that spir cooperates with CycA for heart cell specification and division. Finally, when comparing the spir mutant phenotype with that of a CycA mutant, the results suggest that most Svp-positive progenitors in spir mutant embryos cannot undergo full cell division at cell cycle 15, and that Tin-positive progenitors are arrested at cell cycle 16 as double-nucleated cells. We conclude that Spir plays a crucial role in controlling dorsal vessel formation and has a function in cell division during heart tube morphogenesis.