Male moths compete to arrive first at a female releasing pheromone. A new study reveals that additional pheromone cues released only by younger females may prompt males to avoid them in favor of older but more fecund females.
Chemical signals mediate many of life's processes. For organisms that use these signals to orient and navigate in their environment, where and when these cues are encountered is crucial in determining behavioral responses. In air and water, fluid mechanics impinge directly upon the distribution of odorous molecules in time and space. Animals frequently employ behavioral mechanisms that allow them to take advantage of both chemical and fluid dynamic information in order to move toward the source. In turbulent plumes, where odor is patchily distributed, animals are exposed to a highly intermittent signal. The most detailed studies that have attempted to measure fluid dynamic conditions, odor plume structure, and resultant orientation behavior have involved moths, crabs, and lobsters. The behavioral mechanisms employed by these organisms are different but generally integrate some form of chemically modulated orientation (chemotaxis) with a visual or mechanical assessment of flow conditions in order to steer up-current or upwind (rheo- or anemo-taxis, respectively). Across-stream turns are another conspicuous feature of odor-modulated tracks of a variety of organisms in different fluid conditions. In some cases, turning is initiated by detection of the lateral edges of a well-defined plume (crabs), whereas in other animals turning appears to be steered according to an internally generated program modulated by odor contacts (moth counterturning). Other organisms such as birds and fish may use similar mechanisms, but the experimental data for these organisms is not yet as convincing. The behavioral strategies employed by a variety of animals result in orientation responses that are appropriate for the dispersed, intermittent plumes dictated by the fluid-mechanical conditions in the environments that these different macroscopic organisms inhabit.
We characterized single upwind surges of flying male Helothis virescens moths in response to individual strands of pheromone generated experimentally in a wind tunnel. We then showed how this surge functions in this species as a basic 13.4-cm, 0.38-sec-long building block that is strung together repeatedly during typical male upwind flight in a normal pheromone plume. The template for a single iteration, complete with crosswind casting both before and after the straighter upwind surging portion, was exhibited by males flying upwind to pheromone and experiencing ifiament contactsjust frequently enough to produce successful upwind flight to the source, as hypothesized by an earlier model. Also as predicted, with more frequent filament contact by males, only the straightest upwind portions of the surges were reiterated, producing direct upwind flight with little crosswind casting. Electroantennogram recordings made from males in free Tfight upwind in a normal point source pheromone plume further support the idea that a high frequency offilaments encountered under the usual pheromone plume conditions promotes only these repeated straight surges. In-flight electroantennogram recordings also showed that when filament contacts cease, the casting, counterturning program begins to be expressed after a latency period of 0.30 sec. Together these results provide a plausible explanation for how male and female moths, and maybe other insects, fly successlly upwind in an odor plume and locate the source of odor, using a surging-casting, phasictonic response to the onset and disappearance of each odor strand.In the quest for understanding how male moths fly upwind and locate females (1-5) there have been suggestions (6, 7) that all odor-mediated flight in moths, including host plant location by females, may be explained by two programs, optomotor anemotaxis (2) and self-steered counterturning (8), that are turned on and modulated by odor fluctuations. It has also been pointed out (9, 10) that many other kinds of insects flying upwind to odor exhibit behavior somewhat similar to moths', and these other insects may also use these same mechanisms in odor-source location. Knowledge about the mechanisms used by moths should therefore be important for understanding the neuroethology of olfaction, the evolution of pheromone and host-plant-insect systems, and the potential application of pheromones in insect control.The physical structure of a pheromone plume created by a point source of odor is not a time-averaged homogeneous cloud. Turbulence causes the plume to break up into strands of odor-laden air (filaments) interspersed with pockets of clean air where little or no odor is present (11,12). The physical intermittency of these filaments is a requirement for male moths to sustain their upwind progress; they will not continue to fly upwind upon entering a homogeneous cloud of pheromone (4, 13) but will if this cloud is alternated with swaths of clean air (14).Recently, results from experiments investigating the highspeed beh...
The neural computations used to represent olfactory information in the brain have long been investigated. Recent studies in the insect antennal lobe suggest that precise temporal and/or spatial patterns of activity underlie the recognition and discrimination of different odours, and that these patterns may be strengthened by associative learning. It remains unknown, however, whether these activity patterns persist when odour intensity varies rapidly and unpredictably, as often occurs in nature. Here we show that with naturally intermittent odour stimulation, spike patterns recorded from moth antennal-lobe output neurons varied predictably with the fine-scale temporal dynamics and intensity of the odour. These data support the hypothesis that olfactory circuits compensate for contextual variations in the stimulus pattern with high temporal precision. The timing of output neuron activity is constantly modulated to reflect ongoing changes in stimulus intensity and dynamics that occur on a millisecond timescale.
Single-cell electrophysiological recordings were obtained from olfactory receptor neurons in sensilla trichodea on male antennae of the heliothine species Heliothis subflexa and the closely related congener H. virescens. A large percentage of sensilla (72% and 81%, respectively, of all sensilla sampled) contained a single odor-responsive receptor neuron tuned to the major pheromone component of both species, Z-11-hexadecenal. A second population of sensilla on H. subflexa antennae (18%) housed receptor neurons that were tuned to Z-9-hexadecenal but also responded with less sensitivity to Z-9-tetradecenal. A similar population of sensilla (4%) on H. virescens male antennae housed receptor neurons that were shown to be tuned specifically only to Z-9-tetradecenal, with no response to even high dosages of Z-9-hexadecenal. A third population of sensilla (comprising 8% and 16% of the sensilla sampled in H. subflexa and H. virescens, respectively) housed two olfactory receptor neurons, one of which was tuned to Z-11-hexadecenyl acetate and the other tuned to Z-11-hexadecenol. In H. subflexa the Z-11-hexadecenyl acetate-tuned neuron also responded to Z-9-tetradecenal with nearly equivalent sensitivity. The behavioral requirements of males of these two species for distinct pheromonal blends was, therefore, reflected by the subtle differences in the tuning properties of antennal olfactory receptor neurons.
Long distance sexual communication in moths has fascinated biologists because of the complex, precise female pheromone signals and the extreme sensitivity of males to specific pheromone molecules. Progress has been made in identifying some genes involved in female pheromone production and in male response. However, we have lacked information on the genetic changes involved in evolutionary diversification of these mate-finding mechanisms that is critical to understanding speciation in moths and other taxa. We used a combined quantitative trait locus (QTL) and candidate gene approach to determine the genetic architecture of sexual isolation in males of two congeneric moths, Heliothis subflexa and Heliothis virescens. We report behavioral and neurophysiological evidence that differential male responses to three female-produced chemicals (Z9-14:Ald, Z9-16:Ald, Z11-16:OAc) that maintain sexual isolation of these species are all controlled by a single QTL containing at least four odorant receptor genes. It is not surprising that pheromone receptor differences could control H. subflexa and H. virescens responses to Z9-16:Ald and Z9-14:Ald, respectively. However, central rather than peripheral level control over the positive and negative responses of H. subflexa and H. virescens to Z11-16:OAc had been expected. Tight linkage of these receptor genes indicates that mutations altering male response to complex blends could be maintained in linkage disequilibrium and could affect the speciation process.Other candidate genes such as those coding for pheromone binding proteins did not map to this QTL, but there was some genetic evidence of a QTL for response to Z11-16:OH associated with a sensory neuron membrane protein gene.mating | speciation | AFLP | odorant receptor | Heliothis E volutionary diversification of sexual communication traits remains paradoxical (1, 2) because signal production and signal reception are under independent genetic control, and a mutation causing an alteration in one component of the system is predicted to reduce efficiency of communication and to cause a loss of fitness. The resulting stabilizing selection is expected to promote evolutionary stasis, not diversification (3-5). Systems in which changes in signals and responses are governed by the same genetic alterations (i.e., pleiotropy) should be less evolutionarily constrained in many cases (6), and studies of mating communication have revealed a few systems that appear to have this property (7-9). However, no pleiotropy has been found between signal production and response in moths (e.g., 5, 10). Because female and male moths with divergent signals and responses appear to be selected against (11, 12), we have no simple explanation for the great diversity of moths (∼180,000 species) and moth pheromones (5,13,14).Beyond capturing the attention of evolutionary biologists, the diversity of long distance, pheromone-based sexual communication traits in moths has become a focus of some molecular biologists, biochemists, neurophysiologists, and communi...
Studies on numerous insect species suggest that male-produced sex pheromones play a role in attracting females; as aphrodisiacs, making females more quiescent; or as a means of inhibiting competing males. Male heliothine moths display abdominal hairpencils during courtship, but the specific effects of the odors released on female behavior have not yet been elucidated. This study investigates the role of male hairpencil compounds in female Heliothis virescens mating behavior. Female H. virescens were exposed to filter paper loaded with hairpencil extracts of male H. virescens, Heliothis subflexa and Helicoverpa zea, and observed for behavioral responses to odors. Single synthetic compounds found in the H. virescens hairpencil blend were also tested. In mating assays between single male and female H. virescens it was found that: (i) antennectomized females mated less frequently than sham-operated females; (ii) females mated less frequently with males whose hairpencils had been surgically removed; (iii) females mated with males with ablated hairpencils if a filter paper loaded with one male equivalent of H. virescens hairpencil extract was presented simultaneously; and (iv) this effect was species-specific, as presentation of H. subflexa or H. zea hairpencil extracts did not restore mate acceptance. This study suggests that odors released by male hairpencils are important in mate acceptance by female H. virescens, and may play a role in mate choice and species isolation.
The rules governing the central discrimination of odors are complex and poorly understood, but a growing body of evidence supports the hypothesis that olfactory glomeruli may represent functionally distinct coding modules in the brain. Testing this hypothesis requires that both the functional characteristics and the spatial position of the glomerulus under study be uniquely identifiable. To address these questions, we examined a specialized array of glomeruli (the macroglomerular complex; MGC) in the antennal lobe of male moths that receives input from olfactory receptor cells tuned specifically to female-released odorants that either promote upwind flight (conspecific sex pheromones) or inhibit it (interspecific antagonists). By using a three-dimensional reconstruction method based on high-resolution laser-scanning confocal microscopy, we generated precise spatial maps of the MGC glomeruli in two related noctuid species with similar pheromone chemistry, Heliothis virescens and Helicoverpa zea. To determine the breadth of tuning of individual MGC glomeruli in processing information about these social signals, we used intracellular recording and staining methods to examine the responses of projection (output) neurons that innervate MGC glomeruli and that each project an axon to higher integrative centers. In both species, a close correspondence was found between the odor specificity of the projection neurons and the glomerulus (or glomeruli) supplied by them. The binary blend of pheromone components for each species was represented by neural activity in only two distinct glomeruli in both H. virescens and H. zea. Odorants that antagonize upwind flight when they are added to the respective pheromonal blends evoked excitatory activity in output neurons restricted to a third glomerulus in the MGCs of both species. In summary, these results suggest that the selective activation of different combinations of functionally distinct MGC glomeruli is a general means for discriminating these specific attractant and antagonist chemical signals in the brain.
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