A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth.

Recognition of intra-specific olfactory signals within a complex environment of plant-related volatiles is crucial for reproduction in male moths. Sex pheromone information is detected by specific olfactory receptor neurons (Phe-ORNs), highly abundant on the male antenna. The information is then transmitted to the pheromone processing macroglomerular complex (MGC) within the primary olfactory center, the antennal lobe, where it is processed by local interneurons and projection neurons. Ultimately a behavioral response, orientation toward the pheromone source, is elicited. Volatile plant compounds (VPCs) are detected by other functional types of olfactory receptor neurons (ORNs) projecting in another area of the antennal lobe. However, Phe-ORNs also respond to some VPCs. Female-produced sex pheromones are emitted within a rich environment of VPCs, some of which have been shown to interfere with the detection and processing of sex pheromone information. As interference between the different odor sources might depend on the spatial and temporal features of the two types of stimuli, we investigated here behavioral and neuronal responses to a brief sex pheromone blend pulse in a VPC background as compared to a control background in the male noctuid moth Agrotis ipsilon. We observed male orientation behavior in a wind tunnel and recorded responses of Phe-ORNs and MGC neurons to a brief sex pheromone pulse within a background of individual VPCs. We also recorded the global input signal to the MGC using in vivo calcium imaging with the same stimulation protocol. We found that VPCs eliciting a response in Phe-ORNs and MGC neurons masked responses to the pheromone and decreased the contrast between background odor and the sex pheromone at both levels, whereas α-pinene did not interfere with first order processing. The calcium signal produced in response to a VPC background was tonic, lasting longer than the VPC stimulus duration, and masked entirely the pheromone response. One percent heptanal and linalool, in addition to the masking effect, caused a clear delay in responses of MGC neurons to the sex pheromone. Upwind flight toward the pheromone in a wind tunnel was also delayed but otherwise not altered by different doses of heptanal.

Unexpected plant odor responses in a moth pheromone system.

Male moths rely on olfactory cues to find females for reproduction. Males also use volatile plant compounds (VPCs) to find food sources and might use host-plant odor cues to identify the habitat of calling females. Both the sex pheromone released by conspecific females and VPCs trigger well-described oriented flight behavior toward the odor source. Whereas detection and central processing of pheromones and VPCs have been thought for a long time to be highly separated from each other, recent studies have shown that interactions of both types of odors occur already early at the periphery of the olfactory pathway. Here we show that detection and early processing of VPCs and pheromone can overlap between the two sub-systems. Using complementary approaches, i.e., single-sensillum recording of olfactory receptor neurons, in vivo calcium imaging in the antennal lobe, intracellular recordings of neurons in the macroglomerular complex (MGC) and flight tracking in a wind tunnel, we show that some plant odorants alone, such as heptanal, activate the pheromone-specific pathway in male Agrotis ipsilon at peripheral and central levels. To our knowledge, this is the first report of a plant odorant with no chemical similarity to the molecular structure of the pheromone, acting as a partial agonist of a moth sex pheromone.

Synaptotagmin I, a molecular target for steroid hormone signaling controlling the maturation of sexual behavior in an insect.

UNLABELLED: As in vertebrates, the insect steroid hormones, especially 20-hydroxyecdysone (20E), initiate and regulate sexual behavior by acting on the central nervous system. This 20E action is, in part, triggered by transcriptional events mediated through the binding of 20E to a heterodimer comprising the ecdysone receptor (EcR) and ultraspiracle (USP). However, to date, our knowledge about this genomic steroid pathway remains incomplete. In moths, males detect female sex pheromones, eliciting stereotyped sexual behavior. In Agrotis ipsilon males, the behavioral response and the neuronal sensitivity to sex pheromone in the olfactory center, the antennal lobe (AL), increase with age. We recently showed that 20E controlled this age-dependent olfactory plasticity via the activation of an EcR/USP-dependent pathway in the AL. Here, we cloned the gene encoding A. ipsilon synaptotagmin I (AisytI), a presynaptic vesicle protein known to act as a calcium sensor in neurotransmitter release. AisytI was expressed in the AL, where its amount increased with age, whereas its knockdown inhibited the sex pheromone-oriented flight of males. 20E administration to males induced AL AisytI expression in a dose-dependent and time-dependent manner. Moreover, A. ipsilon EcR silencing caused decreases in AL AisytI expression and the behavioral response to sex pheromone. Our results show that the synaptotagmin I gene is a target gene for the genomic steroid signaling that controls the expression of insect sexual behavior by acting on central sex pheromone processing. This study thus represents a significant advance in our understanding of the steroid actions that influence neural functions, and thereby behavioral plasticity, in various organisms. DATABASE: The nucleotide sequence of Agrotis ipsilon synaptotagmin I is available in the DDBJ/EMBL/GenBank databases under the accession number KJ863735.

The dilemma of Fisherian sexual selection: mate choice for indirect benefits despite rarity and overall weakness of trait-preference genetic correlation.

Fisher's mechanism of sexual selection is a fundamental element of evolutionary theory. In it nonrandom mate choice causes a genetic covariance between a male trait and female preference for that trait and thereby generates a positive feedback process sustaining accelerated coevolution of the trait and preference. Numerous theoretical models of Fisher's mechanism have confirmed its mathematical underpinnings, yet biologists have often failed to find evidence for trait-preference genetic correlation in populations in which the mechanism was expected to function. We undertook a survey of the literature to conduct a formal meta-analysis probing the incidence and strength of trait-preference correlation among animal species. Our meta-analysis found significant positive genetic correlations in fewer than 20% of the species studied and an overall weighted correlation that is slightly positive. Importantly, a significant positive correlation was not found in any thorough study that included multiple subgroups. We discuss several ways in which the dynamic, multivariate nature of mate choice may reduce the trait-preference genetic correlation predicted by Fisher's mechanism. We then entertain the possibilities that Fisherian-like processes sometimes function without genetic correlation, and that mate choice may persist in a population as long as genetic correlation, and therefore Fisher's mechanism, occurs intermittently.

Genetic architecture of sexual selection: QTL mapping of male song and female receiver traits in an acoustic moth.

Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to non-random mate choice or physical linkage. Such linkage disequilibria can accelerate the evolution of traits and preferences to exaggerated levels. Both theory and recent empirical findings on species recognition suggest that such linkage disequilibria may result from physical linkage or pleiotropy, but very little work has addressed this possibility within the context of sexual selection. We studied the genetic architecture of sexually selected traits by analyzing signals and preferences in an acoustic moth, Achroia grisella, in which males attract females with a train of ultrasound pulses and females prefer loud songs and a fast pulse rhythm. Both male signal characters and female preferences are repeatable and heritable traits. Moreover, female choice is based largely on male song, while males do not appear to provide direct benefits at mating. Thus, some genetic correlation between song and preference traits is expected. We employed a standard crossing design between inbred lines and used AFLP markers to build a linkage map for this species and locate quantitative trait loci (QTL) that influence male song and female preference. Our analyses mostly revealed QTLs of moderate strength that influence various male signal and female receiver traits, but one QTL was found that exerts a major influence on the pulse-pair rate of male song, a critical trait in female attraction. However, we found no evidence of specific co-localization of QTLs influencing male signal and female receiver traits on the same linkage groups. This finding suggests that the sexual selection process would proceed at a modest rate in A. grisella and that evolution toward exaggerated character states may be tempered. We suggest that this equilibrium state may be more the norm than the exception among animal species.

From speciation to introgressive hybridization: the phylogeographic structure of an island subspecies of termite, Reticulitermes lucifugus corsicus.

BACKGROUND: Although much research has been carried out into European Reticulitermes taxonomy in recent years, there is still much discussion about phylogenetic relationships. This study investigated the evolution from intra- to interspecific phylogeny in the island subspecies Reticulitermes lucifugus corsicus and threw new light on this phenomenon. An integrative approach based on microsatellites and mitochondrial and nuclear DNA sequences was used to analyze samples taken from a wide area around the Tyrrhenian sea and showed how the subspecies evolved from its origins to its most recent form on continental coasts. RESULTS: According to mitochondrial phylogeny and molecular clock calculations, island and continental taxa diverged significantly by vicariance in the Pleistocene glacial period. However, more recently, numerous migrations, certainly human-mediated, affected the structure of the populations. This study provided evidence of direct hybridization and multiple introgressions which occurred in several hybrid areas. Analysis using STRUCTURE based on microsatellite data identified a population in Provence (France) which differed considerably (Fst = 0.477) from populations on the island of Corsica and in Tuscany in the Italian peninsula. This new population, principally distributed in urban areas, is highly heterogeneous especially within the ITS2 regions where homogenization by concerted evolution does not appear to have been completed. CONCLUSION: This study provides an unusual picture of genetic interaction between termite populations in the Tyrrhenian area and suggests that more attention should be paid to the role of introgression and human impact on the recent evolution of European termites.