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Current Biology : CB Aug 2018To communicate with conspecifics, animals deploy various strategies to release pheromones, chemical signals modulating social and sexual behaviors [1-5]. Importantly, a...
To communicate with conspecifics, animals deploy various strategies to release pheromones, chemical signals modulating social and sexual behaviors [1-5]. Importantly, a single pheromone induces different behaviors depending on the context and exposure dynamics [6-8]. Therefore, to comprehend the ethological role of pheromones, it is essential to characterize how neurons in the recipients respond to temporally and spatially fluctuating chemical signals emitted by donors during natural interactions. In Drosophila melanogaster, the male pheromone 11-cis-vaccenyl acetate (cVA) [9] activates specific olfactory receptor neurons (ORNs) [10, 11] to regulate diverse social and sexual behaviors in recipients [12-15]. Physicochemical analyses have identified this chemical on an animal's body [16, 17] and in its local environment [18, 19]. However, because these methods are imprecise in capturing spatiotemporal dynamics, it is poorly understood how individual pheromone cues are released, detected, and interpreted by recipients. Here, we developed a system based on bioluminescence to monitor neural activity in freely interacting Drosophila, and investigated the active detection and perception of the naturally emitted cVA. Unexpectedly, neurons specifically tuned to cVA did not exhibit significant activity during physical interactions between males, and instead responded strongly to olfactory landmarks deposited by males. These landmarks mediated attraction through Or67d receptors and allured both sexes to the marked region. Importantly, the landmarks remained attractive even when a pair of flies was engaged in courtship behavior. In contrast, female deposits did not affect the exploration pattern of either sex. Thus, Drosophila use pheromone marking to remotely signal their sexual identity and to enhance social interactions.
Topics: Animals; Drosophila melanogaster; Female; Luminescent Measurements; Male; Oleic Acids; Olfactory Perception; Olfactory Receptor Neurons; Pheromones; Sex Attractants; Sexual Behavior, Animal; Smell; Synaptic Transmission
PubMed: 30078566
DOI: 10.1016/j.cub.2018.06.005 -
The Plant Journal : For Cell and... Aug 2014Algae are found in all aquatic and many terrestrial habitats. They are dominant in phytoplankton and biofilms thereby contributing massively to global primary... (Review)
Review
Algae are found in all aquatic and many terrestrial habitats. They are dominant in phytoplankton and biofilms thereby contributing massively to global primary production. Since algae comprise photosynthetic representatives of the various protoctist groups their physiology and appearance is highly diverse. This diversity is also mirrored in their characteristic life cycles that exhibit various facets of ploidy and duration of the asexual phase as well as gamete morphology. Nevertheless, sexual reproduction in unicellular and colonial algae usually has as common motive that two specialized, sexually compatible haploid gametes establish physical contact and fuse. To guarantee mating success, processes during sexual reproduction are highly synchronized and regulated. This review focuses on sex pheromones of algae that play a key role in these processes. Especially, the diversity of sexual strategies as well as of the compounds involved are the focus of this contribution. Discoveries connected to algal pheromone chemistry shed light on the role of key evolutionary processes, including endosymbiotic events and lateral gene transfer, speciation and adaptation at all phylogenetic levels. But progress in this field might also in the future provide valid tools for the manipulation of aquaculture and environmental processes.
Topics: Chlorophyta; Pheromones; Reproduction; Stramenopiles
PubMed: 24597605
DOI: 10.1111/tpj.12496 -
ELife Nov 2022Behavioural economists have identified many psychological manipulations which affect perceived value. A prominent example of this is bundling, in which several small...
Behavioural economists have identified many psychological manipulations which affect perceived value. A prominent example of this is bundling, in which several small gains (or costs) are experienced as more valuable (or costly) than if the same total amount is presented together. While extensively demonstrated in humans, to our knowledge this effect has never been investigated in an animal, let alone an invertebrate. We trained individual workers to two of three conditions in which either costs (travel distance), gains (sucrose reward), or both were either bundled or segregated: (1) both costs and gains bundled, (2) both segregated, and (3) only gains segregated. We recorded pheromone deposition on the ants' return trips to the nest as measure of perceived value. After training, we offer the ants a binary choice between odours associated with the treatments. While bundling treatment did not affect binary choice, it strongly influenced pheromone deposition. Ants deposited c. 80% more pheromone when rewards were segregated but costs bundled as compared with both costs and rewards being bundled. This pattern is further complicated by the pairwise experience each animal made, and which of the treatments it experiences first during training. This demonstrates that even insects are influenced by bundling effects. We propose that the deviation between binary choice and pheromone deposition in this case may be due to a possible linearity in distance perception in ants, while almost all other sensory perception in animals is logarithmic.
Topics: Animals; Humans; Ants; Pheromones; Reward; Odorants; Sucrose
PubMed: 36412093
DOI: 10.7554/eLife.79314 -
ELife Mar 2017Differences in longevity between sexes is a mysterious yet general phenomenon across great evolutionary distances. To test the roles of responses to environmental cues...
Differences in longevity between sexes is a mysterious yet general phenomenon across great evolutionary distances. To test the roles of responses to environmental cues and sexual behaviors in longevity regulation, we examined male lifespan under solitary, grouped, and mated conditions. We find that neurons and the germline are required for male pheromone-dependent male death. Hermaphrodites with a masculinized nervous system secrete male pheromone and are susceptible to male pheromone killing. Male pheromone-mediated killing is unique to androdioecious , and may reduce the number of males in hermaphroditic populations; neither males nor females of gonochoristic species are susceptible to male pheromone killing. By contrast, mating-induced death, which is characterized by germline-dependent shrinking, glycogen loss, and ectopic vitellogenin expression, utilizes distinct molecular pathways and is shared between the sexes and across species. The study of sex- and species-specific regulation of aging reveals deeply conserved mechanisms of longevity and population structure regulation.
Topics: Animals; Caenorhabditis; Longevity; Male; Pheromones; Sexual Behavior, Animal
PubMed: 28290982
DOI: 10.7554/eLife.23493 -
Cellular and Molecular Life Sciences :... Jul 2023Male moths utilize their pheromone communication systems to distinguish potential mates from other sympatric species, which contributes to maintaining reproductive...
Male moths utilize their pheromone communication systems to distinguish potential mates from other sympatric species, which contributes to maintaining reproductive isolation and even drives speciation. The molecular mechanisms underlying the evolution of pheromone communication systems are usually studied between closely-related moth species for their similar but divergent traits associated with pheromone production, detection, and/or processing. In this study, we first identified the functional differentiation in two orthologous pheromone receptors, OR14b, and OR16, in four Helicoverpa species, Helicoverpa armigera, H. assulta, H. zea, and H. gelotopoeon. To understand the substrate response specificity of these two PRs, we performed all-atom molecular dynamics simulations of OR14b and OR16 based on AlphaFold2 structural prediction, and molecular docking, allowing us to predict a few key amino acids involved in substrate binding. These candidate residues were further tested and validated by site-directed mutagenesis and functional analysis. These results together identified two hydrophobic amino acids at positions 164 and 232 are the determinants of the response specificity of HarmOR14b and HzeaOR14b to Z9-14:Ald and Z9-16:Ald by directly interacting with the substrates. Interestingly, in OR16 orthologs, we found that position 66 alone determines the specific binding of Z11-16:OH, likely via allosteric interactions. Overall, we have developed an effective integrated method to identify the critical residues for substrate selectivity of ORs and elucidated the molecular mechanism of the diversification of pheromone recognition systems.
Topics: Animals; Male; Receptors, Pheromone; Molecular Docking Simulation; Pheromones; Moths
PubMed: 37421463
DOI: 10.1007/s00018-023-04837-1 -
BMC Biology Jan 2023Camponotus floridanus ant colonies are comprised of a single reproductive queen and thousands of sterile female offspring that consist of two morphologically distinct...
BACKGROUND
Camponotus floridanus ant colonies are comprised of a single reproductive queen and thousands of sterile female offspring that consist of two morphologically distinct castes: smaller minors and larger majors. Minors perform most of the tasks within the colony, including brood care and food collection, whereas majors have fewer clear roles and have been hypothesized to act as a specialized solider caste associated with colony defense. The allocation of workers to these different tasks depends, in part, on the detection and processing of local information including pheromones and other chemical blends such as cuticular hydrocarbons. However, the role peripheral olfactory sensitivity plays in establishing and maintaining morphologically distinct worker castes and their associated behaviors remains largely unexplored.
RESULTS
We examined the electrophysiological responses to general odorants, cuticular extracts, and a trail pheromone in adult minor and major C. floridanus workers, revealing that the repertoire of social behaviors is positively correlated with olfactory sensitivity. Minors in particular display primarily excitatory responses to olfactory stimuli, whereas major workers primarily manifest suppressed, sub-solvent responses. The notable exception to this paradigm is that both minors and majors display robust, dose-dependent excitatory responses to conspecific, non-nestmate cuticular extracts. Moreover, while both minors and majors actively aggress non-nestmate foes, the larger and physiologically distinct majors display significantly enhanced capabilities to rapidly subdue and kill their adversaries.
CONCLUSIONS
Our studies reveal the behavioral repertoire of minors and majors aligns with profound shifts in peripheral olfactory sensitivity and odor coding. The data reported here support the hypothesis that minors are multipotential workers with broad excitatory sensitivity, and majors are dedicated soldiers with a highly specialized olfactory system for distinguishing non-nestmate foes. Overall, we conclude that C. floridanus majors do indeed represent a physiologically and behaviorally specialized soldier caste in which caste-specific olfactory sensitivity plays an important role in task allocation and the regulation of social behavior in ant colonies.
Topics: Animals; Female; Ants; Smell; Social Behavior; Pheromones; Odorants
PubMed: 36617574
DOI: 10.1186/s12915-022-01505-x -
MSphere Jun 2022The CCAAT-binding heme activator protein (HAP) complex, comprising the DNA-binding heterotrimeric complex Hap2/3/5 and transcriptional activation subunit HapX, is a key...
The CCAAT-binding heme activator protein (HAP) complex, comprising the DNA-binding heterotrimeric complex Hap2/3/5 and transcriptional activation subunit HapX, is a key regulator of iron homeostasis, mitochondrial functions, and pathogenicity in Cryptococcus neoformans, which causes fatal meningoencephalitis. However, its role in the development of human fungal pathogens remains unclear. To elucidate the role of the HAP complex in C. neoformans development, we constructed Δ, Δ, Δ, and Δ mutants and their complemented congenic α H99 and YL99 strains. The HAP complex plays a conserved role in iron utilization and stress responses in cells of both mating types. Deletion of any of the HAP complex components markedly enhances filamentation during bisexual mating. However, the Hap2/3/5 complex, but not HapX, is crucial in repressing pheromone production and cell fusion and is thus a critical repressor of sexual differentiation of C. neoformans. Interestingly, deletion of the heterotrimeric complex transcriptionally regulated both positive and negative regulators in the pheromone-responsive Cpk1 mitogen-activated protein kinase (MAPK) pathway. Chromatin immunoprecipitation-quantitative PCR analysis revealed that the HAP complex physically bound to the CCAAT motif of the and promoter regions. Notably, the HAP complex was differentially localized depending on the mating type in basal conditions; it was enriched in the nuclei of α cells but diffused in the cytoplasm of cells. Interestingly, however, a portion of the HAP complex in both mating types relocalized to the cell membrane during mating. In conclusion, the Hap2/3/5 heterotrimeric complex and HapX play major and minor roles, respectively, in repressing the sexual development of C. neoformans in association with the Cpk1 MAPK pathway. Cryptococcus neoformans isolates are of two mating types: α strains, which are predominant, and strains, isolated from the sub-Saharan African region, where cryptococcosis is most abundant and severe. Here, we demonstrated the function of the CCAAT-binding HAP complex (Hap2/3/5/X) as a transcriptional repressor of Cpk1 pathway-related genes in cells of both mating types. Deletion of any HAP complex component markedly enhanced filamentation without affecting normal sporulation. In particular, deletion of the DNA-binding HAP complex components (Hap2/3/5), but not HapX, markedly enhanced pheromone production and cell fusion efficiency, validating its repressive role in the early stage of mating in C. neoformans. The HAP complex regulates the expression of both negative and positive mating regulators and is thus crucial for the regulation of the Cpk1 MAPK pathway during mating. This study provides insights into the complex signaling networks governing the sexual differentiation of C. neoformans.
Topics: Cryptococcosis; Cryptococcus neoformans; DNA; Heme; Hemeproteins; Humans; Iron; Mitogen-Activated Protein Kinases; Pheromones; Sexual Development
PubMed: 35638350
DOI: 10.1128/msphere.00170-22 -
Biomolecules Apr 2022In , the p21-activated kinase Cla4p regulates polarized morphogenesis and cytokinesis. However, it remains unknown how Cla4p kinase activity is regulated. After...
In , the p21-activated kinase Cla4p regulates polarized morphogenesis and cytokinesis. However, it remains unknown how Cla4p kinase activity is regulated. After pheromone exposure, yeast cells temporally separate the mitotic and mating programs by sequestering Fus2p in the nucleus until cell cycle completion, after which Fus2p exits to facilitate cell fusion. Previously, we showed that sequestration is regulated by two opposing protein kinases, Cla4p and Fus3p. Phosphorylation of Fus2p-S67 by Cla4p promotes nuclear localization by both activating nuclear import and blocking export. During mating, phosphorylation of Fus2p-S85 and Fus2p-S100 by Fus3p promotes nuclear export and blocks import. Here, we find that Cla4p kinase activity is itself down-regulated during mating. Pheromone exposure causes Cla4p hyper-phosphorylation and reduced Fus2p-S67 phosphorylation, dependent on Fus3p. Multiple phosphorylation sites in Cla4p are mating- and/or Fus3p-specific. Of these, Cla4p-S186 phosphorylation reduced the kinase activity of Cla4p, in vitro. A phosphomimetic mutation caused a strong reduction in Fus2p-S67 phosphorylation and nuclear localization, in vivo. More generally, a non-phosphorylatable mutation, , caused failure to maintain pheromone arrest and delayed formation of the mating-specific septin morphology. Thus, as cells enter the mating pathway, Fus3p counteracts Cla4p kinase activity to allow proper mating differentiation.
Topics: Cell Nucleus; Mitogen-Activated Protein Kinases; Pheromones; Phosphorylation; Protein Serine-Threonine Kinases; Saccharomyces cerevisiae; Saccharomyces cerevisiae Proteins
PubMed: 35454186
DOI: 10.3390/biom12040598 -
European Journal of Protistology Jun 2024In Euplotes, protein pheromones regulate cell reproduction and mating by binding cells in autocrine or heterologous fashion, respectively. Pheromone binding sites...
In Euplotes, protein pheromones regulate cell reproduction and mating by binding cells in autocrine or heterologous fashion, respectively. Pheromone binding sites (receptors) are identified with membrane-bound pheromone isoforms determined by the same genes specifying the soluble forms, establishing a structural equivalence in each cell type between the two twin proteins. Based on this equivalence, autocrine and heterologous pheromone/receptor interactions were investigated analyzing how native molecules of pheromones Er-1 and Er-13, distinctive of mating compatible E. raikovi cell types, associate into crystals. Er-1 and Er-13 crystals are equally formed by molecules that associate cooperatively into oligomeric chains rigorously taking a mutually opposite orientation, and each burying two interfaces. A minor interface is pheromone-specific, while a major one is common in Er-1 and Er-13 crystals. A close structural inspection of this interface suggests that it may be used by Er-1 and Er-13 to associate into heterodimers, yet inapt to further associate into higher complexes. Pheromone-molecule homo-oligomerization into chains accounts for clustering and internalization of autocrine pheromone/receptor complexes in growing cells, while the heterodimer unsuitability to oligomerize may explain why heterologous pheromone/receptor complexes fail clustering and internalization. Remaining on the cell surface, they are credited with a key role in cell-cell mating adhesion.
Topics: Pheromones; Euplotes; Protozoan Proteins; Protein Multimerization; Protein Binding; Autocrine Communication; Receptors, Pheromone
PubMed: 38520753
DOI: 10.1016/j.ejop.2024.126075 -
Genes & Genetic Systems Oct 2019The vomeronasal organ (VNO) plays a key role in sensing pheromonal cues, which elicit innate responses and induce social and sexual behaviors. The vomeronasal receptor 1... (Review)
Review
The vomeronasal organ (VNO) plays a key role in sensing pheromonal cues, which elicit innate responses and induce social and sexual behaviors. The vomeronasal receptor 1 genes, V1Rs, encode members of a pheromone receptor family that are mainly expressed in the VNO. Previous studies have revealed that the V1R family shows extraordinary variety among mammalian species owing to successive gene gains and losses. Because species-specific pheromonal interaction may facilitate species-specific reproductive behaviors, understanding the evolution of V1Rs in terms of their origin, repertoire and phylogeny should provide insight into the mechanisms of animal diversification. Here I summarize recent studies about the V1R family from its initial discovery in the rat genome to extensive comparative analyses among vertebrates. I further introduce our recent findings for V1Rs in a broad range of vertebrates, which reveal unexpected diversity as well as shared features common among lineages.
Topics: Animals; Evolution, Molecular; Gene Expression Regulation; Genome; Multigene Family; Pheromones; Phylogeny; Receptors, Pheromone; Sequence Analysis, DNA; Species Specificity; Vertebrates; Vomeronasal Organ
PubMed: 31474650
DOI: 10.1266/ggs.19-00009