Wolbachia influences the production of octopamine and affects Drosophila male aggression (original) (raw)
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Effects of Wolbachia infection on the postmating response in Drosophila melanogaster
Behavioral Ecology and Sociobiology, 2018
The series of stereotypical physiological and behavioral changes that female insects exhibit after mating are called postmating responses (PMR). Wolbachia are widespread intracellular bacteria that are well known for their ability to manipulate the host's reproductive behavior to facilitate their own maternal spreading. The effect of Wolbachia infection on insect hosts' PMR is not well understood. Here, we showed that after mating with male Drosophila melanogaster infected with Wolbachia, the uninfected female showed a significant decrease in egg laying on the first day. Furthermore, both Wolbachia-infected and Wolbachiauninfected females mated with infected males exhibited reduced feeding frequency, low receptivity to remating, and an extended median life span compared to those mated with uninfected males. To determine how Wolbachia triggered these alterations, we detected the influence of Wolbachia infection on the expression of some genes encoding seminal fluid proteins (Sfps) in D. melanogaster. These seminal fluid proteins are known to contribute to PMR upon transfer to females during copulation. We found that Acp26Aa, CG1656, and CG42474 were significantly downregulated in Wolbachia-infected males, whereas SP, CG1652, CG9997, and CG17575 showed no significant difference between Wolbachia-infected and Wolbachia-uninfected males. These results suggest that by decreasing the expression of some Sfps in the male hosts, Wolbachia may modulate sexual conflicts of their insect hosts in a way favoring females, thus benefit their own transmission through host populations. This study provides new insights into the host-endosymbiont interaction, which may support the application of endosymbionts for the control of pests and disease vectors. Significance statement Wolbachia are among the most successful intracellular bacteria that can infect many insect species as well as filarial nematodes. Wolbachia infect host reproductive tissues and are best known for manipulating host reproductive systems to enhance their transmission through host populations. Mating may result in many physiological and behavioral changes in female insects, which are called postmating responses (PMR). Here, we found that after mating with Wolbachia-infected males, Drosophila melanogaster females showed altered PMR, including decreased feeding frequency, attenuated propensity to remating, and prolonged median survival, when compared to those mated with uninfected males. This could be due to a reduction of seminal fluid proteins induced by Wolbachia infection. These findings may raise new speculation about bacteria-host interactions and the ecological and evolutionary consequences of parasitic infection. Keywords Wolbachia. Drosophila melanogaster. Postmating response. Seminal fluid proteins Zhen He and Hua-Bao Zhang contributed equally to this work. Communicated by N. Wedell
PLoS genetics, 2014
Chemosensory pheromonal information regulates aggression and reproduction in many species, but how pheromonal signals are transduced to reliably produce behavior is not well understood. Here we demonstrate that the pheromonal signals detected by Gr32a-expressing chemosensory neurons to enhance male aggression are filtered through octopamine (OA, invertebrate equivalent of norepinephrine) neurons. Using behavioral assays, we find males lacking both octopamine and Gr32a gustatory receptors exhibit parallel delays in the onset of aggression and reductions in aggression. Physiological and anatomical experiments identify Gr32a to octopamine neuron synaptic and functional connections in the suboesophageal ganglion. Refining the Gr32a-expressing population indicates that mouth Gr32a neurons promote male aggression and form synaptic contacts with OA neurons. By restricting the monoamine neuron target population, we show that three previously identified OA-Fru(M) neurons involved in behavior...
BMC evolutionary biology, 2017
One of the most widespread prokaryotic symbionts of invertebrates is the intracellular bacteria of Wolbachia genus which can be found in about 50% of insect species. Wolbachia causes both parasitic and mutualistic effects on its host that include manipulating the host reproductive systems in order to increase their transmission through the female germline, and increasing the host fitness. One of the mechanisms, promoting adaptation in biological organisms, is a non-specific neuroendocrine stress reaction. In insects, this reaction includes catecholamines, dopamine, serotonin and octopamine, which act as neurotransmitters, neuromodulators and neurohormones. The level of dopamine metabolism correlates with heat stress resistance in Drosophila adults. To examine Wolbachia effect on Drosophila survival under heat stress and dopamine metabolism we used five strains carrying the nuclear background of interbred Bi90 strain and cytoplasmic backgrounds with different genotype variants of Wol...
Russian Journal of Genetics, 2007
To determine biologically important effects of the cytoplasmic endosymbiont Wolbachia, two substrains of the same Drosophila melanogaster strain have been studied, one of them infected with Wolbachia and the other treated with tetracycline to eliminate the bacterium. Females of D. melanogaster infected with Wolbachia are more resistant to the fungus Blauveria bassiana (an insect pathogen) than uninfected females; infected females also exhibited changes in oviposition substrate preference. Males infected with the bacterium are more competitive than uninfected males. The possible role of Wolbachia in the formation of alternative ecological strategies of D. melanogaster is discussed.
Mapping Wolbachia distributions in the adult Drosophila brain
Cellular Microbiology, 2013
The maternally inherited bacterium Wolbachia infects the germline of most arthropod species. Using Drosophila simulans and D. melanogaster, we demonstrate that localization of Wolbachia to the fat bodies and adult brain is likely also a conserved feature of Wolbachia infection. Examination of three Wolbachia strains (WMel, WRiv, WPop) revealed that the bacteria preferentially concentrate in the central brain with low titres in the optic lobes. Distribution within regions of the central brain is largely determined by the Wolbachia strain, while the titre is influenced by both, the host species and the bacteria strain. In neurons of the central brain and ventral nerve cord, Wolbachia preferentially localizes to the neuronal cell bodies but not to axons. All examined Wolbachia strains are present intracellularly or in extracellular clusters, with the pathogenic W Pop strain exhibiting the largest and most abundant clusters. We also discovered that 16 of 40 lines from the Drosophila Genetic Reference Panel are Wolbachia infected. Direct comparison of Wolbachia infected and cured lines from this panel reveals that differences in physiological traits (chill coma recovery, starvation, longevity) are partially due to host line influences. In addition, a tetracycline-induced increase in Drosophila longevity was detected many generations after treatment.
Sex-specific behavioural symptoms of viral gut infection and Wolbachia in Drosophila melanogaster
Journal of insect physiology, 2015
All organisms are infected with a range of symbionts spanning the spectrum of beneficial mutualists to detrimental parasites. The fruit fly Drosophila melanogaster is a good example, as both endosymbiotic Wolbachia, and pathogenic Drosophila C Virus (DCV) commonly infect it. While the pathophysiology and immune responses against both symbionts are the focus of intense study, the behavioural effects of these infections have received less attention. Here we report sex-specific behavioural responses to these infections in D. melanogaster. DCV infection caused increased sleep in female flies, but had no detectable effect in male flies. The presence of Wolbachia did not reduce this behavioural response to viral infection. We also found evidence for a sex-specific cost of Wolbachia, as male flies infected with the endosymbiont became more lethargic when awake. We discuss these behavioural symptoms as potentially adaptive sickness behaviours.
Heads or Tails: Host-Parasite Interactions in the Drosophila-Wolbachia System
Applied and Environmental Microbiology, 2004
Wolbachia strains are endosymbiotic bacteria typically found in the reproductive tracts of arthropods. These bacteria manipulate host reproduction to ensure maternal transmission. They are usually transmitted vertically, so it has been predicted that they have evolved a mechanism to target the host's germ cells during development. Through cytological analysis we found that Wolbachia strains display various affinities for the germ line of Drosophila . Different Wolbachia strains show posterior, anterior, or cortical localization in Drosophila embryos, and this localization is congruent with the classification of the organisms based on the wsp ( Wolbachia surface protein) gene sequence. This embryonic distribution pattern is established during early oogenesis and does not change until late stages of embryogenesis. The posterior and anterior localization of Wolbachia resembles that of oskar and bicoid mRNAs, respectively, which define the anterior-posterior axis in the Drosophila o...
Asymmetrical Reinforcement and Wolbachia Infection in Drosophila
PLOS Biology, 2006
Reinforcement refers to the evolution of increased mating discrimination against heterospecific individuals in zones of geographic overlap and can be considered a final stage in the speciation process. One the factors that may affect reinforcement is the degree to which hybrid matings result in the permanent loss of genes from a species' gene pool. Matings between females of Drosophila subquinaria and males of D. recens result in high levels of offspring mortality, due to interspecific cytoplasmic incompatibility caused by Wolbachia infection of D. recens. Such hybrid inviability is not manifested in matings between D. recens females and D. subquinaria males. Here we ask whether the asymmetrical hybrid inviability is associated with a corresponding asymmetry in the level of reinforcement. The geographic ranges of D. recens and D. subquinaria were found to overlap across a broad belt of boreal forest in central Canada. Females of D. subquinaria from the zone of sympatry exhibit much stronger levels of discrimination against males of D. recens than do females from allopatric populations. In contrast, such reproductive character displacement is not evident in D. recens, consistent with the expected effects of unidirectional cytoplasmic incompatibility. Furthermore, there is substantial behavioral isolation within D. subquinaria, because females from populations sympatric with D. recens discriminate against allopatric conspecific males, whereas females from populations allopatric with D. recens show no discrimination against any conspecific males. Patterns of general genetic differentiation among populations are not consistent with patterns of behavioral discrimination, which suggests that the behavioral isolation within D. subquinaria results from selection against mating with Wolbachia-infected D. recens. Interspecific cytoplasmic incompatibility may contribute not only to post-mating isolation, an effect already widely recognized, but also to reinforcement, particularly in the uninfected species. The resulting reproductive character displacement not only increases behavioral isolation from the Wolbachia-infected species, but may also lead to behavioral isolation between populations of the uninfected species. Given the widespread occurrence of Wolbachia among insects, it thus appears that there are multiple ways by which these endosymbionts may directly and indirectly contribute to reproductive isolation and speciation.
The Journal of Experimental Biology
Maternally inherited intracellular bacteria Wolbachia cause both parasitic and mutualistic effects on their numerous insect hosts that include manipulating the host reproductive system in order to increase the bacteria spreading in a host population, and increasing the host fitness. Here we demonstrate that the type of Wolbachia infection determines the effect on Drosophila melanogaster egg production as a proxy for fecundity and metabolism of juvenile hormone (JH), which acts as gonadotropin in adult insects. For this study we used six D. melanogaster lineages carrying the nuclear background of interbred Bi90 lineage and cytoplasmic backgrounds with Wolbachia of different genotype variants or without it. wMelCS genotype of Wolbachia decreases the egg production in the infected D. melanogaster females in the beginning of oviposion and increases it later (since the sixth day after eclosion), wMelPop Wolbachia strain causes the opposite effect, while wMel, wMel2 and wMel4 genotypes of...
Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila. PLoS Biol
2010
Appropriate displays of aggression rely on the ability to recognize potential competitors. As in most species, Drosophila males fight with other males and do not attack females. In insects, sex recognition is strongly dependent on chemosensory communication, mediated by cuticular hydrocarbons acting as pheromones. While the roles of chemical and other sensory cues in stimulating male to female courtship have been well characterized in Drosophila, the signals that elicit aggression remain unclear. Here we show that when female pheromones or behavior are masculinized, males recognize females as competitors and switch from courtship to aggression. To masculinize female pheromones, a transgene carrying dsRNA for the sex determination factor transformer (traIR) was targeted to the pheromone producing cells, the oenocytes. Shortly after copulation males attacked these females, indicating that pheromonal cues can override other sensory cues. Surprisingly, masculinization of female behavior...