scholarly journals The insect somatostatin pathway gates vitellogenesis progression during reproductive maturation and the post-mating response

Author(s):  
Chen Zhang ◽  
Crisalejandra Rivera Pérez ◽  
Fernando Noriega ◽  
Young Joon Kim

Abstract Oogenesis is closely linked with reproductive maturation and mating status in females. In the fruit fly Drosophila melanogaster, vitellogenesis (yolk accumulation) is an important control point for oogenesis. Vitellogenesis begins upon eclosion and continues through the process of sexual maturation. Upon reaching sexual maturity, vitellogenesis is placed on hold until it is induced again by a mating signal. In flies, this mating signal is sex peptide (SP), a seminal substance that triggers robust egg-laying activity. However, the neural mechanisms that gate vitellogenesis in response to developmental and reproductive signals remain unclear. Here, we have identified a pair of thoracic ganglion neurons that produce the neuropeptide allatostatin C (AstC-mTh). AstC inhibits the biogenesis of juvenile hormone (JH), a key endocrine stimulator of vitellogenesis. Our genetic evidence indicates that AstC-mTh neurons gate both the initiation of vitellogenesis that occurs post-eclosion and its re-initiation post-mating. During sexual maturation, which takes place shortly after eclosion, AstC-mTh neurons are activated by excitatory inputs from SP abdominal ganglion (SAG) neurons. In mature virgin females, high sustained activity of SAG neurons seems to shut off vitellogenesis via continuous activation of the AstC-mTh neurons. Upon mating, however, SP inhibits SAG neurons, leading to AstC-mTh neuronal activation. As a result, the inhibition of the CA maintained by the AstC neurons is lifted. This permit both JH biosynthesis and the progression of vitellogenesis in mated females. Our work has uncovered a central neural circuit that gates the progression of oogenesis during sexual maturation and the post-mating response.

2021 ◽  
Vol 12 ◽  
Author(s):  
Ryo Hoshino ◽  
Ryusuke Niwa

In many insect species, mating stimuli can lead to changes in various behavioral and physiological responses, including feeding, mating refusal, egg-laying behavior, energy demand, and organ remodeling, which are collectively known as the post-mating response. Recently, an increase in germline stem cells (GSCs) has been identified as a new post-mating response in both males and females of the fruit fly, Drosophila melanogaster. We have extensively studied mating-induced increase in female GSCs of D. melanogaster at the molecular, cellular, and systemic levels. After mating, the male seminal fluid peptide [e.g. sex peptide (SP)] is transferred to the female uterus. This is followed by binding to the sex peptide receptor (SPR), which evokes post-mating responses, including increase in number of female GSCs. Downstream of SP-SPR signaling, the following three hormones and neurotransmitters have been found to act on female GSC niche cells to regulate mating-induced increase in female GSCs: (1) neuropeptide F, a peptide hormone produced in enteroendocrine cells; (2) octopamine, a monoaminergic neurotransmitter synthesized in ovary-projecting neurons; and (3) ecdysone, a steroid hormone produced in ovarian follicular cells. These humoral factors are secreted from each organ and are received by ovarian somatic cells and regulate the strength of niche signaling in female GSCs. This review provides an overview of the latest findings on the inter-organ relationship to regulate mating-induced female GSC increase in D. melanogaster as a model. We also discuss the remaining issues that should be addressed in the future.


2021 ◽  
Author(s):  
Bailly Tiphaine ◽  
Philip Kohlmeier ◽  
Rampal Etienne ◽  
Bregje Wertheim ◽  
Jean-Christophe Billeter

Being part of a group facilitates cooperation between group members, but also creates competition for limited resources. This conundrum is problematic for gravid females who benefit from being in a group, but whose future offspring may struggle for access to nutrition in larger groups. Females should thus modulate their reproductive output depending on their social context. Although social-context dependent modulation of reproduction is documented in a broad range of species, its underlying mechanisms and functions are poorly understood. In the fruit fly Drosophila melanogaster, females actively attract conspecifics to lay eggs on the same resources, generating groups in which individuals may cooperate or compete. The tractability of the genetics of this species allows dissecting the mechanisms underlying physiological adaptation to their social context. Here, we show that females produce eggs increasingly faster as group size increases. By laying eggs faster in group than alone, females appear to reduce competition between offspring and increase their likelihood of survival. In addition, females in a group lay their eggs during the light phase of the day, while isolated females lay them during the night. We show that responses to the presence of others are determined by vision through the motion detection pathway and that flies from any sex, mating status or species can trigger these responses. The mechanisms of this modulation of egg-laying by group is connected to a lifting of the inhibition of light on oogenesis and egg-laying by stimulating hormonal pathways involving juvenile hormone. Because modulation of reproduction by social context is a hallmark of animals with higher levels of sociality, our findings represent a protosocial mechanism in a species considered solitary that may have been the target of selection for the evolution of more complex social systems.


2021 ◽  
Author(s):  
Ki-Hyeon Seong ◽  
Siu Kang

AbstractMany animal species exhibit sex differences in the time period prior to reaching sexual maturity. However, the underlying mechanism for such biased maturation remains poorly understood. Females of the fruit flyDrosophila melanogastereclose 4 h faster on average than males, owing to differences in the pupal period between the sexes; this characteristic is referred to as the protogyny phenotype. Here, we aimed to elucidate the mechanism underlying the protogyny phenotype in the fruit fly using our newly developedDrosophilaIndividual Activity Monitoring and Detecting System (DIAMonDS), which can continuously detect the precise timing of both pupariation and eclosion of individual flies. Via this system, following the laying of eggs, we detected the precise time points of pupariation and eclosion of a large number of individual flies simultaneously and succeeded in identifying the tiny differences in pupal duration between females and males. We first explored the role of physiological sex by establishing transgender flies via knockdown of the sex-determination gene,transformer(tra) and its co-factortra2, which retained the protogyny phenotype. In addition, disruption of dosage compensation bymale-specific lethal(msl-2) knockdown did not affect the protogyny phenotype. TheDrosophilamaster sex switch gene—Sxlpromotes female differentiation viatraand turns off male dosage compensation through the repression ofmsl-2.However, we observed that stage-specific whole-body knockdown and mutation ofSxlinduced disturbance of the protogyny phenotype. These results suggest that an additional, non-canonical function ofSxlinvolves establishing the protogyny phenotype inD. melanogaster.Author summaryA wide variety of animals show differences in time points of sexual maturation between sexes. For example, in many mammals, including human beings, females mature faster than males. This maturation often takes several months or years, and precisely detecting the time point of maturation is challenging, because of the continuity of growth, especially in mammals. Moreover, the reason behind the difference in sexual maturation time points between sexes is not fully understood. The fruit flyDrosophila—a model organism—also shows biased maturation between the sexes, with females emerging 4 h faster than males (a characteristic known as the protogyny phenotype). To understand the mechanism underlying the protogyny phenotype, we used our newly developed system,DrosophilaIndividual Activity Monitoring and Detecting System (DIAMonDS), to detect the precise eclosion point in individual fruit flies. Surprisingly, our analysis of transgender flies obtained by knockdown and overexpression techniques indicated that a physiological gender might not be necessary requirement for protogyny and that a non-canonical novel function of the fruit fly master sex switch gene,Sxl, regulates protogyny in fruit flies.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Rajib Majumder ◽  
Brodie Sutcliffe ◽  
Phillip W. Taylor ◽  
Toni A. Chapman

Abstract Insects typically host substantial microbial communities (the ‘microbiome’) that can serve as a vital source of nutrients and also acts as a modulator of immune function. While recent studies have shown that diet is an important influence on the gut microbiome, very little is known about the dynamics underpinning microbial acquisition from natural food sources. Here, we addressed this gap by comparing the microbiome of larvae of the polyphagous fruit fly Bactrocera tryoni (‘Queensland fruit fly’) that were collected from five different fruit types (sapodilla [from two different localities], hog plum, pomegranate, green apple, and quince) from North-east to South-east Australia. Using Next-Generation Sequencing on the Illumina MiSeq platform, we addressed two questions: (1) what bacterial communities are available to B. tryoni larvae from different host fruit; and (2) how does the microbiome vary between B. tryoni larvae and its host fruit? The abundant bacterial taxa were similar for B. tryoni larvae from different fruit despite significant differences in the overall microbial community compositions. Our study suggests that the bacterial community structure of B. tryoni larvae is related less to the host fruit (diet) microbiome and more to vertical transfer of the microbiome during egg laying. Our findings also suggest that geographic location may play a quite limited role in structuring of larval microbiomes. This is the first study to use Next-Generation Sequencing to analyze the microbiome of B. tryoni larvae together with the host fruit, an approach that has enabled greatly increased resolution of relationships between the insect’s microbiome and that of the surrounding host tissues.


2021 ◽  
Vol 145 ◽  
pp. 111201
Author(s):  
Xiang Meng ◽  
Junjie Hu ◽  
Richard E. Plant ◽  
Tim E. Carpenter ◽  
James R. Carey
Keyword(s):  

2021 ◽  
Author(s):  
Matthew Smith ◽  
Kyle S. Honegger ◽  
Glenn Turner ◽  
Benjamin de Bivort

AbstractIndividuals vary in their innate behaviors, even when they have the same genome and have been reared in the same environment. The extent of individuality in plastic behaviors, like learning, is less well characterized. Also unknown is the extent to which intragenotypic differences in learning generalize: if an individual performs well in one assay, will it perform well in other assays? We investigated this using the fruit fly Drosophila melanogaster, an organism long-used to study the mechanistic basis of learning and memory. We found that isogenic flies, reared in identical lab conditions, and subject to classical conditioning that associated odorants with electric shock, exhibit clear individuality in their learning responses. Flies that performed well when an odor was paired with shock tended to perform well when other odors were paired with shock, or when the original odor was paired with bitter taste. Thus, individuality in learning performance appears to be prominent in isogenic animals reared identically, and individual differences in learning performance generalize across stimulus modalities. Establishing these results in flies opens up the possibility of studying the genetic and neural circuit basis of individual differences in learning in a highly suitable model organism.


2020 ◽  
Author(s):  
Louis Ho ◽  
Martin Daniel-Ivad ◽  
Swathi Jeedigunta ◽  
Jing Li ◽  
Konstantin Iliadi ◽  
...  

Abstract Actinobacteria such as the filamentous streptomycetes are widely known for their ability to produce specialized metabolites that include antibacterial and antifungal compounds. In addition, a growing body of work demonstrates that many insects harbour actinobacteria on their bodies and in their nests. The result of these mutualistic relationships is the protection of their offspring or food sources by virtue of the bacterially encoded specialized metabolites. However, some actinobacteria produce molecules that are toxic to insects and the relevance of this toxicity in nature is unknown. We have explored interactions between streptomycetes and the fruit fly Drosophila. We find that many streptomycetes produce specialized metabolites that have potent larvicidal effects against the fly. Larvae that ingest spores of the species that produce these toxic molecules die as a result. Strikingly, the mechanism of toxicity is specific to the bacterium’s chemical arsenal: cosmomycin D producing cells induce a relatively slow-acting cell death-like response in the larval digestive tract and avermectin producing cells induce rapid onset, whole-body paralysis. We further show that fruit flies are attracted to the volatile terpene 2-methylisoborneol that is produced by most streptomycetes. This interaction can influence their food choice and egg-laying destination such that they preferentially deposit their eggs on contaminated food sources. As a result, the larvae that hatch in these toxic environments are subsequently killed. This phenomena of terpene-mediated attraction and specialized metabolite toxicity must pose a significant risk to insects in nature.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Yves F Widmer ◽  
Cornelia Fritsch ◽  
Magali M Jungo ◽  
Silvia Almeida ◽  
Boris Egger ◽  
...  

Lasting changes in gene expression are critical for the formation of long-term memories (LTMs), depending on the conserved CrebB transcriptional activator. While requirement of distinct neurons in defined circuits for different learning and memory phases have been studied in detail, only little is known regarding the gene regulatory changes that occur within these neurons. We here use the fruit fly as powerful model system to study the neural circuits of CrebB-dependent appetitive olfactory LTM. We edited the CrebB locus to create a GFP-tagged CrebB conditional knockout allele, allowing us to generate mutant, post-mitotic neurons with high spatial and temporal precision. Investigating CrebB-dependence within the mushroom body (MB) circuit we show that MB α/β and α’/β’ neurons as well as MBON α3, but not in dopaminergic neurons require CrebB for LTM. Thus, transcriptional memory traces occur in different neurons within the same neural circuit.


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