scholarly journals Sexually dimorphic traits and male-specific differentiation are actively regulated by Doublesex during specific developmental windows in Nasonia vitripennis

2020 ◽  
Author(s):  
Yidong Wang ◽  
Anna Rensink ◽  
Ute Fricke ◽  
Megan C. Riddle ◽  
Carol Trent ◽  
...  

AbstractSexually dimorphic traits in insects are rapidly evolving due to sexual selection which can ultimately lead to speciation. However, our knowledge of the underlying sex-specific molecular mechanisms is still scarce. Here we show that the highly conserved gene, Doublesex (Dsx), regulates rapidly diverging sexually dimorphic traits in the model parasitoid wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). We present here the revised full Dsx gene structure with an alternative first exon, and two additional male NvDsx isoforms, which gives important insights into the evolution of the sex-specific oligomerization domains and C-termini. We show the sex-specific NvDsx expression throughout development, and demonstrate that transient NvDsx silencing in different male developmental stages dramatically shifts the morphology of two sexually dimorphic traits from male to female, with the effect being dependent on the timing of silencing. In addition, transient silencing of NvDsx in early male larvae affects male genitalia tissue growth but not morphology. This indicates that male NvDsx is actively required to suppress female-specific traits and to promote male-specific traits during specific developmental windows. These results also strongly suggest that in N. vitripennis most sex-specific tissues fully differentiate in the embryonic stage and only need the input of NvDsx for growth afterwards. This provides a first insight into the regulatory activity of Dsx in the Hymenoptera and will help to better understand the evolutionary and molecular mechanisms involved in sex-specific development in this parasitoid wasp, which can eventually lead to the development of new synthetic genetics-based tools for biological pest control by parasitoid wasps.Significance StatementIn insects, male and female differentiation is regulated by the highly conserved transcription factor Doublesex (Dsx). The role of Dsx in regulating rapidly evolving sexually dimorphic traits has received less attention, especially in wasps and bees. Here, we mainly focused on Dsx regulation of two sexually dimorphic traits and male genitalia morphology in the parasitoid wasp, Nasonia vitripennis. We demonstrate that Dsx actively regulates male-specific tissue growth and morphology during specific developmental windows. These findings will help to better understand the molecular mechanisms underlying the rapid evolution of sexual differentiation and sexually dimorphic traits in insects, but may also be the starting point for the development of new tools for biological control of pest insects by parasitoid wasps.

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Laura Molina-García ◽  
Carla Lloret-Fernández ◽  
Steven J Cook ◽  
Byunghyuk Kim ◽  
Rachel C Bonnington ◽  
...  

Sexually dimorphic behaviours require underlying differences in the nervous system between males and females. The extent to which nervous systems are sexually dimorphic and the cellular and molecular mechanisms that regulate these differences are only beginning to be understood. We reveal here a novel mechanism by which male-specific neurons are generated in Caenorhabditis elegans through the direct transdifferentiation of sex-shared glial cells. This glia-to-neuron cell fate switch occurs during male sexual maturation under the cell-autonomous control of the sex-determination pathway. We show that the neurons generated are cholinergic, peptidergic, and ciliated putative proprioceptors which integrate into male-specific circuits for copulation. These neurons ensure coordinated backward movement along the mate’s body during mating. One step of the mating sequence regulated by these neurons is an alternative readjustment movement performed when intromission becomes difficult to achieve. Our findings reveal programmed transdifferentiation as a developmental mechanism underlying flexibility in innate behaviour.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Laura Pereira ◽  
Florian Aeschimann ◽  
Chen Wang ◽  
Hannah Lawson ◽  
Esther Serrano-Saiz ◽  
...  

The molecular mechanisms that control the timing of sexual differentiation in the brain are poorly understood. We found that the timing of sexually dimorphic differentiation of postmitotic, sex-shared neurons in the nervous system of the Caenorhabditis elegans male is controlled by the temporally regulated miRNA let-7 and its target lin-41, a translational regulator. lin-41 acts through lin-29a, an isoform of a conserved Zn finger transcription factor, expressed in a subset of sex-shared neurons only in the male. Ectopic lin-29a is sufficient to impose male-specific features at earlier stages of development and in the opposite sex. The temporal, sexual and spatial specificity of lin-29a expression is controlled intersectionally through the lin-28/let-7/lin-41 heterochronic pathway, sex chromosome configuration and neuron-type-specific terminal selector transcription factors. Two Doublesex-like transcription factors represent additional sex- and neuron-type specific targets of LIN-41 and are regulated in a similar intersectional manner.


2019 ◽  
Author(s):  
P.C. Liu ◽  
DeJun Hao ◽  
Hao-Yuan Hu ◽  
Jian-Rong Wei

Abstract Background Differences in the expression of genes present in both sexes are assumed to contribute to sex differences including behavioural, physiological and morphological dimorphisms. For enriching our knowledge of gender differences in an important egg parasitoid wasp, Anastatus disparis (Hymenoptera: Eupelmidae), sex-biased differences in gene expression were investigated using Illumina-based transcriptomic analysis. Results A total of 67201 resulting unigenes were annotated, including 4206 genes differentially expressed (i.e., sex-biased genes) between females and males including 243 specific genes; the majority of the sex-biased genes (63.72%) were female-biased. Sexually dimorphic traits related to flyability and longevity were discussed at the level of gene expression, improving our understanding of those biological traits. Besides, Gene Ontology (GO) enrichment analyses showed that the functional categories in sex-biased genes were mainly related to reproduction. Conclusions Overall, this study provides comprehensive insight into the sexually dimorphic traits of parasitoid wasps, offering a basis for future research to better understand the molecular mechanisms underlying such traits and improve the application of these insects to the biological control of pests.


2020 ◽  
Author(s):  
P.C. Liu ◽  
DeJun Hao ◽  
Hao-Yuan Hu ◽  
Jian-Rong Wei

Abstract BackgroundDifferences in the expression of genes present in both sexes are assumed to contribute to sex differences including behavioural, physiological and morphological dimorphisms. For enriching our knowledge of gender differences in an important egg parasitoid wasp, Anastatus disparis (Hymenoptera: Eupelmidae), sex-biased differences in gene expression were investigated using Illumina-based transcriptomic analysis. ResultsA total of 15812 resulting unigenes were annotated, and a large set of genes accounting for 50.09% of the total showed sex-biased expression and included 630 sex-specific genes. Gene Ontology (GO) enrichment analyses showed that the functional categories associated with sex-biased genes were mainly related to reproduction. In addition, the transcriptome data provided evidence that sex pheromones in A. disparis are produced by the female, and activity of 12-desaturases appear to have been replaced by 9-desaturases playing roles in sex pheromone production. The large set of sex-biased genes identified in this study provide a molecular background for sexually dimorphic traits such as flyability, longevity, and aggression in this species and suggests candidate venom proteins expressed only in females that could be used for biological control.ConclusionsThis study provides comprehensive insight into sexually dimorphic traits of a parasitoid wasp and can inform future research into the molecular mechanisms underlying such traits and the application of parasitoids to the biological control of pest species.


2020 ◽  
Author(s):  
P.C. Liu ◽  
DeJun Hao ◽  
Hao-Yuan Hu ◽  
Jian-Rong Wei

Abstract BackgroundDifferences in the expression of genes present in both sexes are assumed to contribute to sex differences including behavioural, physiological and morphological dimorphisms. For enriching our knowledge of gender differences in an important egg parasitoid wasp, Anastatus disparis (Hymenoptera: Eupelmidae), sex-biased differences in gene expression were investigated using Illumina-based transcriptomic analysis. ResultsA total of 15812 resulting unigenes were annotated, and a large set of genes accounting for 50.09% of the total showed sex-biased expression and included 630 sex-specific genes. Gene Ontology (GO) enrichment analyses showed that the functional categories associated with sex-biased genes were mainly related to reproduction. In addition, the transcriptome data provided evidence that sex pheromones in A. disparis are produced by the female, and activity of D12-desaturases appear to have been replaced by D9-desaturases playing roles in sex pheromone production. The large set of sex-biased genes identified in this study provide a molecular background for sexually dimorphic traits such as flyability, longevity, and aggression in this species and suggests candidate venom proteins expressed only in females that could be used for biological control.ConclusionsThis study provides comprehensive insight into sexually dimorphic traits of a parasitoid wasp and can inform future research into the molecular mechanisms underlying such traits and the application of parasitoids to the biological control of pest species.


2021 ◽  
Author(s):  
Garima Prazapati ◽  
Ankit Yadav ◽  
Anoop Ambili ◽  
Abhilasha Sharma ◽  
Rhitoban Raychoudhury

The reproductive success of a male is limited by the number of females it can mate with. Thus, males deploy elaborate mate-finding strategies to maximize access to females. In the haplodiploid wasp genus, Nasonia, which are parasitoids of cyclorrhaphous flies, mate-finding is restricted to the natal patch, where males compete for access to females. This study investigates whether there are any additional mate finding strategies of males, especially, whether they can identify the presence of adult females which are still inside the fly host. Results reveal that only one out of the four species, N. vitripennis, can distinguish which hosts specifically have adult female wasps indicating a species-specific unique mate-finding capability. Behavioral assays revealed that the cues used by N. vitripennis males are olfactory in nature and not auditory or visual. GC-MS analyses show that these olfactory cues are female-specific cuticular hydrocarbons (CHCs), possibly emanating from within the fly puparium. Further assays indicated that N. vitripennis males can also detect differences in the concentrations of compounds to identify female-specific cues from male-specific ones. This study, therefore, uncovers a previously unknown mate-finding strategy in one of the most widely studied parasitoid wasp.


2020 ◽  
Author(s):  
P.C. Liu ◽  
DeJun Hao ◽  
Hao-Yuan Hu ◽  
Jian-Rong Wei

Abstract Background: Differences in the expression of genes present in both sexes are assumed to contribute to sex differences including behavioural, physiological and morphological dimorphisms. For enriching our knowledge of gender differences in an important egg parasitoid wasp, Anastatus disparis (Hymenoptera: Eupelmidae), sex-biased differences in gene expression were investigated using Illumina-based transcriptomic analysis. Results: A total of 15812 resulting unigenes were annotated, and a large set of genes accounting for 50.09% of the total showed sex-biased expression and included 630 sex-specific genes. Gene Ontology (GO) enrichment analyses showed that the functional categories associated with sex-biased genes were mainly related to reproduction. In addition, the transcriptome data provided evidence that sex pheromones in A. disparis are produced by the female, and activity of D12-desaturases appear to have been replaced by D9-desaturases playing roles in sex pheromone production. The large set of sex-biased genes identified in this study provide a molecular background for sexually dimorphic traits such as flyability, longevity, and aggression in this species and suggests candidate venom proteins expressed only in females that could be used for biological control.Conclusions: This study provides comprehensive insight into sexually dimorphic traits of a parasitoid wasp and can inform future research into the molecular mechanisms underlying such traits and the application of parasitoids to the biological control of pest species.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Shimaa A. M. Ebrahim ◽  
Gaëlle J. S. Talross ◽  
John R. Carlson

AbstractParasitoid wasps inflict widespread death upon the insect world. Hundreds of thousands of parasitoid wasp species kill a vast range of insect species. Insects have evolved defensive responses to the threat of wasps, some cellular and some behavioral. Here we find an unexpected response of adult Drosophila to the presence of certain parasitoid wasps: accelerated mating behavior. Flies exposed to certain wasp species begin mating more quickly. The effect is mediated via changes in the behavior of the female fly and depends on visual perception. The sight of wasps induces the dramatic upregulation in the fly nervous system of a gene that encodes a 41-amino acid micropeptide. Mutational analysis reveals that the gene is essential to the behavioral response of the fly. Our work provides a foundation for further exploration of how the activation of visual circuits by the sight of a wasp alters both sexual behavior and gene expression.


2007 ◽  
Vol 139 (5) ◽  
pp. 678-684 ◽  
Author(s):  
B.H. King

AbstractWhen habitat quality is variable, there should be strong selection for the ability to detect and respond to the variation. Adult females of the parasitoid wasp Nasonia vitripennis (Walker) are known to increase their restlessness (the proportion of time in locomotion) both during and after exposure to a poor quality host. Doing so provides a mechanism for leaving a poor host and potentially finding a better host. This study examined whether restlessness also changes in response to competition as indicated by the presence of adult conspecifics. Both restlessness and the probability of dispersing across an inhospitable environment were greater when a female was with another female than when she was alone. However, restlessness did not remain elevated after the other female was removed. In contrast with females, restlessness of males did not increase either during or after exposure to other males, and the probability of dispersing across an inhospitable environment was unaffected by the presence of another male. The difference between females and males may be related to differences in dispersal ability and in the abundance and distribution of hosts versus mates.


2014 ◽  
Vol 104 (3) ◽  
pp. 307-313 ◽  
Author(s):  
Y. Tsutsui ◽  
K. Maeto ◽  
K. Hamaguchi ◽  
Y. Isaki ◽  
Y. Takami ◽  
...  

AbstractAlthough apomixis is the most common form of parthenogenesis in diplodiploid arthropods, it is uncommon in the haplodiploid insect order Hymenoptera. We found a new type of spontaneous apomixis in the Hymenoptera, completely lacking meiosis and the expulsion of polar bodies in egg maturation division, on the thelytokous strain of a parasitoid waspMeteorus pulchricornis(Wesmael) (Braconidae, Euphorinae) on pest lepidopteran larvaeSpodoptera litura(Fabricius) (Noctuidae). The absence of the meiotic process was consistent with a non-segregation pattern in the offspring of heterozygous females, and no positive evidence was obtained for the induction of thelytoky by any bacterial symbionts. We discuss the conditions that enable the occurrence of such rare cases of apomictic thelytoky in the Hymenoptera, suggesting the significance of fixed heterosis caused by hybridization or polyploidization, symbiosis with bacterial agents, and occasional sex. Our finding will encourage further genetic studies on parasitoid wasps to use asexual lines more wisely for biological control.


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