Maternal provision of non‐sex‐specific <i>transformer</i> messenger RNA in sex determination of the wasp <i>Asobara tabida</i>

Geuverink, Elzemiek; Verhulst, Eveline C.; Leussen, M. van; Zande, Louis van de; Beukeboom, Leo W.

doi:10.1111/imb.12352

Cited by 12 publications

(15 citation statements)

References 45 publications

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“…Some parasitoids have developed completely different sex determination mechanisms (e.g. [54–56]). The relatively frequent evolution of countermeasures to DMP suggests strong selection against it in the evolutionary history of these species.…”

Section: Discussionmentioning

confidence: 99%

Increased fluctuation in a butterfly metapopulation leads to diploid males and decline of a hyperparasitoid

2018

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Climate change can increase spatial synchrony of population dynamics, leading to large-scale fluctuation that destabilizes communities. High trophic level species such as parasitoids are disproportionally affected because they depend on unstable resources. Most parasitoid wasps have complementary sex determination, producing sterile males when inbred, which can theoretically lead to population extinction via the diploid male vortex (DMV). We examined this process empirically using a hyperparasitoid population inhabiting a spatially structured host population in a large fragmented landscape. Over four years of high host butterfly metapopulation fluctuation, diploid male production by the wasp increased, and effective population size declined precipitously. Our multitrophic spatially structured model shows that host population fluctuation can cause local extinctions of the hyperparasitoid because of the DMV. However, regionally it persists because spatial structure allows for efficient local genetic rescue via balancing selection for rare alleles carried by immigrants. This is, to our knowledge, the first empirically based study of the possibility of the DMV in a natural host–parasitoid system.

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Section: Discussionmentioning

confidence: 99%

Increased fluctuation in a butterfly metapopulation leads to diploid males and decline of a hyperparasitoid

2018

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“…mellifera, N. vitripennis and As. tabida (Nissen et al, 2012;Geuverink et al, 2017Geuverink et al, , 2018. We performed protein-protein interaction assays in N. vitripennis to test the hypothetical TRA/TRA2 binding complex in Hymenoptera.…”

Section: Discussionmentioning

confidence: 99%

“…The selected transcripts were the female-specific variant of Lc-tra and Nv-tra (Werren et al, 2010) and the single splice variant of Lc-traB. The chosen splice variants of tra2 (Lc-tra2 A and Nv-tra2 A ) were most abundant in N. vitripennis and conserved in other Hymenoptera (translated into FESRGIG motif) (Geuverink et al, 2017(Geuverink et al, , 2018. Primers containing adapters that add restriction sites for EcoRI/NdeI (5'end) and BamHI (3'end) were used to amplify full-length transcripts in RT-PCRs.…”

Section: Protein Interactions Between Lc-tra Lc-trab and Lc-tra2mentioning

confidence: 99%

“…It contains a number of distinctive domains of which the most conserved is the Ceratitis-Apis-Musca (CAM) domain, which is believed to implement the autoregulatory splicing loop of tra (Hediger et al, 2010). It has been found in all investigated tra orthologues, including those of Tribolium castaneum, Apis mellifera, Nasonia vitripennis, Asobara tabida and various dipterans, with the exception of drosophilids (Pane et al, 2005;Lagos et al, 2007;Ruiz et al, 2007;Hasselmann et al, 2008a;Hediger et al, 2010;Verhulst et al, 2010b;Saccone et al, 2011;Shukla and Palli, 2012;Geuverink et al, 2018). TRA also possesses order-specific domains, one of which is only shared amongst the Diptera (the DIP domain) and another that is only present in the Hymenoptera (the HYM domain) (Verhulst et al, 2010b).…”

Section: Introductionmentioning

confidence: 99%

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Evidence for involvement of atransformerparalogue in sex determination of the waspLeptopilina clavipes

Geuverink

Kraaijeveld

Leussen

et al. 2018

Insect Molecular Biology

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Transformer (tra) is the central gear in many insect sex determination pathways and transduces a wide range of primary signals. Mediated by transformer-2 (tra2) it directs sexual development into the female or male mode. Duplications of tra have been detected in numerous Hymenoptera, but a function in sex determination has been confirmed only in Apis mellifera. We identified a tra2 orthologue (Lc-tra2), a tra orthologue (Lc-tra) and a tra paralogue (Lc-traB) in the genome of Leptopilina clavipes (Hymenoptera: Cynipidae). We compared the sequence and structural conservation of these genes between sexual (arrhenotokous) and asexual all-female producing (thelytokous) individuals. Lc-tra is sex-specifically spliced in adults consistent with its orthologous function. The male-specific regions of Lc-tra are conserved in both reproductive modes. The paralogue Lc-traB lacks the genomic region coding for male-specific exons and can only be translated into a full-length TRA-like peptide sequence. Furthermore, unlike LC-TRA, the LC-TRAB interstrain sequence variation is not differentiated into a sexual and an asexual haplotype. The LC-TRAB protein interacts with LC-TRA as well as LC-TRA2. This suggests that Lc-traB functions as a conserved element in sex determination of sexual and asexual individuals.

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“…We also detected the maternally contributed Btau-traF mRNA (unpublished data). The maternally contributed tra2 transcripts have been detected in many insect species and appear to be required for initiation of female development (Geuverink et al, 2017(Geuverink et al, , 2018. In Ce.…”

Section: Btau-tra2 Produced Three Transcript Variancesmentioning

confidence: 99%

The transformer2 gene of the pumpkin fruit fly, Bactrocera tau (Walker), functions in sex determination, male fertility and testis development

Thongsaiklaing

Nipitwattanaphon

Ngernsiri

2018

Insect Molecular Biology

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The insect transformer2 (tra2) gene has a prevalent role in cooperating with the sex-determining gene transformer (tra) to direct female differentiation. Here, we report the identification and characterization of Btau-tra2, the tra2 orthologue of the pumpkin fruit fly, Bactrocera tau, an invasive agricultural pest. The Btau-tra2 gene produces three transcript variants. However, only two transcripts can be examined; one is present at all developmental stages in the soma and germline of both sexes and the other one is specific to the embryo and the germline. Knocking down the function of Btau-tra2 produced a male-biased sex ratio and some intersexes. Consistent with a role in sex determination, the obtained intersexual and male sterility phenotypes express a mix of male and female splice variants of the tra and doublesex (dsx) orthologues, indicating that Btau-tra2 has a conserved splicing regulatory function and acts together with/upstream of tra and dsx. In addition, some males obtained from the knock down are fertile but their fertilities are extremely reduced. Moreover, almost all surviving RNA interference (RNAi) males harbour testes having some defects in their external morphologies. Most notably, the body size of a few surviving RNAi flies was two-to threefold increased with respect to the normal size. Our findings suggest that Btau-tra2 is involved in male fertility and may also have an unprecedented role in body size control besides its conserved role in sex determination.

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Maternal provision of non‐sex‐specific transformer messenger RNA in sex determination of the wasp Asobara tabida

Cited by 12 publications

References 45 publications

Increased fluctuation in a butterfly metapopulation leads to diploid males and decline of a hyperparasitoid

Increased fluctuation in a butterfly metapopulation leads to diploid males and decline of a hyperparasitoid

Evidence for involvement of atransformerparalogue in sex determination of the waspLeptopilina clavipes

The transformer2 gene of the pumpkin fruit fly, Bactrocera tau (Walker), functions in sex determination, male fertility and testis development

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