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Distinct developmental mechanisms influence sexual dimorphisms in the milkweed bug Oncopeltus fasciatus.

ABSTRACT: Sexual dimorphism is common in animals. The most complete model of sex determination comes from Drosophila melanogaster, where the relative dosage of autosomes and X chromosomes leads indirectly to sex-specific transcripts of doublesex (dsx). Female Dsx interacts with a mediator complex protein encoded by intersex (ix) to activate female development. In males, the transcription factor encoded by fruitless (fru) promotes male-specific behaviour. The genetics of sex determination have been examined in a small number of other insects, yet several questions remain about the plesiomorphic state. Is dsx required for female and male development? Is fru conserved in male behaviour or morphology? Are other components such as ix functionally conserved? To address these questions, we report expression and functional tests of dsx, ix and fru in the hemipteran Oncopeltus fasciatus, characterizing three sexual dimorphisms. dsx prevents ix phenotypes in all sexes and dimorphic traits in the milkweed bug. ix and fru are expressed across the body, in females and males. fru and ix also affect the genitalia of both sexes, but have effects limited to different dimorphic structures in different sexes. These results reveal roles for ix and fru distinct from other insects, and demonstrate distinct development mechanisms in different sexually dimorphic structures.

SUBMITTER: Just J

PROVIDER: S-EPMC9890105 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Distinct developmental mechanisms influence sexual dimorphisms in the milkweed bug Oncopeltus fasciatus.

Just Josefine J Laslo Mara M Lee Ye Jin YJ Yarnell Michael M Zhang Zhuofan Z Angelini David R DR

Proceedings. Biological sciences 20230201 1992

Sexual dimorphism is common in animals. The most complete model of sex determination comes from Drosophila melanogaster, where the relative dosage of autosomes and X chromosomes leads indirectly to sex-specific transcripts of doublesex (dsx). Female Dsx interacts with a mediator complex protein encoded by intersex (ix) to activate female development. In males, the transcription factor encoded by fruitless (fru) promotes male-specific behaviour. Th ...[more]

PMID: 36722087

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Project description:BackgroundMost evolutionary developmental biology ("evo-devo") studies of emerging model organisms focus on small numbers of candidate genes cloned individually using degenerate PCR. However, newly available sequencing technologies such as 454 pyrosequencing have recently begun to allow for massive gene discovery in animals without sequenced genomes. Within insects, although large volumes of sequence data are available for holometabolous insects, developmental studies of basally branching hemimetabolous insects typically suffer from low rates of gene discovery.ResultsWe used 454 pyrosequencing to sequence over 500 million bases of cDNA from the ovaries and embryos of the milkweed bug Oncopeltus fasciatus, which lacks a sequenced genome. This indirectly developing insect occupies an important phylogenetic position, branching basal to Diptera (including fruit flies) and Hymenoptera (including honeybees), and is an experimentally tractable model for short-germ development. 2,087,410 reads from both normalized and non-normalized cDNA assembled into 21,097 sequences (isotigs) and 112,531 singletons. The assembled sequences fell into 16,617 unique gene models, and included predictions of splicing isoforms, which we examined experimentally. Discovery of new genes plateaued after assembly of ~1.5 million reads, suggesting that we have sequenced nearly all transcripts present in the cDNA sampled. Many transcripts have been assembled at close to full length, and there is a net gain of sequence data for over half of the pre-existing O. fasciatus accessions for developmental genes in GenBank. We identified 10,775 unique genes, including members of all major conserved metazoan signaling pathways and genes involved in several major categories of early developmental processes. We also specifically address the effects of cDNA normalization on gene discovery in de novo transcriptome analyses.ConclusionsOur sequencing, assembly and annotation framework provide a simple and effective way to achieve high-throughput gene discovery for organisms lacking a sequenced genome. These data will have applications to the study of the evolution of arthropod genes and genetic pathways, and to the wider evolution, development and genomics communities working with emerging model organisms.[The sequence data from this study have been submitted to GenBank under study accession number SRP002610 (http://www.ncbi.nlm.nih.gov/sra?term=SRP002610). Custom scripts generated are available at http://www.extavourlab.com/protocols/index.html. Seven Additional files are available.].

Project description:Regional populations of geographically widespread species may respond to different environmental factors across the species' range, generating divergent effects of climate change on life-history phenology. Using thousands of citizen science observations extracted from iNaturalist and associated with corresponding temperature, precipitation, elevation, and daylength information, we examined the drivers of adult mating and of nymphal phenology, development, and group size for populations of the large milkweed bug, Oncopeltus fasciatus, in different ecoregions. Research-grade iNaturalist images were correctly identified 98.3% of the time and yielded more than 3000 observations of nymphal groups and 1000 observations of mating adults spanning 18 years. Mating phenology showed distinct regional patterns, ranging from year-round mating in California to temporally restricted mating in the Great Lakes Northeastern Coast ecoregion. Relative temperature increases of 1°C for a given daylength expanded the mating season by more than a week in western ecoregions. While increases in relative temperature delayed mating phenology in all ecoregions, greater winter precipitation advanced mating in the California ecoregion. In the eastern ecoregions, nymphal phenology was delayed by increases in summer rainfall but was advanced by relative temperature increases, whereas in western regions, relative temperature increases delayed nymphal phenology. Furthermore, accumulated growing degree days (AGDD) was a poor predictor of developmental progression, as we found a positive but weak correlation between AGDD and age structure only for the Appalachian Southeast North America and the Great Lakes Northern Coast ecoregions. These complex phenological responses of O. fasciatus are just one example of how populations may be differentially susceptible to a diversity of climatic effects; using data across a species' whole distribution is critical for exposing regional variations, especially for species with large, continental-scale ranges. This study demonstrates the potential of photodocumented biodiversity data to aid in the monitoring of life history, host plant-insect interactions, and climate responsiveness.

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Distinct developmental mechanisms influence sexual dimorphisms in the milkweed bug Oncopeltus fasciatus.

Publications

Distinct developmental mechanisms influence sexual dimorphisms in the milkweed bug <i>Oncopeltus fasciatus</i>.

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