The Evolution of Sexual Development in Arthropods

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Animal Genetics and Genomics".

Deadline for manuscript submissions: closed (20 April 2021) | Viewed by 20433

Special Issue Editors


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Guest Editor
Department of Evolution and Ecology, University of California—Davis, One Shields Avenue, Davis, CA 95616, USA
Interests: evolutionary innovations; sexual dimorphism; insect development and evolution; evolutionary genetics; convergent evolution

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Guest Editor
Department of Biology, University Federico II of Naples, 80126 Naples, Italy
Interests: sex determination; evolution of genes and of developmental pathways; insect pests and biotechnology

Special Issue Information

Dear Colleagues,

The genetic control of insect sexual development, first uncovered in Drosophila, is now beginning to be elucidated in other, distantly related lineages. Investigations in a number of insect orders have shown that sexual differentiation is based on a deeply conserved regulatory module that functions via sex-specific alternative splicing of three genes: transformer, doublesex, and fruitless. However, this module responds to different upstream sex determination signals, controls different target genes, and generates different sex-specific traits in different insect species. Research in non-insect arthropods suggests that the splicing-based mechanism of sexual differentiation may be unique to insects, and that other arthropod groups rely on different mechanisms. These observations raise a number of evolutionary questions. Why is there such a diversity of sex determining primary signals? How did the insect sexual differentiation pathway evolve? What are the key features of sexual development in non-insect arthropods? What genes act during metamorphosis to produce sexually dimorphic traits? Is insect sex determination fully cell-autonomous, or do systemic signals play a role as well? What neural substrates are responsible for sex-specific behaviour? What evolutionary forces shape the diversity of sex-specific traits? Experts in the fields of arthropod development and evolution are invited to contribute original articles, reviews, and hypothesis papers to this special issue.

Prof. Dr. Artyom Kopp
Dr. Giuseppe Saccone
Guest Editors

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Keywords

  • drosophila
  • insects
  • arthropoda
  • sexual development and differentiation
  • evolutionary genetics
  • comparative genomics

Published Papers (5 papers)

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Research

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14 pages, 3653 KiB  
Article
Pleiotropic Roles of the Orthologue of the Drosophila melanogaster Intersex Gene in the Brown Planthopper
by Hou-Hong Zhang, Yu-Cheng Xie, Han-Jing Li, Ji-Chong Zhuo and Chuan-Xi Zhang
Genes 2021, 12(3), 379; https://doi.org/10.3390/genes12030379 - 7 Mar 2021
Cited by 6 | Viewed by 2299
Abstract
Intersex(ix), a gene involved in the sex-determining cascade of Drosophila melanogaster, works in concert with the female-specific product of doublesex (dsx) at the end of the hierarchy to implement the sex-specific differentiation of sexually dimorphic characters in [...] Read more.
Intersex(ix), a gene involved in the sex-determining cascade of Drosophila melanogaster, works in concert with the female-specific product of doublesex (dsx) at the end of the hierarchy to implement the sex-specific differentiation of sexually dimorphic characters in female individuals. In this study, the ix homolog was identified in the brown planthopper (BPH), Nilaparvata lugens, which contained two splice variants expressed in both female and male insects. We found that Nlix played a vital role in the early nymphal development of BPH, showing an accumulated effect. RNAi-mediated knockdown of Nlix at 4th instar led to the external genital defects in both sexes, consequently resulting in the loss of reproductive ability in female and male individuals. After dsRNA injection, the males were normal on testes, while the females had defective ovarian development. Nlix was also required for early embryogenesis. Notably, when the dsNlix microinjection was performed in newly emerged females, the copulatory bursas were abnormally enlarged while the other tissues of the reproductive system developed normally. Our results demonstrated the pleiotropic roles of Nlix in embryogenesis and development of the reproductive system in a hemimetabolous insect species. Full article
(This article belongs to the Special Issue The Evolution of Sexual Development in Arthropods)
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13 pages, 2885 KiB  
Article
Bracon brevicornis Genome Showcases the Potential of Linked-Read Sequencing in Identifying a Putative Complementary Sex Determiner Gene
by Kim B. Ferguson, Bart A. Pannebakker, Alejandra Centurión, Joost van den Heuvel, Ronald Nieuwenhuis, Frank F. M. Becker, Elio Schijlen, Andra Thiel, Bas J. Zwaan and Eveline C. Verhulst
Genes 2020, 11(12), 1390; https://doi.org/10.3390/genes11121390 - 24 Nov 2020
Cited by 2 | Viewed by 3063
Abstract
Bracon brevicornis is an ectoparasitoid of a wide range of larval-stage Lepidopterans, including several pests of important crops, such as the corn borer, Ostrinia nubilalis. It is also one of the earliest documented cases of complementary sex determination in Hymenoptera. Here, we [...] Read more.
Bracon brevicornis is an ectoparasitoid of a wide range of larval-stage Lepidopterans, including several pests of important crops, such as the corn borer, Ostrinia nubilalis. It is also one of the earliest documented cases of complementary sex determination in Hymenoptera. Here, we present the linked-read-based genome of B. brevicornis, complete with an ab initio-derived annotation and protein comparisons with fellow braconids, Fopius arisanus and Diachasma alloeum. We demonstrate the potential of linked-read assemblies in exploring regions of heterozygosity and search for structural and homology-derived evidence of the complementary sex determiner gene (csd). Full article
(This article belongs to the Special Issue The Evolution of Sexual Development in Arthropods)
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17 pages, 2060 KiB  
Article
Multi-Tissue Transcriptome Analysis Identifies Key Sexual Development-Related Genes of the Ornate Spiny Lobster (Panulirus ornatus)
by Tomer Ventura, Jennifer C. Chandler, Tuan V. Nguyen, Cameron J. Hyde, Abigail Elizur, Quinn P. Fitzgibbon and Gregory G. Smith
Genes 2020, 11(10), 1150; https://doi.org/10.3390/genes11101150 - 29 Sep 2020
Cited by 23 | Viewed by 3890
Abstract
Sexual development involves the successive and overlapping processes of sex determination, sexual differentiation, and ultimately sexual maturation, enabling animals to reproduce. This provides a mechanism for enriched genetic variation which enables populations to withstand ever-changing environments, selecting for adapted individuals and driving speciation. [...] Read more.
Sexual development involves the successive and overlapping processes of sex determination, sexual differentiation, and ultimately sexual maturation, enabling animals to reproduce. This provides a mechanism for enriched genetic variation which enables populations to withstand ever-changing environments, selecting for adapted individuals and driving speciation. The molecular mechanisms of sexual development display a bewildering diversity, even in closely related taxa. Many sex determination mechanisms across animals include the key family of “doublesex- and male abnormal3-related transcription factors” (Dmrts). In a few exceptional species, a single Dmrt residing on a sex chromosome acts as the master sex regulator. In this study, we provide compelling evidence for this model of sex determination in the ornate spiny lobster Panulius ornatus, concurrent with recent reports in the eastern spiny lobster Sagmariasus verreauxi. Using a multi-tissue transcriptomic database established for P. ornatus, we screened for the key factors associated with sexual development (by homology search and using previous knowledge of these factors from related species), providing an in-depth understanding of sexual development in decapods. Further research has the potential to close significant gaps in our understanding of reproductive development in this ecologically and commercially significant order. Full article
(This article belongs to the Special Issue The Evolution of Sexual Development in Arthropods)
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Review

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11 pages, 1412 KiB  
Review
The Sex Determination Cascade in the Silkworm
by Xu Yang, Kai Chen, Yaohui Wang, Dehong Yang and Yongping Huang
Genes 2021, 12(2), 315; https://doi.org/10.3390/genes12020315 (registering DOI) - 23 Feb 2021
Cited by 16 | Viewed by 4655
Abstract
In insects, sex determination pathways involve three levels of master regulators: primary signals, which determine the sex; executors, which control sex-specific differentiation of tissues and organs; and transducers, which link the primary signals to the executors. The primary signals differ widely among insect [...] Read more.
In insects, sex determination pathways involve three levels of master regulators: primary signals, which determine the sex; executors, which control sex-specific differentiation of tissues and organs; and transducers, which link the primary signals to the executors. The primary signals differ widely among insect species. In Diptera alone, several unrelated primary sex determiners have been identified. However, the doublesex (dsx) gene is highly conserved as the executor component across multiple insect orders. The transducer level shows an intermediate level of conservation. In many, but not all examined insects, a key transducer role is performed by transformer (tra), which controls sex-specific splicing of dsx. In Lepidoptera, studies of sex determination have focused on the lepidopteran model species Bombyx mori (the silkworm). In B. mori, the primary signal of sex determination cascade starts from Fem, a female-specific PIWI-interacting RNA, and its targeting gene Masc, which is apparently specific to and conserved among Lepidoptera. Tra has not been found in Lepidoptera. Instead, the B. mori PSI protein binds directly to dsx pre-mRNA and regulates its alternative splicing to produce male- and female-specific transcripts. Despite this basic understanding of the molecular mechanisms underlying sex determination, the links among the primary signals, transducers and executors remain largely unknown in Lepidoptera. In this review, we focus on the latest findings regarding the functions and working mechanisms of genes involved in feminization and masculinization in Lepidoptera and discuss directions for future research of sex determination in the silkworm. Full article
(This article belongs to the Special Issue The Evolution of Sexual Development in Arthropods)
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16 pages, 1550 KiB  
Review
Sex Determination and Differentiation in Decapod and Cladoceran Crustaceans: An Overview of Endocrine Regulation
by Kenji Toyota, Hitoshi Miyakawa, Chizue Hiruta, Tomomi Sato, Hidekazu Katayama, Tsuyoshi Ohira and Taisen Iguchi
Genes 2021, 12(2), 305; https://doi.org/10.3390/genes12020305 - 21 Feb 2021
Cited by 30 | Viewed by 5536
Abstract
Mechanisms underlying sex determination and differentiation in animals are known to encompass a diverse array of molecular clues. Recent innovations in high-throughput sequencing and mass spectrometry technologies have been widely applied in non-model organisms without reference genomes. Crustaceans are no exception. They are [...] Read more.
Mechanisms underlying sex determination and differentiation in animals are known to encompass a diverse array of molecular clues. Recent innovations in high-throughput sequencing and mass spectrometry technologies have been widely applied in non-model organisms without reference genomes. Crustaceans are no exception. They are particularly diverse among the Arthropoda and contain a wide variety of commercially important fishery species such as shrimps, lobsters and crabs (Order Decapoda), and keystone species of aquatic ecosystems such as water fleas (Order Branchiopoda). In terms of decapod sex determination and differentiation, previous approaches have attempted to elucidate their molecular components, to establish mono-sex breeding technology. Here, we overview reports describing the physiological functions of sex hormones regulating masculinization and feminization, and gene discovery by transcriptomics in decapod species. Moreover, this review summarizes the recent progresses of studies on the juvenile hormone-driven sex determination system of the branchiopod genus Daphnia, and then compares sex determination and endocrine systems between decapods and branchiopods. This review provides not only substantial insights for aquaculture research, but also the opportunity to re-organize the current and future trends of this field. Full article
(This article belongs to the Special Issue The Evolution of Sexual Development in Arthropods)
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