doublesex regulates sexually dimorphic beetle horn formation by integrating spatial and temporal developmental contexts in the Japanese rhinoceros beetle Trypoxylus dichotomus

Abstract:Many scarab beetles have sexually dimorphic exaggerated horns that are an evolutionary novelty. Since the shape, number, size, and location of horns are highly diverged within Scarabaeidae, beetle horns are an attractive model for studying the evolution of sexually dimorphic and novel traits. In beetles including the Japanese rhinoceros beetle Trypoxylus dichotomus, the sex determination gene doublesex (dsx) plays a crucial role in sexually dimorphic horn formation during larval-pupal development. However, knowledge of when and how dsx drives the gene regulatory network (GRN) for horn formation to form sexually dimorphic horns during development remains elusive. To address this issue, we identified a Trypoxylus-ortholog of the sex determination gene, transformer (tra), that regulates sex-specific splicing of the dsx pre-mRNA, and whose loss of function results in sex transformation. By knocking down tra function at multiple developmental timepoints during larval-pupal development, we estimated the onset when the sex-specific GRN for horn formation is driven. In addition, we also revealed that dsx regulates different aspects of morphogenetic activities during the prepupal and pupal developmental stages to form appropriate morphologies of pupal head and thoracic horn primordia as well as those of adult horns. Based on these findings, we discuss the evolutionary developmental background of sexually dimorphic trait growth in horned beetles.Author Summary:Beetle horns are highly enriched in a particular family Scarabaeidae, although the shape, size and number of horns are diversified within the group. In addition, many scarab beetle horns are sexually dimorphic. It has been questioned how a particular group of beetles has originated and diversified evolutionary novel horns. Here we found the exact time when morphological sexual dimorphism of horn primordia appeared, estimated the onset of the developmental program for sexually dimorphic horn formation driven by Doublesex, and revealed that Doublesex regulates different aspects of cell activities of horn primordia depending on the spatiotemporal contexts. Our study provides our understanding regarding regulatory shifts in these mechanisms during the evolution of sexually dimorphic traits in horned beetles.

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The draft genome sequence of Japanese rhinoceros beetle Trypoxylus dichotomus

10.1101/2022.01.10.475740 ◽

2022 ◽

Author(s):

Shinichi Morita ◽

Tomoko F. Shibata ◽

Tomoaki Nishiyama ◽

Yuuki Kobayashi ◽

Katsushi Yamaguchi ◽

...

Keyword(s):

De Novo Assembly ◽

Molecular Mechanisms ◽

Developmental Stages ◽

De Novo ◽

Genetic Regulation ◽

Draft Genome ◽

Evolutionary Developmental Biology ◽

Rhinoceros Beetle ◽

Insect Order ◽

Trypoxylus Dichotomus

Beetles are the largest insect order and one of the most successful animal groups in terms of number of species. The Japanese rhinoceros beetle Trypoxylus dichotomus (Coleoptera, Scarabaeidae, Dynastini) is a giant beetle with distinctive exaggerated horns present on the head and prothoracic regions of the male. T. dichotomus has been used as research model in various fields such as evolutionary developmental biology, ecology, ethology, biomimetics, and drug discovery. In this study, de novo assembly of 615 Mb, representing 80% of the genome estimated by flow cytometry, was obtained using the 10x Chromium platform. The scaffold N50 length of the genome assembly was 8.02 Mb, with repetitive elements predicted to comprise 49.5% of the assembly. In total, 23,987 protein-coding genes were predicted in the genome. In addition, de novo assembly of the mitochondrial genome yielded a contig of 20,217 bp. We also analyzed the transcriptome by generating 16 RNA-seq libraries from a variety of tissues of both sexes and developmental stages, which allowed us to identify 13 co-expressed gene modules. The detailed genomic and transcriptomic information of T. dichotomus is the most comprehensive among those reported for any species of Dynastinae. This genomic information will be an excellent resource for further functional and evolutionary analyses, including the evolutionary origin and genetic regulation of beetle horns and the molecular mechanisms underlying sexual dimorphism.

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Identification, Expression and Evolution of Short-Chain Dehydrogenases/Reductases in Nile Tilapia (Oreochromis niloticus)

International Journal of Molecular Sciences ◽

10.3390/ijms22084201 ◽

2021 ◽

Vol 22 (8) ◽

pp. 4201

Author(s):

Shuai Zhang ◽

Lang Xie ◽

Shuqing Zheng ◽

Baoyue Lu ◽

Wenjing Tao ◽

...

Keyword(s):

Transcriptome Analysis ◽

Tandem Duplication ◽

Developmental Stages ◽

Short Chain ◽

Sexually Dimorphic ◽

Physiological Processes ◽

Genome Wide ◽

Nile Tilapia Oreochromis Niloticus ◽

Tandem Duplications

The short-chain dehydrogenases/reductases (SDR) superfamily is involved in multiple physiological processes. In this study, genome-wide identification and comprehensive analysis of SDR superfamily were carried out in 29 animal species based on the latest genome databases. Overall, the number of SDR genes in animals increased with whole genome duplication (WGD), suggesting the expansion of SDRs during evolution, especially in 3R-WGD and polyploidization of teleosts. Phylogenetic analysis indicated that vertebrates SDRs were clustered into five categories: classical, extended, undefined, atypical, and complex. Moreover, tandem duplication of hpgd-a, rdh8b and dhrs13 was observed in teleosts analyzed. Additionally, tandem duplications of dhrs11-a, dhrs7a, hsd11b1b, and cbr1-a were observed in all cichlids analyzed, and tandem duplication of rdh10-b was observed in tilapiines. Transcriptome analysis of adult fish revealed that 93 SDRs were expressed in more than one tissue and 5 in one tissue only. Transcriptome analysis of gonads from different developmental stages showed that expression of 17 SDRs were sexually dimorphic with 11 higher in ovary and 6 higher in testis. The sexually dimorphic expressions of these SDRs were confirmed by in situ hybridization (ISH) and qPCR, indicating their possible roles in steroidogenesis and gonadal differentiation. Taken together, the identification and the expression data obtained in this study contribute to a better understanding of SDR superfamily evolution and functions in teleosts.

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Phylogeny and biogeography of the Japanese rhinoceros beetle, Trypoxylus dichotomus (Coleoptera: Scarabaeidae) based on SNP markers

Ecology and Evolution ◽

10.1002/ece3.6982 ◽

2020 ◽

Author(s):

Huan Yang ◽

Chong Juan You ◽

Clement K. M. Tsui ◽

Luke R. Tembrock ◽

Zhi Qiang Wu ◽

...

Keyword(s):

Snp Markers ◽

Rhinoceros Beetle ◽

Trypoxylus Dichotomus

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16. Physiological effects of IDH1 loss-of-function on Chondrocyte Differentiation through Hedgehog Pathway upregulation

Inquiry@Queen's Undergraduate Research Conference Proceedings ◽

10.24908/iqurcp.9897 ◽

2018 ◽

Author(s):

Cassie Tyson

Keyword(s):

Developmental Stages ◽

Hedgehog Pathway ◽

Chondrocyte Differentiation ◽

Loss Of Function ◽

Wild Type ◽

Phenotypic Analysis ◽

Growth Plate Chondrocytes ◽

Idh Mutations ◽

Cartilage Tumors ◽

Deficient Mice

Cartilage tumors are the most common and terminal primary neoplasms in bone. Physiologically, bones formed through endochondral ossification are regulated by the Hedgehog pathway and Parathyroid hormone-like hormone feedback loop. The upregulation of the infamous Hedgehog pathway has been demonstrated in several non-cartilaginous neoplasms. Recently, frequent mutational events of isocitrate dehydrogenase1 (IDH1) were identified in cartilage tumors. In other neoplasms, IDH mutations produces an oncometabolite that can promote HIF1a activation, contributing to tumorigenesis. Currently, the role of IDH1 mutations in cartilage tumors remain unknown. Investigating the physiological aspect of IDH1proves useful in identifying novel therapeutic targets for cartilage tumors. IDH1 deficient and wild-type littermates, were harvested for forelimbs and hindlimbs at various developmental stages for phenotypic analysis via hematoxylin and eosin staining. Histological analysis demonstrated IDH1 homozygous deficient mice at embryonic stages exhibited dwarfism and an elongated layer of hypertrophic chondrocytes. This was verified via immunohistochemistry Type 10 Collagen staining and Quantitative PCR (qPCR) using the chondrocyte terminal differentiation marker Col10a1. Whole skeletons of IDH1 deficient mice were subjected to skeletal double staining which demonstrated delayed mineralization of underdeveloped IDH1 deficient mice contrasted with wild-type littermates. qPCR was performed to examine the status of chondrocyte differentiation through the Hedgehog pathway in cultured primarymouse growth plate chondrocytes. Interestingly, IDH1 deficient non-neoplastic cells revealed significant upregulation of Hedgehog target molecules in IDH1 deficient chondrocytes. As a result, the loss-offunction of IDH1 was identified as a potential impairment of chondrocyte differentiation and a factor towards chondrocyte tumorgenisis.

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Genetic characterization of ms (3) K81, a paternal effect gene of Drosophila melanogaster.

Genetics ◽

10.1093/genetics/140.1.219 ◽

1995 ◽

Vol 140 (1) ◽

pp. 219-229 ◽

Cited By ~ 3

Author(s):

G K Yasuda ◽

G Schubiger ◽

B T Wakimoto

Keyword(s):

Drosophila Melanogaster ◽

Developmental Stages ◽

Normal Function ◽

Loss Of Function ◽

Male Sterile ◽

Specific Product ◽

Paternal Effect ◽

Developmental Arrest ◽

Effect Gene

Abstract The vast majority of known male sterile mutants of Drosophila melanogaster fail to produce mature sperm or mate properly. The ms(3) K81(1) mutation is one of a rare class of male sterile mutations in which sterility is caused by developmental arrest after sperm entry into the egg. Previous studies showed that males homozygous for the K81(1) mutation produce progeny that arrest at either of two developmental stages. Most embryos arrest during early nuclear cycles, whereas the remainder are haploid embryos that arrest at a later stage. This description of the mutant phenotype was based on the analysis of a single allele isolated from a natural population. It was therefore unclear whether this unique paternal effect phenotype reflected the normal function of the gene. The genetic analysis and initial molecular characterization of five new K81 mutations are described here. Hemizygous conditions and heteroallelic combinations of the alleles were associated with male sterility caused by defects in embryogenesis. No other mutant phenotypes were observed. Thus, the K81 gene acted as a strict paternal effect gene. Moreover, the biphasic pattern of developmental arrest was common to all the alleles. These findings strongly suggested that the unusual embryonic phenotype caused by all five new alleles was due to loss of function of the K81+ gene. The K81 gene is therefore the first clear example of a strict paternal effect gene in Drosophila. Based on the embryonic lethal phenotypes, we suggest that the K81+ gene encodes a sperm-specific product that is essential for the male pronucleus to participate in the first few embryonic nuclear divisions.

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Human Sex Matters: Y-linked lysine demethylase 5D drives accelerated male osteogenic differentiation

10.1101/2021.11.10.468047 ◽

2021 ◽

Author(s):

Madlen Merten ◽

Johannes F.W. Greiner ◽

Tarek Niemann ◽

Meike Grosse Venhaus ◽

Daniel Kronenberg ◽

...

Keyword(s):

Osteogenic Differentiation ◽

Molecular Mechanisms ◽

Female Rats ◽

Sexually Dimorphic ◽

Loss Of Function ◽

Calvarial Bone ◽

Sexual Dimorphisms ◽

Increased Risk ◽

Elevated Expression ◽

Lysine Demethylase

Female sex is increasingly associated to a loss of bone mass during aging and an increased risk for fractures developing nonunion. Hormonal factors and cell-intrinsic mechanisms are suggested to drive these sexual dimorphisms, although underlying molecular mechanisms are still a matter of debate. Here, we observed a decreased capacity of calvarial bone recovery in female rats and a profound sexually dimorphic osteogenic differentiation human adult neural crest-derived stem cells (NCSCs). Next to an elevated expression of pro-osteogenic regulators, global trancriptomics revealed Lysine Demethylase 5D (KDM5D) to be highly upregulated in differentiating male NCSCs. Loss of function by siRNA or pharmacological inhibition of KDM5D significantly reduced the osteogenic differentiation capacity of male NCSCs. In summary, we demonstrate craniofacial osteogenic differentiation to be sexually dimorphic with the expression of KDM5D as a prerequisite for accelerated male osteogenic differentiation, emphasizing the analysis of sex-specific differences as a crucial parameter for treating bone defects.

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Cross-sexual Transfer

Developmental Plasticity and Evolution ◽

10.1093/oso/9780195122343.003.0021 ◽

2003 ◽

Author(s):

Mary Jane West-Eberhard

Keyword(s):

Sex Determination ◽

Sexually Dimorphic ◽

Male And Female ◽

Alternative Phenotypes ◽

Opposite Sex ◽

Critical Age ◽

Sexual Traits ◽

Discrete Traits ◽

Dimorphic Species ◽

Determination Mechanism

Distinctive male and female traits are perhaps the most familiar of all divergent specializations within species. In cross-sexual transfer, discrete traits that are expressed exclusively in one sex in an ancestral species appear in the opposite sex of descendants. An example is the expression of brood care by males in a lineage where ancestral females are the exclusive caretakers of the young, as in some voles (Thomas and Birney, 1979). Despite the prominence of sexual dimorphism and sex reversals in nature, and an early explicit treatment by Darwin, discussed in the next section, cross-sexual transfer is not often recognized as a major factor in the evolution of novelty (but see, on animals, Mayr, 1963, pp. 435-439; Mayr, 1970, p. 254; on plants, Iltis, 1983). When more widely investigated, cross-sexual transfer may prove to rival heterochrony and duplication as an important source of novelties in sexually dimorphic lineages. For this reason, I devote more attention here to cross-sexual transfer than to these other, well-established general patterns of change. The male and female of a sexually dimorphic species may be so different that it is easy to forget that each individual carries most or all of the genes necessary to produce the phenotype of the opposite sex. Sex determination, like caste determination and other switches between alternative phenotypes, depends on only a few genetic loci or, in many species, environmental factors (Bull, 1983). There is considerable flexibility in sex determination and facultative reversal in some taxa. Among fish, for example, there is even a species wherein sex is determined by juvenile size at a critical age (Francis and Barlow, 1993). The sex determination mechanism, whatever its nature, leads to a series of sex-limited responses, often coordinated by hormones and not necessarily all occurring at once. A distinguishing aspect of sexually dimorphic traits in adults is that there is often a close homology between the secondary sexual traits that are differently modified in the two sexes.

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