Biology subjects

Gotoh, H.

Publications and source records attributed to Gotoh, H..

8 recordsLinked to original sources

bioRxiv2024

Conserved interhemispheric morphogenesis in amniotes preceded the evolution of the corpus callosum

The corpus callosum (CC) is the large axon bundle connecting the telencephalic hemispheres. The CC is formed exclusively in placental mammals, and the lack of comparable structures in other amniotes obscures the evolutionary origin of the CC. We here demonstrate that interhemispheric remodeling, a prior developmental step for CC formation, is highly conserved in non-mammalian amniotes, such as reptiles and birds. In these animal groups, the spatiotemporal dynamics of interhemispheric remodeling are tightly connected with distinct commissural formations. We observed a high degree of similarity between the mammalian CC and reptilian rostral pallial commissure, (RPC) and significant modifications in the avian pallial projection. Furthermore, we determined that Satb2 plays crucial roles in interhemispheric remodeling, which is associated with proper formation of both the CC and RPC in mice and geckoes, via the use of CRISPR-mediated gene-targeting. Our findings suggest that developmental mechanisms for midline remodeling were already present in the common ancestor of amniotes, which contributed to the evolution of eutherian-specific CC formation.

developmental biology↗

bioRxiv2023

A Neanderthal/Denisovan GLI3 variant contributes to anatomical variations in mice

Changes in genomic structures underlie phenotypic diversification in organisms. Amino acid-changing mutations affect pleiotropic functions of proteins, although little is known about how mutated proteins are adapted in existing developmental programs. Here we investigate the biological effects of a variant of the GLI3 transcription factor (GLI3R1537C) carried in Neanderthals and Denisovans, which are extinct hominins close to modern humans. R1537C does not compromise protein stability or GLI3 activator-dependent transcriptional activities. In contrast, R1537C affects the regulation of downstream target genes associated with developmental processes. Furthermore, genome-edited mice carrying the Neanderthal/Denisovan GLI3 mutation exhibited various alterations in skeletal morphology. Our data suggest that an extinct hominin-type GLI3 contributes to species-specific anatomical variations, which were tolerated by relaxed constraint in developmental programs during human evolution.

evolutionary biology↗

bioRxiv2023

Evolution of horn length and lifting strength in the Japanese rhinoceros beetle Trypoxylus dichotomus

Rhinoceros beetle (Trypoxylus dichotomus) males have pitchfork-shaped head horns, which they use to pry rival males from the trunks of trees. In the largest males these horns can be three times the length of horns in the two closest sister species. Because this weapon functions as a lever, longer horns should lift with less force than shorter horns (the paradox of the weakening combatant) unless other elements of the weapon system (e.g., input lever length, muscle mass) evolve to compensate. We used next-generation sequencing approaches to consolidate 23 sample locations into 8 genetically distinguishable populations, reconstructing their historical relationships and providing a comprehensive picture of the evolution of this horn lever system. We show that head horns likely increased in length independently in the Northern and Southern lineages. In both instances this resulted in weaker lifting forces, but this mechanical disadvantage was later ameliorated, to some extent and in some locations, by subsequent reductions to horn length, changes in muscle size, or by an increase in input lever length (head height). Our results reveal an exciting geographic mosaic of differences in weapon size, weapon force, and in the extent and nature of mechanical compensation. Reconstructing the evolution of this weapon system offers critical insights towards meaningfully linking mating system dynamics, selection patterns, and diversity in sexually selected traits.

evolutionary biology↗

bioRxiv2023

Mechanical models affecting beetle horn remodeling

Clarifying the mechanisms of shape alteration by insect metamorphosis is important for comprehending exoskeletal morphogenesis. The large horn of the Japanese rhinoceros beetle Trypoxylus dichotomus is the result of drastic metamorphosis, wherein it appears as a rounded shape via pupation and then undergoes remodeling into an angular adult shape. However, the mechanical mechanisms of this remodeling process remain unknown. In this study, we investigated the remodeling mechanisms of the Japanese rhinoceros beetle horn by developing a physical simulation. We identified three factors contributing to remodeling by biological experiments--ventral adhesion, uneven shrinkage, and volume reduction--which were demonstrated to be crucial to the transformation by a physical simulation. We also corroborated our findings by applying the simulation to the stag beetles mandibular remodeling. These results indicate that the physical simulation is applicable to pupal remodeling in other beetles, and the morphogenic mechanisms could explain various exoskeletal shapes. Significance statementThe metamorphosis in insects is a mysterious process. By metamorphosis, insects sometimes change their shape dramatically. The head horn of the Japanese rhinoceros beetle is one of the most famous examples of metamorphosis. In larva-to-pupa molting, the horn appears suddenly, caused by the "furrow formation and unfolding" mechanism. The unfolding process makes the pupal horn rounded. However, pupa-to-adult molting transforms the rounded shape into an angular shape. In this paper, we investigated the mechanisms of the transformation. We extracted factors contributing to it through observations and experiments and developed a physical simulation. It could reproduce the adult shape from the pupal shape and could be a general model for the pupa-adult transformation of beetles.

developmental biology↗

bioRxiv2022

The draft genome sequence of Japanese rhinoceros beetle 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.

genomics↗

bioRxiv2021

Genomic and transcriptomic analyses of the subterranean termite Reticulitermes speratus: gene duplication facilitates social evolution

Termites are model social organisms characterized by a polyphenic caste system. Subterranean termites (Rhinotermitidae) are ecologically and economically important species, including acting as destructive pests. Rhinotermitidae occupies an important evolutionary position within the clade representing an intermediate taxon between the higher (Termitidae) and lower (other families) termites. Here, we report the genome, transcriptome and methylome of the Japanese subterranean termite Reticulitermes speratus. The analyses highlight the significance of gene duplication in social evolution in this termite. Gene duplication associated with caste-biased gene expression is prevalent in the R. speratus genome. Such duplicated genes encompass diverse categories related to social functions, including lipocalins (chemical communication), cellulases (wood digestion and social interaction), lysozymes (social immunity), geranylgeranyl diphosphate synthase (social defense) and a novel class of termite lineage-specific genes with unknown functions. Paralogous genes were often observed in tandem in the genome, but the expression patterns were highly variable, exhibiting caste biases. Some duplicated genes assayed were expressed in caste-specific organs, such as the accessory glands of the queen ovary and frontal glands in soldier heads. We propose that gene duplication facilitates social evolution through regulatory diversification leading to caste-biased expression and subfunctionalization and/or neofunctionalization that confers caste-specialized functions. Significance StatementTermites are model social organisms characterized by a sophisticated caste system, where distinct castes arise from the same genome. Our genomics data of Japanese subterranean termite provides insights into the evolution of the social system, highlighting the significance of gene duplication. Gene duplication associated with caste-biased gene expression is prevalent in the termite genome. Many of the duplicated genes were related to social functions, such as chemical communication, social immunity and defense, and they often expressed in caste-specific organs. We propose that gene duplication facilitates social evolution through regulatory diversification leading to caste-biased expression and functional specialization. In addition, since subterranean termites are ecologically and economically important species including destructive pests in the world, our genomics data serves as a foundation for these studies.

genomics↗

bioRxiv2021

Evolutionary transition of doublesex regulation in termites and cockroaches: from sex-specific splicing to male-specific transcription

The sex determination gene doublesex (dsx), which encodes a transcription factor with two domains: oligomerisation domain 1 (OD1) and OD2, is conserved among insects. The sex-specific Dsx splicing isoforms regulate the transcription of target genes and trigger sex differentiation in all holometabolous insects examined to date. However, in some hemimetabolous insects, dsx is less conserved and not spliced sexually. Here, to elucidate evolutionary changes in dsx in the gene structure and its regulatory manner in termites, we searched genome and/or transcriptome databases for the OD1 and OD2 of dsx in six termite species and their sister group (woodroach). Molecular phylogenetic analysis identified OD1 sequences of termites and a woodroach clustered with dsx of holometabolous insects and regarded them as dsx orthologues. In the woodroach, a dsx orthologue containing OD2 was spliced sexually, as previously shown in other insects. However, OD2 were not found in all termite dsx orthologues. These orthologues were encoded by only a single exon in three termites with genome information; they were not alternatively spliced, but transcribed in a male-specific manner in two species examined. Evolution of dsx regulation from sex-specific splicing to male-specific transcription might be occurred at the early stage of social evolution in termites.

evolutionary biology↗

bioRxiv2020

Genetical control of 2D pattern and depth of the primordial furrow that codes 3D shape of the rhinoceros beetle horn

The head horn of the Asian rhinoceros beetle develops as extensively folded primordia before unfurling into its final 3D shape at the pupal molt. The information of the final 3D structure of the beetle horn is encoded in the folding pattern of the developing primordia. However, the developmental mechanism underlying epithelial folding of the primordia is unknown. In this study, we addressed this gap in our understanding of the developmental patterning of the 3D horn shape of beetles by focusing on the formation of surficial furrows that become the bifurcated 3D shape of the horn. By gene knockdown screening via RNAi, we found that knockdown of the gene Notch disturbed overall horn primordia furrow depth without affecting 2D furrow pattern. In contrast, knockdown of CyclinE altered 2D horn primordia furrow pattern without affecting furrow depth. From these results, depth and 2D pattern of primordial surficial furrow are likely to be regulated independently during the development and both of change can alter the final 3D shape. Author SummaryIn insects, some large structure is made under the old exoskeleton before the molting. Long horn of rhino-beetle is one of extreme cases. The beetle horn is compactly packed as furrowed primordia under the larval exoskeleton. At molting, the primordia is extended to form its final 3D horn shape as blowing up furrows like a balloon. This transformation from primordia to final horn does not required any living cell activities. Thus, characteristics of furrows of primordia actually determine the final 3D shape. However, molecular mechanisms and genetic basis of furrow formation is not well understood not only in beetle horn but also in any other insects. In this study, by using beetle horn as a model, we addressed what kind of genetic factors are contributed to primordial furrow formation. By gene knockdown screening, we found that knockdown of the gene Notch disturbed primordial furrow depth without affecting 2D furrow pattern. In contrast, knockdown of CyclinE altered 2D furrow pattern without affecting furrow depth. In both case, final horn shapes were disturbed. From these results, we concluded that both of the depth and 2D pattern of primordial furrow can contribute final shape, but their development is controlled independently.

developmental biology↗