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Journal of experimental zoology. Part B, Molecular and developmental evolution
Feb 17, 2025;

Differential Expression of Hormone-Related Genes in the Heads of Adult and Nymphal Woodroaches (Cryptocercus).

Takumi Hanada, Hajime Yaguchi, Kokuto Fujiwara, Yoshinobu Hayashi, Christine A Nalepa, Kiyoto Maekawa
Author Information
  1. Takumi Hanada: Graduate School of Science and Engineering, University of Toyama, Toyama, Japan.
  2. Hajime Yaguchi: Department of Forest Entomology, Forestry and Forest Products Research Institute, Tsukuba, Japan.
  3. Kokuto Fujiwara: Graduate School of Science and Engineering, University of Toyama, Toyama, Japan.
  4. Yoshinobu Hayashi: Department of Biology, Keio University, Yokohama, Japan.
  5. Christine A Nalepa: Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, North Carolina, USA.
  6. Kiyoto Maekawa: University of Toyama, Toyama, Japan. ORCID
PMID: 39959923 DOI: 10.1002/jez.b.23290

Abstract

Termites are eusocial cockroaches, but the crucial distinctions in gene expression during the evolution of eusociality remain unclear. One reason for the lack of this information is that comparative transcriptome analysis of termites with their sister group, the cockroach genus Cryptocercus, has not been conducted. We identified genes associated with three vital hormones (juvenile hormone [JH], 20-hydoroxyecdysone [20E], and insulin) from the genome sequence of Cryptocercus punctulatus and conducted RNA-seq analysis using the heads of female/male adults and nymphs to elucidate their expression levels. The comprehensive gene expression analysis revealed a multitude of genes exhibiting differences in expression between developmental stages rather than between sexes. Subsequently, we compared the differences in expression patterns of each hormone-related gene by combining the results of a previous RNA-seq study conducted on the heads of castes (reproductives, workers, and soldiers) in the termite Reticulitermes speratus. The results indicated that genes with expression differences among castes in R. speratus, particularly those related to JH and 20E, were significantly more abundant compared to genes with expression differences between adults and nymphs in C. punctulatus. While no significant difference was observed in the number of genes within the insulin signaling pathway, a trend of homologs highly expressed in adult woodroaches but not in adult termites was observed, and the expression patterns of positive and negative regulators in the pathway differed significantly between adults and nymphs. The differences in the expression patterns between Cryptocercus and termites are believed to reflect variations in hormone levels and signaling activities between adults and juveniles, the latter encompassing workers and soldiers in the case of termites.

Keywords

20‐hydoroxyecdysone (20E) Cryptocercus castes insulin juvenile hormone (JH) termites

References

  1. Billeter, J. C., E. J. Rideout, A. J. Dornan, and S. F. Goodwin. 2006. “Control of Male Sexual Behavior in Drosophila by the Sex Determination Pathway.” Current Biology 16: R766–R776. https://doi.org/10.1016/j.cub.2006.08.025.
  2. Bourguignon, T., Q. Tang, S. Y. W. Ho, et al. 2018. “Transoceanic Dispersal and Plate Tectonics Shaped Global Cockroach Distributions: Evidence From Mitochondrial Phylogenomics.” Molecular Biology and Evolution 35: 970–983. https://doi.org/10.1093/molbev/msy013.
  3. Chuan, J., A. Zhou, L. R. Hale, M. He, and X. Li. 2021. “Atria: An Ultra‐Fast and Accurate Trimmer for Adapter and Quality Trimming.” Gigabyte 2021: 1–18. https://doi.org/10.46471/gigabyte.31.
  4. Engel, M. 2011. “Family Group Names for Termites (Isoptera), Redux.” ZooKeys 148: 171–184. https://doi.org/10.3897/zookeys.148.1682.
  5. Evangelista, D. A., B. Wipfler, O. Béthoux, et al. 2019. “An Integrative Phylogenomic Approach Illuminates the Evolutionary History of Cockroaches and Termites (Blattodea).” Proceedings of the Royal Society B: Biological Sciences 286: 20182076. https://doi.org/10.1098/rspb.2018.2076.
  6. Fujiwara, K., A. Karasawa, T. Hanada, et al. 2023. “Caste‐Specific Expressions and Diverse Roles of Takeout Genes in the Termite Reticulitermes speratus.” Scientific Reports 13: 8422. https://doi.org/10.1038/s41598-023-35524-7.
  7. Grabherr, M. G., B. J. Haas, M. Yassour, et al. 2011. “Full‐Length Transcriptome Assembly From RNA‐Seq Data Without a Reference Genome.” Nature Biotechnology 29: 644–652. https://doi.org/10.1038/nbt.1883.
  8. Haas, B. J. 2003. “Improving the Arabidopsis Genome Annotation Using Maximal Transcript Alignment Assemblies.” Nucleic Acids Research 31: 5654–5666. https://doi.org/10.1093/nar/gkg770.
  9. Harrison, M. C., E. Jongepier, H. M. Robertson, et al. 2018. “Hemimetabolous Genomes Reveal Molecular Basis of Termite Eusociality.” Nature Ecology & Evolution 2: 557–566. https://doi.org/10.1038/s41559-017-0459-1.
  10. Hattori, A., Y. Sugime, C. Sasa, et al. 2013. “Soldier Morphogenesis in the Damp‐Wood Termite Is Regulated by the Insulin Signaling Pathway.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 320: 295–306. https://doi.org/10.1002/jez.b.22501.
  11. Hayashi, Y., K. Maekawa, C. A. Nalepa, T. Miura, and S. Shigenobu. 2017. “Transcriptome Sequencing and Estimation of DNA Methylation Level in the Subsocial Wood‐Feeding Cockroach Cryptocercus punctulatus (Blattodea: Cryptocercidae).” Applied Entomology and Zoology 52: 643–651. https://doi.org/10.1007/s13355-017-0519-7.
  12. Husseneder, C., C. McGregor, R. P. Lang, R. Collier, and J. Delatte. 2012. “Transcriptome Profiling of Female Alates and Egg‐Laying Queens of the Formosan Subterranean Termite.” Comparative Biochemistry and Physiology. Part D, Genomics & Proteomics 7: 14–27. https://doi.org/10.1016/j.cbd.2011.10.002.
  13. Jongepier, E., C. Kemena, A. Lopez‐Ezquerra, X. Belles, E. Bornberg‐Bauer, and J. Korb. 2018. “Remodeling of the Juvenile Hormone Pathway Through Caste‐Biased Gene Expression and Positive Selection Along a Gradient of Termite Eusociality.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 330: 296–304. https://doi.org/10.1002/jez.b.22805.
  14. Kim, D., B. Langmead, and S. L. Salzberg. 2015. “HISAT: A Fast Spliced Aligner With Low Memory Requirements.” Nature Methods 12: 357–360. https://doi.org/10.1038/nmeth.3317.
  15. Kim, D., J. M. Paggi, C. Park, C. Bennett, and S. L. Salzberg. 2019. “Graph‐Based Genome Alignment and Genotyping With HISAT2 and HISAT‐Genotype.” Nature Biotechnology 37: 907–915. https://doi.org/10.1038/s41587-019-0201-4.
  16. Korb, J., and X. Belles. 2017. “Juvenile Hormone and Hemimetabolan Eusociality: A Comparison of Cockroaches With Termites.” Current Opinion in Insect Science 22: 109–116. https://doi.org/10.1016/j.cois.2017.06.002.
  17. Korb, J., M. Poulsen, H. Hu, et al. 2015. “A Genomic Comparison of Two Termites With Different Social Complexity.” Frontiers in Genetics 6: 9. https://doi.org/10.3389/fgene.2015.00009.
  18. Koshikawa, S., S. Miyazaki, R. Cornette, T. Matsumoto, and T. Miura. 2008. “Genome Size of Termites (Insecta, Dictyoptera, Isoptera) and Wood Roaches (Insecta, Dictyoptera, Cryptocercidae).” Naturwissenschaften 95: 859–867. https://doi.org/10.1007/s00114-008-0395-7.
  19. Kremer, L. P. M., J. Korb, and E. Bornberg‐Bauer. 2018. “Reconstructed Evolution of Insulin Receptors in Insects Reveals Duplications in Early Insects and Cockroaches.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 330: 305–311. https://doi.org/10.1002/jez.b.22809.
  20. Lavine, L., H. Gotoh, C. S. Brent, I. Dworkin, and D. J. Emlen. 2015. “Exaggerated Trait Growth in Insects.” Annual Review of Entomology 60: 453–472. https://doi.org/10.1146/annurev-ento-010814-021045.
  21. Liao, Y., G. K. Smyth, and W. Shi. 2014. “Featurecounts: An Efficient General Purpose Program for Assigning Sequence Reads to Genomic Features.” Bioinformatics 30: 923–930. https://doi.org/10.1093/bioinformatics/btt656.
  22. Lo, N., G. Tokuda, H. Watanabe, et al. 2000. “Evidence From Multiple Gene Sequences Indicates That Termites Evolved From Wood‐Feeding Cockroaches.” Current Biology 10: 801–804. https://doi.org/10.1016/S0960-9822(00)00561-3.
  23. Maekawa, K., Y. Hayashi, and N. Lo. 2022. “Termite Sociogenomics: Evolution and Regulation of Caste‐Specific Expressed Genes.” Current Opinion in Insect Science 50: 100880. https://doi.org/10.1016/j.cois.2022.100880.
  24. Masuoka, Y., K. Toga, C. A. Nalepa, and K. Maekawa. 2018. “A Crucial Caste Regulation Gene Detected by Comparing Termites and Sister Group Cockroaches.” Genetics 209: 1225–1234. https://doi.org/10.1534/genetics.118.301038.
  25. Mirth, C. K., and L. M. Riddiford. 2007. “Size Assessment and Growth Control: How Adult Size Is Determined in Insects.” BioEssays 29: 344–355. https://doi.org/10.1002/bies.20552.
  26. Miura, T., and K. Maekawa. 2020. “The Making of the Defensive Caste: Physiology, Development, and Evolution of the Soldier Differentiation in Termites.” Evolution & Development 22: 425–437. https://doi.org/10.1111/ede.12335.
  27. Miura, T., and M. E. Scharf. 2011. “Molecular Basis Underlying Caste Differentiation in Termites.” In Biology of Termites: A Modern Synthesis, edited by D. E. Bignell, Y. Roisin, and N. Lo, 211–253. Springer. https://doi.org/10.1007/978-90-481-3977-4_9.
  28. Nalepa, C. A. 1984. “Colony Composition, Protozoan Transfer and Some Life History Characteristics of the Woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae).” Behavioral Ecology and Sociobiology 14: 273–279. https://doi.org/10.1007/BF00299498.
  29. Nalepa, C. A. 2011. “Altricial Development in Wood‐Feeding Cockroaches: The Key Antecedent of Termite Eusociality.” In Biology of Termites: A Modern Synthesis, edited by D. E. Bignell, Y. Roisin, and N. Lo, 69–95. Kluwer Academic Press. https://doi.org/10.1007/978-90-481-3977-4_4.
  30. Priyam, A., B. J. Woodcroft, V. Rai, et al. 2019. “Sequenceserver: A Modern Graphical User Interface for Custom BLAST Databases.” Molecular Biology and Evolution 36: 2922–2924. https://doi.org/10.1093/molbev/msz185.
  31. Pujal, D., J. Escudero, P. Cabrera, et al. 2024. “Functional Redundancy of the Three Insulin Receptors of Cockroaches.” Insect Biochemistry and Molecular Biology 172: 104161. https://doi.org/10.1016/j.ibmb.2024.104161.
  32. R Core Team. 2022. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/.
  33. Rewitz, K. F., R. Rybczynski, J. T. Warren, and L. I. Gilbert. 2006. “The Halloween Genes Code for Cytochrome P450 Enzymes Mediating Synthesis of the Insect Moulting Hormone.” Biochemical Society Transactions 34: 1256–1260. https://doi.org/10.1042/BST0341256.
  34. Robinson, G. E., C. M. Grozinger, and C. W. Whitfield. 2005. “Sociogenomics: Social Life in Molecular Terms.” Nature Reviews Genetics 6: 257–270. https://doi.org/10.1038/nrg1575.
  35. Robinson, M. D., D. J. McCarthy, and G. K. Smyth. 2010. “edgeR: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data.” Bioinformatics 26: 139–140. https://doi.org/10.1093/bioinformatics/btp616.
  36. Saiki, R., Y. Hayashi, K. Toga, et al. 2022. “Comparison of Gene Expression Profiles Among Caste Differentiations in the Termite Reticulitermes speratus.” Scientific Reports 12: 11947. https://doi.org/10.1038/s41598-022-15984-z.
  37. Séité, S., M. C. Harrison, D. Sillam‐Dussès, et al. 2022. “Lifespan Prolonging Mechanisms and Insulin Upregulation Without Fat Accumulation in Long‐Lived Reproductives of a Higher Termite.” Communications Biology 5: 44. https://doi.org/10.1038/s42003-021-02974-6.
  38. Shigenobu, S., Y. Hayashi, D. Watanabe, et al. 2022. “Genomic and Transcriptomic Analyses of the Subterranean Termite Reticulitermes Speratus: Gene Duplication Facilitates Social Evolution.” Proceedings of the National Academy of Sciences United Stated 119: e2110361119. https://doi.org/10.1073/pnas.2110361119.
  39. Smýkal, V., M. Pivarči, J. Provazník, et al. 2020. “Complex Evolution of Insect Insulin Receptors and Homologous Decoy Receptors, and Functional Significance of Their Multiplicity.” Molecular Biology and Evolution 37: 1775–1789. https://doi.org/10.1093/molbev/msaa048.
  40. Sugime, Y., K. Oguchi, H. Gotoh, et al. 2019. “Termite Soldier Mandibles Are Elongated by Dachshund Under Hormonal and Hox Gene Controls.” Development 146: dev171942. https://doi.org/10.1242/dev.171942.
  41. Teleman, A. A. 2010. “Molecular Mechanisms of Metabolic Regulation by Insulin in Drosophila.” Biochemical Journal 425: 13–26. https://doi.org/10.1042/BJ20091181.
  42. Ureña, E., C. Manjón, X. Franch‐Marro, and D. Martín. 2014. “Transcription Factor E93 Specifies Adult Metamorphosis in Hemimetabolous and Holometabolous Insects.” Proceedings of the National Academy of Sciences United States of America 111: 7024–7029. https://doi.org/10.1073/pnas.1401478111.
  43. Wu, Q., and M. R. Brown. 2006. “Signaling and Function of Insulin‐Like Peptides in Insects.” Annual Review of Entomology 51: 1–24. https://doi.org/10.1146/annurev.ento.51.110104.151011.

Grants

  1. /This study was supported in part by the JST SPRING (No. JPMJSP2145), and Scientific Research (Nos. JP21K19293, and JP22H02672 to Kiyoto Maekawa) from the Japan Society for the Promotion of Science.
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