Treffer: A Breeding System Derived From Asexual Queen Succession in Termite Colonies From Cold Climate Regions.

A Breeding System Derived From Asexual Queen Succession in Termite Colonies From Cold Climate Regions.

Takahashi M; Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto, Japan., Konishi T; Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto, Japan., Yabe K; Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto, Japan., Takata M; Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto, Japan., Matsuura K; Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto, Japan.

Molecular ecology [Mol Ecol] 2025 Apr; Vol. 34 (8), pp. e17724. Date of Electronic Publication: 2025 Mar 21.

Journal Article

English

Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 9214478 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-294X (Electronic) Linking ISSN: 09621083 NLM ISO Abbreviation: Mol Ecol Subsets: MEDLINE

Original Publication: Oxford, UK : Blackwell Scientific Publications, c1992-

Isoptera*/genetics , Isoptera*/physiology , Cold Climate* , Reproduction, Asexual*/genetics , Genetics, Population* , Parthenogenesis*/genetics, Animals ; Female ; Inbreeding ; Reproduction/genetics

Alexander, D. H., J. Novembre, and K. Lange. 2009. “Fast Model‐Based Estimation of Ancestry in Unrelated Individuals.” Genome Research 19, no. 9: 1655–1664.
Arquier, N., C. Géminard, M. Bourouis, et al. 2008. “ Drosophila ALS Regulates Growth and Metabolism Through Functional Interaction With Insulin‐Like Peptides.” Cell Metabolism 7, no. 4: 333–338.
Baudouin, G., F. Dedeine, N. Bech, S. Bankhead‐Dronnet, S. Dupont, and A. G. Bagnères. 2017. “An American Termite in Paris: Temporal Colony Dynamics.” Genetica 145, no. 6: 491–502.
Bolger, A. M., M. Lohse, and B. Usadel. 2014. “Trimmomatic: A Flexible Trimmer for Illumina Sequence Data.” Computer Applications in the Biosciences: CABIOS 30, no. 15: 2114–2120.
Bridle, J. R., and T. H. Vines. 2007. “Limits to Evolution at Range Margins: When and Why Does Adaptation Fail?” Trends in Ecology & Evolution 22, no. 3: 140–147.
Calleri, D. V., E. M. G. Reid, R. B. Rosengaus, E. L. Vargo, and J. F. A. Traniello. 2006. “Inbreeding and Disease Resistance in a Social Insect: Effects of Heterozygosity on Immunocompetence in the Termite Zootermopsis Angusticollis .” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 273, no. 1601: 2633–2640.
Carbonell, J. A., Y. J. Wang, and R. Stoks. 2021. “Evolution of Cold Tolerance and Thermal Plasticity in Life History, Behaviour and Physiology During a Poleward Range Expansion.” Journal of Animal Ecology 90, no. 7: 1666–1677.
Chen, S., Y. Zhou, Y. Chen, and J. Gu. 2018. “Fastp: An Ultra‐Fast All‐in‐One FASTQ Preprocessor.” Bioinformatics 34, no. 17: i884–i890.
Cronin, A. L., N. Azuma, S. Miyazaki, E. Oguri, M. P. Schwarz, and F. Ito. 2020. “Geographic Patterns in Colonial Reproductive Strategy in Myrmecina Nipponica: Links Between Biogeography and a Key Polymorphism in Ants.” Journal of Evolutionary Biology 33, no. 9: 1192–1202.
Darriba, D., D. Posada, A. M. Kozlov, A. Stamatakis, B. Morel, and T. Flouri. 2020. “ModelTest‐NG: A New and Scalable Tool for the Selection of DNA and Protein Evolutionary Models.” Molecular Biology and Evolution 37, no. 1: 291–294.
Dauwalder, B., S. Tsujimoto, J. Moss, and W. Mattox. 2002. “The Drosophila Takeout Gene Is Regulated by the Somatic Sex‐Determination Pathway and Affects Male Courtship Behavior.” Genes & Development 16: 2879–2892.
Dobin, A., C. A. Davis, F. Schlesinger, et al. 2013. “STAR: Ultrafast Universal RNA‐seq Aligner.” Bioinformatics 29, no. 1: 15–21.
Doucet, D., V. K. Walker, and W. Qin. 2009. “The Bugs That Came in From the Cold: Molecular Adaptations to Low Temperatures in Insects.” Cellular and Molecular Life Sciences: CMLS 66, no. 8: 1404–1418.
Dronnet, S., M. Chapuisat, E. L. Vargo, C. Lohou, and A. G. Bagnères. 2005. “Genetic Analysis of the Breeding System of an Invasive Subterranean Termite, Reticulitermes Santonensis, in Urban and Natural Habitats.” Molecular Ecology 14, no. 5: 1311–1320.
Esenther, G. R. 1969. “Termites in Wisconsin.” Annals of the Entomological Society of America 62, no. 6: 1274–1284.
Eyer, P. A., and E. L. Vargo. 2022. “Short and Long‐Term Costs of Inbreeding in the Lifelong‐Partnership in a Termite.” Communications Biology 5, no. 1: 1–12.
Eyer, P.‐A., and E. L. Vargo. 2021. “Breeding Structure and Invasiveness in Social Insects.” Current Opinion in Insect Science 46: 24–30.
Fujita, A., I. Shimizu, and T. Abe. 2001. “Distribution of Lysozyme and Protease, and Amino Acid Concentration in the Guts of a Wood‐Feeding Termite, Reticulitermes Speratus (Kolbe): Possible Digestion of Symbiont Bacteria Transferred by Trophallaxis.” Physiological Entomology 26, no. 2: 116–123.
Fujiwara, Y., C. Hermann‐Luibl, M. Katsura, et al. 2018. “The CCHamide1 Neuropeptide Expressed in the Anterior Dorsal Neuron 1 Conveys a Circadian Signal to the Ventral Lateral Neurons in Drosophila Melanogaster .” Frontiers in Physiology 9: 1–15.
Fick, S. E., and R. J. Hijmans. 2017. “WorldClim 2: New 1‐km Spatial Resolution Climate Surfaces for Global Land Areas.” International Journal of Climatology 37, no. 12: 4302–4315.
Ghiselin, M. T. 1974. The Economy of Nature and the Evolution of Sex. University of California Press.
Glesener, R. R., and D. Tilman. 1978. “Sexuality and the Components of Environmental Uncertainty: Clues From Geographic Parthenogenesis in Terrestrial Animals.” American Naturalist 112, no. 986: 659–673.
Gottar, M., V. Gobert, A. A. Matskevich, et al. 2006. “Dual Detection of Fungal Infections in Drosophila via Recognition of Glucans and Sensing of Virulence Factors.” Cell 127, no. 7: 1425–1437.
Hamilton, W. D., P. A. Henderson, and N. A. Moran. 1981. “Fluctuation of Environment and Coevolved Antagonist Polymorphism as Factors n the Maintenance of Sex.” In Natural Selection and Social Behavior, edited by R. D. Alexander and D. Tinkle , 363–381. Chiron Press.
Hayashi, Y., O. Kitade, and J.‐I. Kojima. 2003. “Parthenogenetic Reproduction in Neotenics of the Subterranean Termite Reticulitermes Speratus (Isoptera: Rhinotermitidae).” Entomological Science 6, no. 4: 253–257.
Hayashi, Y., N. Lo, H. Miyata, and O. Kitade. 2007. “Sex‐Linked Genetic Influence on Caste Determination in a Termite.” Science 318, no. 5852: 985–987.
Hellemans, S., K. Dolejšová, J. Křivánek, D. Fournier, R. Hanus, and Y. Roisin. 2019. “Widespread Occurrence of Asexual Reproduction in Higher Termites of the Termes Group (Termitidae: Termitinae).” BMC Evolutionary Biology 19, no. 1: 1–14.
Hull‐Thompson, J., J. Muffat, D. Sanchez, et al. 2009. “Control of Metabolic Homeostasis by Stress Signaling Is Mediated by the Lipocalin NLaz.” PLoS Genetics 5, no. 4: e1000460.
Jollès, P., and J. Jollès. 1984. “What's New in Lysozyme Research? – Always a Model System, Today as Yesterday.” Molecular and Cellular Biochemistry 63, no. 2: 165–189.
Jomori, T., and S. Natori. 1992. “Function of the Lipopolysaccharide‐Binding Protein of Periplaneta Americana as an Opsonin.” FEBS Letters 296, no. 3: 283–286.
Jouvenaz, D. P., D. P. Wojcik, and R. K. Vander Meer. 1989. “First Observation of Polygyny in Fire Ants, Solenopsis spp., in South America.” Psyche: A Journal of Entomology 96, no. 3–4: 161–165.
Koizumi, N., Y. Imai, A. Morozumi, et al. 1999. “Lipopolysaccharide‐Binding Protein of Bombyx mori Participates in a Hemocyte‐Mediated Defense Reaction Against Gram‐Negative Bacteria.” Journal of Insect Physiology 45, no. 9: 853–859.
Kozlov, A. M., D. Darriba, T. Flouri, B. Morel, and A. Stamatakis. 2019. “RAxML‐NG: A Fast, Scalable and User‐Friendly Tool for Maximum Likelihood Phylogenetic Inference.” Computer Applications in the Biosciences: CABIOS 35, no. 21: 4453–4455.
Ladle, R. J. 1992. “Parasites and Sex: Catching the Red Queen.” Trends in Ecology & Evolution 7, no. 12: 405–408.
LeMosy, E. K., Y. Q. Tan, and C. Hashimoto. 2001. “Activation of a Protease Cascade Involved in Patterning the Drosophila Embryo.” Proceedings of the National Academy of Sciences of the United States of America 98, no. 9: 5055–5060.
Levin, D. A. 1975. “Pest Pressure and Recombination Systems in Plants.” American Naturalist 109, no. 968: 437–451.
Li, B., and C. N. Dewey. 2011. “RSEM: Accurate Transcript Quantification From RNA‐Seq Data With or Without a Reference Genome.” BMC Bioinformatics 12, no. 323: 21–40.
Li, H., and R. Durbin. 2009. “Fast and Accurate Short Read Alignment With Burrows‐Wheeler Transform.” Bioinformatics 25, no. 14: 1754–1760.
Li, H., B. Handsaker, A. Wysoker, et al. 2009. “The Sequence Alignment/Map Format and SAMtools.” Bioinformatics 25, no. 16: 2078–2079.
Ligoxygakis, P., N. Pelte, J. A. Hoffmann, and J. M. Reichhart. 2002. “Activation of Drosophila Toll During Fungal Infection by a Blood Serine Protease.” Science 297, no. 5578: 114–116.
Lorenzi, M. C., and S. Turillazzi. 1986. “Behavioural and Ecological Adaptations to the High Mountain Environment of Polistes Biglumis Bimaculatus .” Ecological Entomology 11, no. 2: 199–204.
Luchetti, A., A. Velonà, M. Mueller, and B. Mantovani. 2013. “Breeding Systems and Reproductive Strategies in Italian Reticulitermes Colonies (Isoptera: Rhinotermitidae).” Insectes Sociaux 60, no. 2: 203–211.
Ludwig, M. Z., I. I. Uspensky, A. I. Ivanov, et al. 1991. “Genetic Control and Expression of the Major Ejaculatory Bulb Protein (PEB‐me) in Drosophila Melanogaster .” Biochemical Genetics 29, no. 5–6: 215–239.
Matsuura, K. 2017. “Evolution of the Asexual Queen Succession System and Its Underlying Mechanisms in Termites.” Journal of Experimental Biology 220, no. 1: 63–72.
Matsuura, K., and N. Kobayashi. 2007. “Size, Hatching Rate, and Hatching Period of Sexually and Asexually Produced Eggs in the Facultatively Parthenogenetic Termite Reticulitermes speratus (Isoptera: Rhinotermitidae).” Applied Entomology and Zoology 42, no. 2: 241–246.
Matsuura, K., N. Mizumoto, K. Kobayashi, et al. 2018. “A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate.” American Naturalist 191, no. 6: 677–690.
Matsuura, K., E. L. Vargo, K. Kawatsu, et al. 2009. “Queen Succession Through Asexual Reproduction in Termites.” Science 323, no. 5922: 1687.
Mitaka, Y., T. Akino, and K. Matsuura. 2023. “Development of a Standard Medium for Culturing the Termite Reticulitermes speratus .” Insectes Sociaux 70, no. 2: 265–274.
Miyata, H., H. Furuichi, and O. Kitade. 2004. “Patterns of Neotenic Differentiation in a Subterranean Termite, Reticulitermes speratus (Isoptera: Rhinotermitidae).” Entomological Science 7, no. 4: 309–314.
Mussmann, S. M., M. R. Douglas, T. K. Chafin, and M. E. Douglas. 2019. “BA3‐SNPs: Contemporary Migration Reconfigured in BayesAss for Next‐Generation Sequence Data.” Methods in Ecology and Evolution 10, no. 10: 1808–1813.
Oster, G. F., and E. O. Wilson. 1978. Caste and Ecology in the Social Insects. Princeton University Press.
Perdereau, E., A. G. Bagnères, S. Dupont, and F. Dedeine. 2010. “High Occurrence of Colony Fusion in a European Population of the American Termite Reticulitermes flavipes .” Insectes Sociaux 57, no. 4: 393–402.
Perez, R., and S. Aron. 2020. “Adaptations to Thermal Stress in Social Insects: Recent Advances and Future Directions.” Biological Reviews of the Cambridge Philosophical Society 95, no. 6: 1535–1553.
Porter, S. D., H. G. Fowler, and W. P. Mackay. 1992. “Fire Ant Mound Densities in the United States and Brazil (Hymenoptera: Formicidae).” Journal of Economic Entomology 85, no. 4: 1154–1161.
Porter, S. D., D. F. Williams, R. S. Patterson, and H. G. Fowler. 1997. “Intercontinental Differences in the Abundance of Solenopsis Fire Ants (Hymenoptera: Formicidae): Escape From Natural Enemies?” Environmental Entomology 26, no. 2: 373–384.
Purcell, S., B. Neale, K. Todd‐Brown, et al. 2007. “PLINK: A Tool Set for Whole‐Genome Association and Population‐Based Linkage Analyses.” American Journal of Human Genetics 81: 559–575.
Rambaut, A., A. J. Drummond, D. Xie, G. Baele, and M. A. Suchard. 2018. “Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7.” Systematic Biology 67, no. 5: 901–904.
Robinson, G. E. 1992. “Regulation of Division of Labor in Insect Societies.” Annual Review of Entomology 37, no. 1: 637–665.
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, no. 1: 139–140.
Robinson, M. D., and A. Oshlack. 2010. “A Scaling Normalization Method for Differential Expression Analysis of RNA‐seq Data.” Genome Biology 11, no. 3: 1–9.
Rochette, N. C., A. G. Rivera‐Colón, and J. M. Catchen. 2019. “Stacks 2: Analytical Methods for Paired‐End Sequencing Improve RADseq‐Based Population Genomics.” Molecular Ecology 28, no. 21: 4737–4754.
Ross, K. G., E. L. Vargo, and L. Keller. 1996. “Social Evolution in a New Environment: The Case of Introduced Fire Ants.” Proceedings of the National Academy of Sciences of the United States of America 93, no. 7: 3021–3025.
Sanchez, D., B. López‐Arias, L. Torroja, et al. 2006. “Loss of Glial Lazarillo, a Homolog of Apolipoprotein D, Reduces Lifespan and Stress Resistance in Drosophila .” Current Biology: CB 16, no. 7: 680–686.
Sato, D. X., Y. Matsuda, N. Usio, R. Funayama, K. Nakayama, and T. Makino. 2023. “Genomic Adaptive Potential to Cold Environments in the Invasive Red Swamp Crayfish.” IScience 26, no. 8: 107267.
Scaduto, D. A., S. R. Garner, E. L. Leach, and G. J. Thompson. 2012. “Genetic Evidence for Multiple Invasions of the Eastern Subterranean Termite Into Canada.” Environmental Entomology 41, no. 6: 1680–1686.
Suyama, Y., and Y. Matsuki. 2015. “MIG‐Seq: An Effective PCR‐Based Method for Genome‐Wide Single‐Nucleotide Polymorphism Genotyping Using the Next‐Generation Sequencing Platform.” Scientific Reports 5, no. 1: 1–12.
Takata, M., T. Konishi, S. Nagai, et al. 2023. “Discovery of an Underground Chamber to Protect Kings and Queens During Winter in Temperate Termites.” Scientific Reports 13, no. 1: 1–10.
Takata, M., M. Takahashi, T. Ishibashi, et al. 2024. “Reticulitermes speratus Genome Annotation.” https://doi.org/10.6084/m9.figshare.27100453.v2.
Thomas, P. D., M. J. Campbell, A. Kejariwal, et al. 2003. “PANTHER: A Library of Protein Families and Subfamilies Indexed by Function.” Genome Research 13, no. 9: 2129–2141.
Tu, C. P. D., and B. Akgül. 2005. “ Drosophila Glutathione S‐Transferases.” Methods in Enzymology, 401, 204–226. Elsevier.
Vargo, E. L. 2019. “Diversity of Termite Breeding Systems.” Insects 10, no. 2: 1–12.
Vandel, A. 1928. “La parthénogenèse géographique. Contribution à l'étude biologique et cytologique de la parthénogenèse naturelle.” Bulletin Biologique de la France et de la Belgique 62: 164–182.
Vargo, E. L., and C. Husseneder. 2009. “Biology of Subterranean Termites: Insights From Molecular Studies of Reticulitermes and Coptotermes .” Annual Review of Entomology 54, no. 1: 379–403.
Vargo, E. L., P. E. Labadie, and K. Matsuura. 2012. “Asexual Queen Succession in the Subterranean Termite Reticulitermes virginicus .” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 279, no. 1729: 813–819.
Vargo, E. L., L. Leniaud, L. E. Swoboda, et al. 2013. “Clinal Variation in Colony Breeding Structure and Level of Inbreeding in the Subterranean Termites Reticulitermes Flavipes and R. grassei .” Molecular Ecology 22, no. 5: 1447–1462.
Zhang, J., Y. Zhang, J. Li, M. Liu, and Z. Liu. 2016. “Midgut Transcriptome of the Cockroach Periplaneta Americana and Its Microbiota: Digestion, Detoxification and Oxidative Stress Response.” PLoS One 11, no. 5: e0155254.

20J20278 Japan Society for the Promotion of Science; JP18H05268 Japan Society for the Promotion of Science; JP20K20380 Japan Society for the Promotion of Science; JP21K14863 Japan Society for the Promotion of Science

Keywords: adjustments to cold regions; asexual queen succession; breeding system; population genetics; social insects; termite

Date Created: 20250321 Date Completed: 20250514 Latest Revision: 20250514

20250514

10.1111/mec.17724

40116473

MEDLINE