The object of study of the research group are the mechanisms that regulate the metamorphosis of insects , and how these mechanisms have evolved from ancestral species, with a gradual metamorphosis (like in cockroaches or locusts), to the most modified species, with a discontinuous metamorphosis (like in butterflies or flies). Therefore, the questions that the research group on the Evolution of insect metamorphosis seek to answer are: How did metamorphosis develop in insects? What endocrine and molecular mechanisms led to the evolutionary transition from gradual to discontinuous metamorphosis?

Lab website: Bellés Lab


Investigador principal

Xavier Bellés Ros

Bellés Ros, Xavier
Ad Honorem CSIC Researcher
Evolution of Insect Metamorphosis Lab

Membres del grup

Judit Gonzalvo Colmena

Gonzalvo Colmena, Judit
Scientific Support Personnel
Nutritional signals in Insects Lab & Evolution of Insect Metamorphosis Lab

Projectes en curs


Fernandez-Nicolas A, Machaj G, Ventos-Alfonso A, Pagone V, Minemura T, Ohde T, Daimon T, Ylla G, Belles X. 2023. Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis. Proceedings of the National Academy of Sciences, 120(7):2017. DOI:10.1073/pnas.2216640120

Shirai Y, Piulachs M, Belles X, Daimon T. 2022. DIPA-CRISPR is a simple and accessible method for insect gene editing. Cell Reports Methods, 2(5):100215. DOI:10.1016/j.crmeth.2022.100215

Fernandez-Nicolas A, Ventos-Alfonso A, Kamsoi O, Clark-Hachtel C, Tomoyasu Y, Belles X. 2022. Broad complex and wing development in cockroaches. Insect Biochemistry and Molecular Biology, 147. DOI:10.1016/j.ibmb.2022.103798

Elias-Neto M, Alvarez N, Ventos-Alfonso A, Belles X. 2022. Flight or protection: the genes Ultrabithorax and apterous in the determination of membranous and sclerotized wings in insects. Proceedings of the Royal Society B: Biological Sciences, 289(1981). DOI:10.1098/rspb.2022.0967

Belles X. 2022. The sex of scents. Nature Ecology & Evolution, 6(8):1058-1059. DOI:10.1038/s41559-022-01818-8

Kamsoi O, Ventos-Alfonso A, Casares F, Almudi I, Belles X.  2021. Regulation of metamorphosis in neopteran insects is conserved in the paleopteran Cloeon dipterum (Ephemeroptera). Proceedings of the National Academy of Sciences, 118(34):e2105272118. DOI:10.1073/pnas.2105272118

Clark-Hachtel C, Fernandez-Nicolas A, Belles X, Tomoyasu Y. 2021. Tergal and pleural wing-related tissues in the German cockroach and their implication to the evolutionary origin of insect wingsEvolution & development, 23(2): 100–116. DOI: 10.1111/ede.12372.

Belles X. 2021. A synopsis of the spider beetles (Coleoptera: Ptinidae) of Socotra, with the description of a new genus and two new species. Zoology in the Middle East, 67(2):133-143. DOI:10.1080/09397140.2021.1883623

Ventós-Alfonso A, Ylla G, Montañes JC, Belles X. 2020. DNMT1 Promotes Genome Methylation and Early Embryo Development in Cockroaches. iScience, 23(12). DOI:10.1016/j.isci.2020.101778

Kamsoi O, Belles X. 2020. E93-depleted adult insects preserve the prothoracic gland and molt again. Development, 147(22). DOI: 10.1242/dev.190066.

Belles X. 2020. Krüppel homolog 1 and E93: The doorkeeper and the key to insect metamorphosisArchives of Insect Biochemistry and Physiology, 103(3):1-8. DOI:10.1002/arch.21609

Wexler J, Delaney EK, Belles X, Schal C, Wada-Katsumata A, Amicucci MJ, Kopp A. 2019. Hemimetabolous insects elucidate the origin of sexual development via alternative splicing. eLife, 8:587964. DOI:10.7554/eLife.47490

Ventos-Alfonso A, Ylla G, Belles X. 2019. Zelda and the maternal-to-zygotic transition in cockroaches. FEBS Journal, 286(16):3206-3221. DOI:10.1111/febs.14856

Kamsoi O, Belles X. 2019. Myoglianin triggers the premetamorphosis stage in hemimetabolan insects. FASEB Journal, 33(3):3659-3669. DOI:10.1096/fj.201801511R

Belles X. 2019. The innovation of the final moult and the origin of insect metamorphosis. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1783). DOI:10.1098/rstb.2018.0415.

Ylla G, Piulachs MD, Belles X. 2018. Comparative Transcriptomics in Two Extreme Neopterans Reveals General Trends in the Evolution of Modern Insects. iScience, 4:164-179. DOI:10.1016/j.isci.2018.05.017

Ylla G, Piulachs MD, Belles X. 2018. Comparative Transcriptomics in Two Extreme Neopterans Reveals General Trends in the Evolution of Modern Insects. iScience, 4:164-179. DOI:10.1016/j.isci.2018.05.017

Rubio M, Maestro JL, Piulachs MD, Belles X. 2018. Conserved association of Argonaute 1 and 2 proteins with miRNA and siRNA pathways throughout insect evolution, from cockroaches to flies. Biochimica et Biophysica Acta - Gene Regulatory Mechanisms, 1861(6):554-560. DOI:10.1016/j.bbagrm.2018.04.001

Llonga N, Ylla G, Bau J, Belles X, Piulachs MD. 2018. Diversity of piRNA expression patterns during the ontogeny of the German cockroach. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 330(5):288-295. DOI:10.1002/jez.b.22815

Jongepier E, Kemena C, Lopez-Ezquerra A, Belles X, Bornberg-Bauer E, Korb J. 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(5):296-304. DOI:10.1002/jez.b.22805

Huang JH, Liu Y, Lin YH, Belles X, Lee HJ. 2018. Practical use of RNA interference: Oral delivery of double-stranded RNA in liposome carriers for cockroaches. Journal of Visualized Experiments, 135:1-6. DOI:10.3791/57385

Harrison MC, Jongepier E, Robertson HM, Arning N, Bitard-Feildel T, Chao H, Childers CP, Dinh H, Doddapaneni H, Dugan S, Gowin J, Greiner C, Han Y, Hu H, Hughes DST, Huylmans AK, Kemena C, Kremer LPM, Lee SL, Lopez-Ezquerra A, Mallet L, Monroy-Kuhn JM, Moser A, Murali SC, Muzny DM, Otani S, Piulachs MD, Poelchau M, Qu J, Schaub F, Wada-Katsumata A, Worley KC, Xie Q, Ylla G, Poulsen M, Gibbs RA, Schal C, Richards S, Belles X, Korb J, Bornberg-Bauer E. 2018. Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology & Evolution, 2(3):557-566. DOI:10.1038/s41559-017-0459-1

Harrison MC, Arning N, Kremer LPM, Ylla G, Belles X, Bornberg-Bauer E, Huylmans AK, Jongepier E, Piulachs MD, Richards S, Schal C. 2018. Expansions of key protein families in the German cockroach highlight the molecular basis of its remarkable success as a global indoor pest. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 330(5):254-264. DOI:10.1002/jez.b.22824

Bukejs A, Bellés X, Alekseev VI. 2018. A new species of Dignomus Wollaston (Coleoptera: Ptinidae) from Eocene Baltic amber. Zootaxa, 4486(2):195-200. DOI:10.11646/zootaxa.4486.2.9

Ylla G, Piulachs MD, Belles X. 2017. Comparative analysis of miRNA expression during the development of insects of different metamorphosis modes and germ-band types. BMC Genomics, 18(1):1-13. DOI:10.1186/s12864-017-4177-5

Lin YH, Huang JH, Liu Y, Belles X, Lee HJ. 2017. Oral delivery of dsRNA lipoplexes to German cockroach protects dsRNA from degradation and induces RNAi response. Pest Management Science, 73(5):960-966. DOI:10.1002/ps.4407

Korb J, Belles X. 2017. Juvenile hormone and hemimetabolan. Current Opinion in Insect Science, 22:109-116. DOI:10.1016/j.cois.2017.06.002

Fernandez-Nicolas A, Belles X. 2017. Juvenile hormone signaling in short germ-band hemimetabolan embryos. Development (Cambridge), 144(24):4637-4644. DOI:10.1242/dev.152827

Borras-Castells F, Nieva C, Maestro JL, Maestro O, Belles X, Martín D. 2017. Juvenile hormone biosynthesis in adult Blattella germanica requires nuclear receptors Seven-up and FTZ-F1. Scientific Reports, 7:1-15. DOI:10.1038/srep40234

Belles X. 2017. MicroRNAs and the Evolution of Insect Metamorphosis. Annual Review of Entomology, 62(1):111-125. DOI:10.1146/annurev-ento-031616-034925

Ylla G, Fromm B, Piulachs MD, Belles X. 2016. The microRNA toolkit of insects. Scientific Reports, 6(November):1-13. DOI:10.1038/srep37736

Santos CG, Fernandez-Nicolas A, Belles X. 2016. Smads and insect hemimetabolan metamorphosis. Developmental Biology, 417(1):104-113. DOI:10.1016/j.ydbio.2016.07.006

Fernandez-Nicolas A, Belles X. 2016. CREB-binding protein contributes to the regulation of endocrine and developmental pathways in insect hemimetabolan pre-metamorphosis. Biochimica et Biophysica Acta - General Subjects, 1860(3):508-515. DOI:10.1016/j.bbagen.2015.12.008

Elias-Neto M, Belles X. 2016. Tergal and pleural structures contribute to the formation of ectopic prothoracic wings in cockroaches. Royal Society Open Science, 3(8). DOI:10.1098/rsos.160347

Ons S, Bellés X, Maestro JL. 2015. Orcokinins contribute to the regulation of vitellogenin transcription in the cockroach Blattella germanica. Journal of Insect Physiology, 82:129-133. DOI:10.1016/j.jinsphys.2015.10.002

Lozano J, Montañez R, Belles X. 2015. MiR-2 family regulates insect metamorphosis by controlling the juvenile hormone signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 112(12):3740-3745. DOI:10.1073/pnas.1418522112

Jindra M, Bellés X, Shinoda T. 2015. Molecular basis of juvenile hormone signaling. Current Opinion in Insect Science, 11:39-46. DOI:10.1016/j.cois.2015.08.004

Dillon MB, Schulten V, Oseroff C, Paul S, Dullanty LM, Frazier A, Belles X, Piulachs MD, Visness C, Bacharier L, Bloomberg GR, Busse P, Sidney J, Peters B, Sette A. 2015. Different Bla-g T cell antigens dominate responses in asthma versus rhinitis subjects. Clinical and Experimental Allergy, 45(12):1856-1867. DOI:10.1111/cea.12643

Belles X, Ylla G. 2015. Towards understanding the molecular basis of cockroach tergal gland morphogenesis. A transcriptomic approach. Insect Biochemistry and Molecular Biology, 63:104-112. DOI:10.1016/j.ibmb.2015.06.008

Belles X, Piulachs MD. 2015. Ecdysone signalling and ovarian development in insects: From stem cells to ovarian follicle formation. Biochimica et Biophysica Acta - Gene Regulatory Mechanisms, 1849(2):181-186. DOI:10.1016/j.bbagrm.2014.05.025

Patiño-Navarrete R, Piulachs MD, Belles X, Moya A, Latorre A, Peretó J. 2014. The cockroach Blattella germanica obtains nitrogen from uric acid through a metabolic pathway shared with its bacterial endosymbiont. Biology Letters, 10(7):7-10. DOI:10.1098/rsbl.2014.0407

Lozano J, Belles X. 2014. Role of methoprene-tolerant (Met) in adult morphogenesis and in adult ecdysis of Blattella germanica. PLoS ONE, 9(7). DOI:10.1371/journal.pone.0103614

Lozano J, Kayukawa T, Shinoda T, Belles X. 2014. A Role for Taiman in Insect Metamorphosis. PLoS Genetics, 10(10). DOI:10.1371/journal.pgen.1004769

Herraiz A, Belles X, Piulachs MD. 2014. Chorion formation in panoistic ovaries requires windei and trimethylation of histone 3 lysine 9. Experimental Cell Research, 320(1):46-53. DOI:10.1016/j.yexcr.2013.07.006

Belles X, Santos CG. 2014. The MEKRE93 (Methoprene tolerant-Krüppel homolog 1-E93) pathway in the regulation of insect metamorphosis, and the homology of the pupal stage. Insect Biochemistry and Molecular Biology, 52(1):60-68. DOI:10.1016/j.ibmb.2014.06.009

Rubio M, Belles X. 2013. Subtle roles of microRNAs let-7, miR-100 and miR-125 on wing morphogenesis in hemimetabolan metamorphosis. Journal of Insect Physiology, 59(11):1089-1094. DOI:10.1016/j.jinsphys.2013.09.003

Rubio M, Montañez R, Perez L, Milan M, Belles X. 2013. Regulation of atrophin by both strands of the mir-8 precursor. Insect Biochemistry and Molecular Biology, 43(11):1009-1014. DOI:10.1016/j.ibmb.2013.08.003

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