Biochemistry, Genetics and Molecular Biology, Developmental Biology, Insect Science, Genetics
143
Scopus Publications
Scopus Publications
Retroelement expansions underlie genome evolution in stingless bees Natalia de Souza Araujo, Patricia Azevedo, Rafael Rodrigues Ferrari, Lucas Borges dos Santos, Florence Rodriguez, Roberta Cornélio Ferreira Nocelli, Matthew Hudson, Thiago Mafra Batista, Klaus Hartfelder, Serge Aron BMC Genomics, 2026 Stingless bees serve as crucial pollinators and are increasingly recognized as models for investigating behavioral and genomic evolution in insects. In the genus Melipona, a major difference in heterochromatin organization defines two groups: Group I species (e.g., M. quadrifasciata) with < 50% of pericentromeric heterochromatin and Group II species (e.g., M. scutellaris) containing > 50% heterochromatin across their chromosomes. These differences are believed to correlate with genome size and transposable element (TE) content, offering a unique opportunity to explore how heterochromatin variation, TE dynamics, and chromosomal evolution interact in a phylogenetic context. We present pseudo-chromosome-level genome assemblies for M. quadrifasciata and M. scutellaris obtained through long-read sequencing and 3D chromosome conformation scaffolding. Comparative analyses reveal conserved synteny but marked divergence in structural variants and TE types. M. scutellaris exhibits an expansion of retrotransposons, particularly Gypsy/DIRS1 elements, concentrated in TE hotspots linked to chromosomal rearrangements and structural variants. This coincides with distinct methylation entropy patterns across the genome and an expansion of histone deacetylase orthologs. The increased proportion of retrotransposons in M. scutellaris is counterbalanced by more DNA transposons in M. quadrifasciata, resulting in genomes of similar overall sizes but with distinct heterochromatin distributions. Advancing our understanding of genome evolution in eusocial insects, we provide high-resolution genomic resources for two Melipona species that differ in heterochromatin content. Our results highlight the complex role of TEs in shaping genomes and underscore their influence on chromosomal and epigenetic innovation, providing compelling evidence that TE dynamics underlie the pronounced heterochromatic differences observed in Melipona.
Rethinking the epigenetic foundations of social behavior evolution in insects Carlos AM Cardoso-Júnior, Klaus Hartfelder Current Opinion in Insect Science, 2026 Gene body DNA methylation is an evolutionarily conserved, stable yet reversible modification of DNA, where cytosines in CpG contexts are covalently methylated (5-methyl-cytosine) by DNA methyltransferase (DNMT) enzymes. The discovery of a functional gene body DNA methylation system in honey bees (Apis mellifera L.) with high homology to the human machinery has positioned social insects, including wasps, ants, and bees, as tractable models for epigenetic research. Their advanced societies consist of multiple phenotypes with distinct morphologies, physiologies, and behaviors, all developed from the same genome. Here we examine seminal studies on DNA methylation in social Hymenoptera, focusing on three recent advances: (i) gene body DNA methylation has minimal, if any, effect on transcription; (ii) methylomes are faithfully inherited across generations and somatic tissues; and (iii) DNMT1 is essential for the germline but dispensable for somatic development. As a mechanistic complement to Hamilton's inclusive fitness theory, we propose that colony-specific gene body DNA methylation patterns may facilitate (but not determine) the multiple independent transitions to eusociality in Hymenoptera. With the framework of a 'DNA methylation-mediated Genetic Recombination Hypothesis', we suggest that DNMT1-maintained gene body DNA methylation accelerates genome evolution toward social complexity in eusocial species. On the other hand, DNMT3, likely operating downstream of the sex-determination pathways, promotes altruism in sterile workers in the presence of the queen, possibly through DNA methylation-independent mechanisms.
Sex-specific division of labor in termites is linked to differential brain architecture and foraging gene expression Iago Bueno da Silva, Arthur Roque Justino, Jaqueline Eterna Batista, Lohan Valadares, Klaus Hartfelder, Fabio Santos do Nascimento Iscience, 2026 gene expression in workers and soldiers of different termite species, suggesting species-dependent effects on foraging. Our findings represent a first step toward elucidating how structural and functional brain changes underlie sex-specific division of labor in termites.
A sterility-associated long noncoding RNA involved in honey bee caste determination and adult queen and worker fertility Carlos A. M. Cardoso-Júnior, Gustavo J. Tibério, Marina C. Peruzzolo, Luiz C. Vieira, Denyse C. Lago, Alexandre R. Paschoal, Isobel Ronai, Benjamin P. Oldroyd, Klaus Hartfelder Proceedings of the National Academy of Sciences of the United States of America, 2026 Insect sociality is a major evolutionary transition based on the suppression of worker reproduction in favor of a queen’s reproductive monopoly. Although sophisticated insect societies have arisen independently on multiple occasions in the Hymenoptera (bees, ants, and wasps), how worker sterility evolved through natural selection is not fully understood. In honey bees ( Apis mellifera ), dietary cues (royal or worker jelly) and social chemical signals (e.g., queen pheromones) promote caste differentiation by modulating the levels of juvenile hormone (JH), the key physiological orchestrator of caste determination in larvae and the maintenance of caste identity in adults. However, the precise molecular effects of JH on the ovaries of larvae and adult bees remain open questions. Here, we describe lncov1 , a long noncoding RNA (lncRNA), whose expression correlates with sterility in the ovaries of larvae and adult honey bees. Mechanistically, the low JH levels in worker larvae promote high lncov1 expression in their ovaries, which subsequently show extensive programmed cell death. Moreover, lncov1 expression is tightly connected to a reduction in the reproductive capacity of adult queens and workers, as this lncRNA responds to key environmental cues that regulate fertility, including royal jelly and queen pheromone. The sequence conservation of the lncov1 gene across eusocial bees, especially the genus Apis , suggests the evolutionary stability of the JH/ lncov1 pathway. Therefore, by revealing how nutritional and social cues acting through JH and lncov1 shape queen and worker fertility in honey bees, these findings position lncRNAs as key components in the evolution of social complexity in insects.
The genomes sequenced for the neotropical stingless bees Scaptotrigona bipunctata and S. depilis strengthen the phylogenomics support for the taxonomy of social bees Paulo Gonzalez Hofstatter, Flávia Cristina de Paula Freitas, Danielle Luna-Lucena, Leonardo Campana, Klaus Hartfelder Genetics and Molecular Biology, 2025 Bees are fundamental factors in ecology and agriculture due to their ecosystem services as pollinators, including many important crops. Because of its ecological significance and value to humans, the honey bee, Apis mellifera, was one of the earliest insect species targeted for genome sequencing, and over the last decades, many other species of social bees, including practically all species comprising the genus Apis and dozens of bumble bee species (Bombini) have complete genome assemblies deposited in public databases. The largest clade of the social bees, the stingless bees (Meliponini), is, however, strongly underrepresented. To date, only five genomes for species of three genera have been released for the New World stingless bees, which comprise over 400 species distributed in 32 genera. Different from the honey bee, these species are native to the Neotropics, being important pollinators of many native plants and cultivars, including greenhouse cultures. We present here the genome assemblies for two species of the genus Scaptotrigona, one of the largest genera among the stingless bees in Brazil. The new datasets are highly complete and, as shown in our phylogenomics analysis, these genomes provide robust support for the clades of the corbiculate bees and their evolutionary history.
Positive selection in cytochrome P450 genes is associated with gonad phenotype and mating strategy in social bees Denyse Cavalcante Lago, Luísa Czamanski Nora, Martin Hasselmann, Klaus Hartfelder Scientific Reports, 2023 The honey bee, Apis mellifera differs from all other social bees in its gonad phenotype and mating strategy. Honey bee queens and drones have tremendously enlarged gonads, and virgin queens mate with several males. In contrast, in all the other bees, the male and female gonads are small, and the females mate with only one or very few males, thus, suggesting an evolutionary and developmental link between gonad phenotype and mating strategy. RNA-seq comparisons of A. mellifera larval gonads revealed 870 genes as differentially expressed in queens versus workers and drones. Based on Gene Ontology enrichment we selected 45 genes for comparing the expression levels of their orthologs in the larval gonads of the bumble bee Bombus terrestris and the stingless bee, Melipona quadrifasciata, which revealed 24 genes as differentially represented. An evolutionary analysis of their orthologs in 13 solitary and social bee genomes revealed four genes with evidence of positive selection. Two of these encode cytochrome P450 proteins, and their gene trees indicated a lineage-specific evolution in the genus Apis, indicating that cytochrome P450 genes may be involved in the evolutionary association of polyandry and the exaggerated gonad phenotype in social bees.
Reproductive potential shapes the expression of nurse-to-forager transition genes in the workers of stingless bees (Meliponini) Larissa D. Ribeiro de Souza, Klaus Hartfelder Apidologie, 2023 Little is known about the molecular mechanisms that underlie the division of labor in stingless bees. We investigated the expression of a set of candidate genes associated with the nurse-to-forager transition in the honey bee in two stingless bee species, Melipona quadrifasciata and Frieseomelitta varia. These species differ with respect to worker reproduction. The workers of M. quadrifasciata lay trophic and reproductive eggs, but those of F. varia are completely sterile. For M. quadrifasciata nurses, we found elevated vitellogenin (Vg) and low juvenile hormone esterase (jhe) transcript levels in the abdomen, in agreement with their reproductive potential. In F. varia, Vg and methyl farnesoate epoxidase (mfe) transcript levels were high in the heads of foragers, indicating an association with foraging behavior. For malvolio (mvl) and foraging (for), both involved with food search behavior, mvl showed persistent low expression in the head, but increasing levels in the abdomen of both species, speaking against a role in behavioral development. The for transcript levels in F. varia were higher in foragers, both in the head and the abdomen, i.e., consistent with foraging. In M. quadrifasciata, however, for expression was higher in the heads of nurse bees, and, thus, is unlikely to play a role in foraging. The results for the two stingless bee species, in comparison with honey bees and bumble bees, indicate that the degree of worker sterility appears to be the primary factor that shapes the expression pattern of key genes in the life history of social bees.
The nuclear and mitochondrial genomes of Frieseomelitta varia - A highly eusocial stingless bee (Meliponini) with a permanently sterile worker caste Flávia C. de Paula Freitas, Anete P. Lourenço, Francis M. F. Nunes, Alexandre R. Paschoal, Fabiano C. P. Abreu, Fábio O. Barbin, Luana Bataglia, Carlos A. M. Cardoso-Júnior, Mário S. Cervoni, Saura R. Silva, Fernanda Dalarmi, Marco A. Del Lama, Thiago S. Depintor, Kátia M. Ferreira, Paula S. Gória, Michael C. Jaskot, Denyse C. Lago, Danielle Luna-Lucena, Livia M. Moda, Leonardo Nascimento, Matheus Pedrino, Franciene Rabiço Oliveira, Fernanda C. Sanches, Douglas E. Santos, Carolina G. Santos, Joseana Vieira, Angel R. Barchuk, Klaus Hartfelder, Zilá L. P. Simões, Márcia M. G. Bitondi, Daniel G. Pinheiro BMC Genomics, 2020
Genomic signatures of evolutionary transitions from solitary to group living Karen M. Kapheim, Hailin Pan, Cai Li, Steven L. Salzberg, Daniela Puiu, Tanja Magoc, Hugh M. Robertson, Matthew E. Hudson, Aarti Venkat, Brielle J. Fischman, Alvaro Hernandez, Mark Yandell, Daniel Ence, Carson Holt, George D. Yocum, William P. Kemp, Jordi Bosch, Robert M. Waterhouse, Evgeny M. Zdobnov, Eckart Stolle, F. Bernhard Kraus, Sophie Helbing, Robin F. A. Moritz, Karl M. Glastad, Brendan G. Hunt, Michael A. D. Goodisman, Frank Hauser, Cornelis J. P. Grimmelikhuijzen, Daniel Guariz Pinheiro, Francis Morais Franco Nunes, Michelle Prioli Miranda Soares, Érica Donato Tanaka, Zilá Luz Paulino Simões, Klaus Hartfelder, Jay D. Evans, Seth M. Barribeau, Reed M. Johnson, Jonathan H. Massey, Bruce R. Southey, Martin Hasselmann, Daniel Hamacher, Matthias Biewer, Clement F. Kent, Amro Zayed, Charles Blatti, Saurabh Sinha, J. Spencer Johnston, Shawn J. Hanrahan, Sarah D. Kocher, Jun Wang, Gene E. Robinson, Guojie Zhang Science, 2015
The genomes of two key bumblebee species with primitive eusocial organization Ben M Sadd, Seth M Barribeau, Guy Bloch, Dirk C de Graaf, Peter Dearden, Christine G Elsik, Jürgen Gadau, Cornelis JP Grimmelikhuijzen, Martin Hasselmann, Jeffrey D Lozier, Hugh M Robertson, Guy Smagghe, Eckart Stolle, Matthias Van Vaerenbergh, Robert M Waterhouse, Erich Bornberg-Bauer, Steffen Klasberg, Anna K Bennett, Francisco Câmara, Roderic Guigó, Katharina Hoff, Marco Mariotti, Monica Munoz-Torres, Terence Murphy, Didac Santesmasses, Gro V Amdam, Matthew Beckers, Martin Beye, Matthias Biewer, Márcia MG Bitondi, Mark L Blaxter, Andrew FG Bourke, Mark JF Brown, Severine D Buechel, Rossanah Cameron, Kaat Cappelle, James C Carolan, Olivier Christiaens, Kate L Ciborowski, David F Clarke, Thomas J Colgan, David H Collins, Andrew G Cridge, Tamas Dalmay, Stephanie Dreier, Louis du Plessis, Elizabeth Duncan, Silvio Erler, Jay Evans, Tiago Falcon, Kevin Flores, Flávia CP Freitas, Taro Fuchikawa, Tanja Gempe, Klaus Hartfelder, Frank Hauser, Sophie Helbing, Fernanda C Humann, Frano Irvine, Lars S Jermiin, Claire E Johnson, Reed M Johnson, Andrew K Jones, Tatsuhiko Kadowaki, Jonathan H Kidner, Vasco Koch, Arian Köhler, F Bernhard Kraus, H Michael G Lattorff, Megan Leask, Gabrielle A Lockett, Eamonn B Mallon, David S Marco Antonio, Monika Marxer, Ivan Meeus, Robin FA Moritz, Ajay Nair, Kathrin Näpflin, Inga Nissen, Jinzhi Niu, Francis MF Nunes, John G Oakeshott, Amy Osborne, Marianne Otte, Daniel G Pinheiro, Nina Rossié, Olav Rueppell, Carolina G Santos, Regula Schmid-Hempel, Björn D Schmitt, Christina Schulte, Zilá LP Simões, Michelle PM Soares, Luc Swevers, Eva C Winnebeck, Florian Wolschin, Na Yu, Evgeny M Zdobnov, Peshtewani K Aqrawi, Kerstin P Blankenburg, Marcus Coyle, Liezl Francisco, Alvaro G Hernandez, Michael Holder, Matthew E Hudson, LaRonda Jackson, Joy Jayaseelan, Vandita Joshi, Christie Kovar, Sandra L Lee, Robert Mata, Tittu Mathew, Irene F Newsham, Robin Ngo, Geoffrey Okwuonu, Christopher Pham, Ling-Ling Pu, Nehad Saada, Jireh Santibanez, DeNard Simmons, Rebecca Thornton, Aarti Venkat, Kimberly KO Walden, Yuan-Qing Wu, Griet Debyser, Bart Devreese, Claire Asher, Julie Blommaert, Ariel D Chipman, Lars Chittka, Bertrand Fouks, Jisheng Liu, Meaghan P O’Neill, Seirian Sumner, Daniela Puiu, Jiaxin Qu, Steven L Salzberg, Steven E Scherer, Donna M Muzny, Stephen Richards, Gene E Robinson, Richard A Gibbs, Paul Schmid-Hempel, Kim C Worley Genome Biology, 2015
The use of open reading frame ESTs (ORESTES) for analysis of the honey bee transcriptome Francis MF Nunes, Valeria Valente, Josane F Sousa, Marco AV Cunha, Daniel G Pinheiro, Rafaela M Maia, Daniela D Araujo, Maria CR Costa, Waleska K Martins, Alex F Carvalho, Nadia Monesi, Adriana M Nascimento, Pablo MV Peixoto, Maria FR Silva, Ricardo GP Ramos, Luis FL Reis, Emmanuel Dias-Neto, Sandro J Souza, Andrew JG Simpson, Marco A Zago, Ademilson EE Soares, Marcia MG Bitondi, Enilza M Espreafico, Foued S Espindola, Maria L Paco-Larson, Zila LP Simoes, Klaus Hartfelder, Wilson A Silva BMC Genomics, 2004
Ventral nerve cord remodeling in a stingless bee (Melipona quadrifasciata anthidioides, Hymenoptera, Apidae) depends on ecdysteroid fluctuation and programmed cell death International Journal of Developmental Biology, 2003