Wen-Cong Huang, Maraike Probst, Zheng-Shuang Hua, Lénárd L Szánthó, Gergely J Szöllősi, Thijs J G Ettema, Christian Rinke, Tom A Williams, Anja Spang
{"title":"Phylogenomic Analyses Reveal that Panguiarchaeum Is a Clade of Genome-Reduced Asgard Archaea Within the Njordarchaeia.","authors":"Wen-Cong Huang, Maraike Probst, Zheng-Shuang Hua, Lénárd L Szánthó, Gergely J Szöllősi, Thijs J G Ettema, Christian Rinke, Tom A Williams, Anja Spang","doi":"10.1093/molbev/msaf201","DOIUrl":"10.1093/molbev/msaf201","url":null,"abstract":"<p><p>The Asgard archaea are a diverse archaeal phylum important for our understanding of cellular evolution because they include the lineage that gave rise to eukaryotes. Recent phylogenomic work has focused on characterizing the diversity of Asgard archaea in an effort to identify the closest extant relatives of eukaryotes. However, resolving archaeal phylogeny is challenging, and the positions of 2 recently described lineages-Njordarchaeales and Panguiarchaeales-are uncertain, in ways that directly bear on hypotheses of early evolution. In initial phylogenetic analyses, these lineages branched either with Asgards or with the distantly related Korarchaeota, and it has been suggested that their genomes may be affected by metagenomic contamination. Resolving this debate is important because these clades include genome-reduced lineages that may help inform our understanding of the evolution of symbiosis within Asgard archaea. Here, we performed phylogenetic analyses revealing that the Njordarchaeales and Panguiarchaeales constitute the new class Njordarchaeia within Asgard archaea. We found no evidence of metagenomic contamination affecting phylogenetic analyses. Njordarchaeia exhibit hallmarks of adaptations to (hyper-)thermophilic lifestyles, including biased sequence compositions that can induce phylogenetic artifacts unless adequately modeled. Panguiarchaeum is metabolically distinct from its relatives, with reduced metabolic potential and various auxotrophies. Phylogenetic reconciliation recovers a complex common ancestor of Asgard archaea that encoded the Wood-Ljungdahl pathway. The subsequent loss of this pathway during the reductive evolution of Panguiarchaeum may have been associated with the switch to a symbiotic lifestyle, potentially based on H2-syntrophy. Thus, Panguiarchaeum may contain the first obligate symbionts within Asgard archaea besides the lineage leading to eukaryotes.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12411855/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144835721","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Hanon Solomon McShea, Robb A Viens, Babatunde O Olagunju, José-Luis Giner, Paula V Welander
{"title":"The Evolutionary History and Modern Diversity of Triterpenoid Cyclases.","authors":"Hanon Solomon McShea, Robb A Viens, Babatunde O Olagunju, José-Luis Giner, Paula V Welander","doi":"10.1093/molbev/msaf203","DOIUrl":"10.1093/molbev/msaf203","url":null,"abstract":"<p><p>Cyclic terpenoids are a class of lipid compounds containing immense structural and functional diversity, with many cyclic triterpenoids acting as regulators of the physical properties and spatial organization of lipid membranes. Cyclic terpenoids are also readily preserved as terpane fossils, such as steranes and hopanes, forming a rich record of the evolution of life on Earth. Formation of the multiple ring structure of all cyclic terpenoids is catalyzed by terpenoid cyclase enzymes, among which are whole clades of proteins-many from environmental metagenomes and uncultured organisms-whose substrates and products are completely unknown. We investigate the function of these divergent cyclases through biochemical assays, and the evolutionary processes that produced them by testing and applying a variety of evolutionary models. We find deep divergence between the diterpenoid cyclases and triterpenoid cyclases, with other clades branching between the two, rooting the triterpenoid cyclase subtree between squalene-hopene cyclases and sterol cyclases. Through a simple test of evolutionary rate shifts, we find an elevated evolutionary rate in the enzyme active site on the squalene-hopene cyclase stem, potentially indicative of positive selection. Finally, by testing the activity of divergent cyclases for a variety of substrates, we find a group of early branching sterol cyclases from bacteria that synthesize arborinols, two of which produce the molecular precursor to a Permian \"orphan biomarker.\" Together, our data present an evolutionary framework for triterpenoid cyclases that can inform both the biochemical potential of these proteins and their products' occurrence in the geological record.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12414744/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144874169","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Amado Villalobos-Leiva, Enrique Rodriguez-Serrano, Franco Cruz-Jofré, Isabel A Lobos, Alejandro Piñeiro González, Javier Pinochet, Hugo A Benítez
{"title":"Tales of a Super Butterfly: Is Vanessa carye a Truly Migrant Species? Unraveling Migration Using Morphological and Genomics Approaches.","authors":"Amado Villalobos-Leiva, Enrique Rodriguez-Serrano, Franco Cruz-Jofré, Isabel A Lobos, Alejandro Piñeiro González, Javier Pinochet, Hugo A Benítez","doi":"10.1093/molbev/msaf212","DOIUrl":"10.1093/molbev/msaf212","url":null,"abstract":"<p><p>Among movement strategies, migratory behavior is particularly intriguing in insects. Home-breeding is often permanent, and return journeys can take several generations. Although migration is crucial to the ecological and evolutionary processes of the species involved, knowledge of insect migratory behavior needs to be better understood. Vanessa carye, a butterfly native to South America with a latitudinal range of ∼7,000 km, exemplifies this problem. This study analyzed samples collected across the species' range using single-nucleotide polymorphisms (SNPs) to assess population structure, genetic diversity, and geometric morphometrics to examine wing shape variation. Results indicate that V. carye forms a genetically homogeneous unit composed of only two potential populations spanning ∼5,000 km, geographically correlated with the Pacific Ocean and the Andes, maintaining constant gene flow, and with a mean heterozygosity of 5.74% (SE: ±0.048%). Geometric morphometrics detected no geographic differentiation in wing shapes and sizes across ∼7,000 km, suggesting an absence of local adaptation and indicating a conserved wing shape adapted to flight throughout the species' range. Our findings support V. carye as a migratory species with the longest migratory journey among American butterflies, revealing two migratory routes. With these approaches, we provide a consistent methodological framework for migratory studies in species with important gaps in knowledge of their natural history.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":"42 9","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12449186/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145091912","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Alice Namias, Julien Martinez, Iliana Boussou, Kevin Terretaz, William R Conner, Fabienne Justy, Patrick Makoundou, Marco Perriat-Sanguinet, Pierrick Labbé, Mathieu Sicard, Frederic Landmann, Mylène Weill
{"title":"Recombination, Truncation and Horizontal Transfer Shape the Diversity of Wolbachia-induced Cytoplasmic Incompatibility Patterns.","authors":"Alice Namias, Julien Martinez, Iliana Boussou, Kevin Terretaz, William R Conner, Fabienne Justy, Patrick Makoundou, Marco Perriat-Sanguinet, Pierrick Labbé, Mathieu Sicard, Frederic Landmann, Mylène Weill","doi":"10.1093/molbev/msaf200","DOIUrl":"10.1093/molbev/msaf200","url":null,"abstract":"<p><p>Wolbachia are endosymbiotic bacteria inducing various reproductive manipulations of which cytoplasmic incompatibility is the most common. Cytoplasmic incompatibility leads to reduced embryo viability in crosses between males carrying Wolbachia and uninfected females or those carrying an incompatible symbiont strain. In the mosquito Culex pipiens, the Wolbachia wPip causes highly complex crossing patterns. This complexity is linked to the amplification and diversification of the cytoplasmic incompatibility causal genes, cidA and cidB, with polymorphism located in the CidA-CidB interaction regions. We previously showed that some compatibility patterns correlated with the presence or absence of specific cid variants. It is still unknown, however, whether cid gene polymorphism alone is sufficient to explain the diversity of crossing patterns observed in Cx. pipiens. Taking advantage of a new method enabling full-gene acquisition, we sequenced complete cid repertoires from 45 wPip strains collected worldwide. We demonstrated that the extensive diversity of cid genes arises from recombination and horizontal transfers. We uncovered further cidB polymorphism located outside the interface regions and strongly correlated with cytoplasmic incompatibility patterns. Most importantly, we showed that in every wPip genome, all but one cidB variant are truncated. Truncated cidBs located in palindromes are partially or completely deprived of their deubiquitinase domain, crucial for cytoplasmic incompatibility. The identity of the sole full-length cidB variant seems to dictate cytoplasmic incompatibility patterns, irrespective of the truncated cidBs present. Truncated CidBs exhibit reduced toxicity and stability in Drosophila cells, which potentially hinders their loading into sperm, essential for cytoplasmic incompatibility induction.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12461563/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144835723","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jordan Douglas, Remco Bouckaert, Charles W Carter, Peter R Wills
{"title":"Reduced Amino Acid Substitution Matrices Find Traces of Ancient Coding Alphabets in Modern Day Proteins.","authors":"Jordan Douglas, Remco Bouckaert, Charles W Carter, Peter R Wills","doi":"10.1093/molbev/msaf197","DOIUrl":"10.1093/molbev/msaf197","url":null,"abstract":"<p><p>All known living systems make proteins from the same 20 canonically coded amino acids, but this was not always the case. Early genetic coding systems likely operated with a restricted pool of amino acid types and limited means to distinguish between them. Despite this, amino acid substitution models like LG and WAG all assume a constant coding alphabet over time. That makes them especially inappropriate for the aminoacyl-tRNA synthetases (aaRS)-the enzymes that govern translation. To address this limitation, we created a class of substitution models that account for evolutionary changes in the coding alphabet size by defining the transition from 19 states in a past epoch to 20 now. We use a Bayesian phylogenetic framework to improve phylogeny estimation and testing of this two-alphabet hypothesis. The hypothesis was strongly rejected by datasets composed exclusively of \"young\" eukaryotic proteins. It was generally supported by \"old\" (aaRS and non-aaRS) proteins whose origins date from before the last universal common ancestor. Standard methods overestimate the divergence ages of proteins that originated under reduced coding alphabets in both simulated and aaRS alignments. The new model provides a timeline slightly more consistent with the Earth's history. Our findings suggest that aaRS functional bifurcation events can explain much of the genetic code's evolution, but there remain other unknown forces at play too. This work provides a robust, seamless framework for reconstructing phylogenies from ancient protein datasets and offers further insights into the dawn of molecular biology.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12402984/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144835724","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yu Han, Zhihan Zhao, David W G Stanton, Xiao-Le Lei, Zhuang Wu, Yiting Liu, Chong Yu, Xi Chen, Wenyan Li, Juan Wang, Yue You, Yue Li, Sha Lei, Hailin Yi, Wenquan Fan, Quanfa Cai, Rui Min, Changcheng Hu, Canping Chen, Yingjie Cui, Jiqiao Guo, Hongliang Zhang, Haichao Song, Xin Guo, Qiurong Ruan, Yuhua Tan, Ziyi Li, Xiangyu Zhang, Xingyu Shi, Xu Zhou, Yan Zhuang, Aurélie Manin, Laurent A F Frantz, Joel M Alves, Yan Pan, Xiaohong Wu, Shu-Jin Luo, Greger Larson, He Yu
{"title":"Ancient Genomics Reveals the Origin, Dispersal, and Human Management of East Asian Domestic Pigs.","authors":"Yu Han, Zhihan Zhao, David W G Stanton, Xiao-Le Lei, Zhuang Wu, Yiting Liu, Chong Yu, Xi Chen, Wenyan Li, Juan Wang, Yue You, Yue Li, Sha Lei, Hailin Yi, Wenquan Fan, Quanfa Cai, Rui Min, Changcheng Hu, Canping Chen, Yingjie Cui, Jiqiao Guo, Hongliang Zhang, Haichao Song, Xin Guo, Qiurong Ruan, Yuhua Tan, Ziyi Li, Xiangyu Zhang, Xingyu Shi, Xu Zhou, Yan Zhuang, Aurélie Manin, Laurent A F Frantz, Joel M Alves, Yan Pan, Xiaohong Wu, Shu-Jin Luo, Greger Larson, He Yu","doi":"10.1093/molbev/msaf214","DOIUrl":"10.1093/molbev/msaf214","url":null,"abstract":"<p><p>Pigs are the most commercially important modern livestock animal in East Asia. Numerous aspects of their domestication history remain unclear, however, including the geographic center of their domestication, their subsequent dispersal routes, and the emergence of phenotypic traits specific to domestic pigs. To address these questions, we generated 21 nuclear genomes and 23 mitogenomes from ancient domestic pigs and wild boar from 5,800 BCE to 1,300 CE across China. Our analyses of newly generated and previously published Eurasian suid genomes confirmed Northern China and eliminated Southwestern China as the domestication origin of modern East Asian pigs. Following their association with people and the first appearance of black coat coloration, Northern Chinese domestic pigs dispersed alongside Yellow River millet farmers to the Yangtze River Basin and Southwestern China, which they admixed with local wild boar. A genome-wide loss of diversity and signatures of inbreeding in ancient Northern pigs may have been the result of intensified human management as early as 3,000 BCE. Our results reveal the geographic and temporal origins and subsequent dispersal and admixture of pigs in China, mirroring human migration and agricultural development history.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":"42 9","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12461208/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145137979","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Louise D Heitzmann, Paul A Saunders, Julie Perez, Pierre Boursot, Frederic Veyrunes
{"title":"Influence of Gonadal and Chromosomal Sex on the Brain Transcriptome in a Mouse Species with Natural Sex Reversal.","authors":"Louise D Heitzmann, Paul A Saunders, Julie Perez, Pierre Boursot, Frederic Veyrunes","doi":"10.1093/molbev/msaf208","DOIUrl":"10.1093/molbev/msaf208","url":null,"abstract":"<p><p>Sex chromosomes are expected to play a role in shaping the transcriptional architecture of sexual dimorphism, through the direct expression of sex-linked genes, by regulating autosomal genes, or in interactions with hormones. Yet, their degree of involvement remains elusive partly because chromosomal sex (e.g. XX/XY) and gonadal sex (ovaries or testes) are usually inextricably intertwined. They are, however, dissociated in the African pygmy mouse, Mus minutoides, in which a feminizing X (X*) has evolved, resulting in three female genotypes (XX, XX*, and X*Y) and one male genotype (XY). Furthermore, all sex chromosomes are fused to autosomes (neo-sex chromosomes: neo-X, neo-X* and neo-Y). Despite complete sex reversal, X*Y females show distinctive phenotypes with greater fertility, divergent maternal care strategies, and the masculinization of some traits (e.g. enhanced aggressiveness). By comparing the brain transcriptome of the four sexual genotypes, we show that differential gene expression is mainly linked to gonadal sex but also, and significantly, to chromosomal sex. Genes influenced by chromosomal sex are overrepresented on sex-linked genomic regions, and some are strong candidates to explain X*Y-specific behavioral and reproductive traits. Our results also suggest the preferential inactivation of the X* chromosome in XX* females, only in the brain, which could explain their trait similarities with XX females. Overall, we show that sex and neo-sex chromosomes have profoundly impacted the brain transcriptome in ways that reflect their new transmission modes, evolutionary trajectories, and resulting genomic conflicts.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12453993/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144961596","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Shoulu Dai, Pengju Zhao, Wenhao Li, Lingwei Peng, Enhui Jiang, Yuqin Du, Wengang Zhang, Xuelei Dai, Liu Yang, Zhiqiang Li, Linjing Xu, Xianyong Lan, Wenfa Lyu, Liguo Yang, Lingzhao Fang, George E Liu, Yang Zhou
{"title":"Global Pangenome Analysis Highlights the Critical Role of Structural Variants in Cattle Improvement and Identifies a Unique Event as a Novel Enhancer in IGFBP7+ Cells.","authors":"Shoulu Dai, Pengju Zhao, Wenhao Li, Lingwei Peng, Enhui Jiang, Yuqin Du, Wengang Zhang, Xuelei Dai, Liu Yang, Zhiqiang Li, Linjing Xu, Xianyong Lan, Wenfa Lyu, Liguo Yang, Lingzhao Fang, George E Liu, Yang Zhou","doi":"10.1093/molbev/msaf205","DOIUrl":"10.1093/molbev/msaf205","url":null,"abstract":"<p><p>Based on a pangenome graph platform, we simultaneously analyzed the impacts of SNPs and SVs in the population structure and phenotypic formation of global cattle using 2,409 individuals from 82 breeds. We demonstrated that SVs, like SNPs, effectively explain the population structure of global cattle. Genomic regions under strong selection, identified using both SNPs and SVs, consistently revealed footprints associated with human-mediated selection of economic traits in European improved cattle or natural selection of geographical adaptations. Notably, we detected that ∼40.14% of SVs were not tagged (LD, r2 < 0.6) by nearby SNPs. These \"orphan\" SVs may uncover new genetic signals and represent recent mutations associated with specific selection pressures or local environmental adaptation. Selected SVs tagged by SNPs also play causal or dominant roles in regions under selection. For example, our single-cell RNA sequencing has demonstrated that a notable SNP-tagged SV functions as an enhancer of the IGFBP7 gene, regulating fat deposition through IGFBP7+ cells. In conclusion, these SV-related mechanisms likely have caused some differences in economic traits and local adaptability across global cattle populations. Our integrated approaches highlight the unique and indispensable roles of SVs in shaping genetic diversity, offering novel insights into adaptation, selection, and strategies for improving cattle populations.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12401084/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144883163","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Teruyuki Matsunaga, Carolina E Reisenman, Benjamin Goldman-Huertas, Srivarsha Rajshekar, Hiromu C Suzuki, David Tadres, Joshua Wong, Matthieu Louis, Santiago R Ramírez, Noah K Whiteman
{"title":"Odorant Receptors Mediating Avoidance of Toxic Mustard Oils in Drosophila melanogaster Are Expanded in Herbivorous Relatives.","authors":"Teruyuki Matsunaga, Carolina E Reisenman, Benjamin Goldman-Huertas, Srivarsha Rajshekar, Hiromu C Suzuki, David Tadres, Joshua Wong, Matthieu Louis, Santiago R Ramírez, Noah K Whiteman","doi":"10.1093/molbev/msaf164","DOIUrl":"10.1093/molbev/msaf164","url":null,"abstract":"<p><p>Plants release defense volatile compounds that can deter herbivores. Among them are electrophilic toxins, such as isothiocyanates from mustard plants, that activate pain receptors by contact (i.e. taste) in many animals, including Drosophila melanogaster. While specialist insects have evolved strategies to tolerate toxicity and use mustard plants as hosts, it is unclear whether nonspecialist insects detect and avoid electrophilic toxins via olfaction. To address this, and to understand if specialized insects co-opted these toxic compounds as host plant olfactory cues, we leveraged closely related drosophilid species, including the microbe-feeding D. melanogaster and Scaptomyza pallida, and the mustard-feeding specialist Scaptomyza flava. In olfactory assays, D. melanogaster exposed to allyl isothiocyanate volatiles were rapidly immobilized, demonstrating the high toxicity of this wasabi-derived compound to nonspecialists. Through single sensillum electrophysiological recordings from olfactory organs and behavioral assays, we identified an olfactory receptor (Or) necessary for volatile detection and behavioral aversion to allyl isothiocyanate in D. melanogaster. RNA-sequencing and heterologous expression revealed that S. flava possess lineage-specific, triplicated homologs of this Or and that each paralog exhibited broadened and distinct sensitivity to isothiocyanate compounds. Using AlphaFold2 modeling, site-directed mutagenesis, and electrophysiological recordings, we identified two critical amino acid substitutions that changed the sensitivity of these paralogs from fruit-derived odors to isothiocyanates in the mustard specialist S. flava. Our findings show that nonspecialists can detect electrophiles via olfaction and that their olfactory systems can rapidly adapt to toxic host plant niches through co-option and duplication of ancestral chemosensory genes with few amino acid changes.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12448936/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144564950","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Joaquin C B Nunez, Marta Coronado-Zamora, Mathieu Gautier, Martin Kapun, Sonja Steindl, Lino Ometto, Katja Hoedjes, Julia Beets, R Axel W Wiberg, Giovanni R Mazzeo, David J Bass, Denys Radionov, Iryna Kozeretska, Mariia Zinchenko, Oleksandra Protsenko, Svitlana V Serga, Cristina Amor-Jimenez, Sònia Casillas, Alejandro Sánchez-Gracia, Aleksandra Patenkovic, Amanda Glaser-Schmitt, Antonio Barbadilla, Antonio J Buendia-Ruíz, Astra Clelia Bertelli, Balázs Kiss, Banu Sebnem Önder, Bélen Roldán Matrín, Bregje Wertheim, Candice Deschamps, Carlos E Arboleda-Bustos, Carlos Tinedo, Christian Feller, Christian Schlötterer, Clancy Lawler, Claudia Fricke, Cristina P Vieira, Cristina Vieira, Darren J Obbard, Dorcas Juana Orengo, Doris Vela, Eduardo Amat, Elgion Loreto, Envel Kerdaffrec, Esra Durmaz Mitchell, Eva Puerma, Fabian Staubach, M Florencia Camus, Hervé Colinet, Jan Hrcek, Jesper Givskov Sørensen, Jessica Abbott, Joan Torro, John Parsch, Jorge Vieira, Jose Luis Olmo, Khalid Khfif, Krzysztof Wojciechowski, Lilian Madi-Ravazzi, Maaria Kankare, Mads F Schou, Emmanuel D Ladoukakis, M Josefa Gómez-Julián, M Luisa Espinosa-Jimenez, Maria Pilar Garcia Guerreiro, Maria-Eleni Parakatselaki, Marija Savic Veselinovic, Marija Tanaskovic, Marina Stamenkovic-Radak, Margot Paris, Marta Pascual, Michael G Ritchie, Michel Rera, Mihailo Jelić, Mina Hojat Ansari, Mina Rakic, Miriam Merenciano, Natalia Hernandes, Nazar Gora, Nicolas Rode, Omar Rota-Stabelli, Paloma Sepulveda, Patricia Gibert, Pau Carazo, Pinar Kohlmeier, Priscilla A Erickson, Renaud Vitalis, Jorge Roberto Torres, Sara Guirao-Rico, Sebastian E Ramos-Onsins, Silvana Castillo, Tânia F Paulo, Venera Tyukmaeva, Zahara Alonso, Vladimir E Alatortsev, Elena Pasyukova, Dmitry V Mukha, Dmitri A Petrov, Paul Schmidt, Thomas Flatt, Alan O Bergland, Josefa Gonzalez
{"title":"Footprints of Worldwide Adaptation in Structured Populations of Drosophila melanogaster Through the Expanded DEST 2.0 Genomic Resource.","authors":"Joaquin C B Nunez, Marta Coronado-Zamora, Mathieu Gautier, Martin Kapun, Sonja Steindl, Lino Ometto, Katja Hoedjes, Julia Beets, R Axel W Wiberg, Giovanni R Mazzeo, David J Bass, Denys Radionov, Iryna Kozeretska, Mariia Zinchenko, Oleksandra Protsenko, Svitlana V Serga, Cristina Amor-Jimenez, Sònia Casillas, Alejandro Sánchez-Gracia, Aleksandra Patenkovic, Amanda Glaser-Schmitt, Antonio Barbadilla, Antonio J Buendia-Ruíz, Astra Clelia Bertelli, Balázs Kiss, Banu Sebnem Önder, Bélen Roldán Matrín, Bregje Wertheim, Candice Deschamps, Carlos E Arboleda-Bustos, Carlos Tinedo, Christian Feller, Christian Schlötterer, Clancy Lawler, Claudia Fricke, Cristina P Vieira, Cristina Vieira, Darren J Obbard, Dorcas Juana Orengo, Doris Vela, Eduardo Amat, Elgion Loreto, Envel Kerdaffrec, Esra Durmaz Mitchell, Eva Puerma, Fabian Staubach, M Florencia Camus, Hervé Colinet, Jan Hrcek, Jesper Givskov Sørensen, Jessica Abbott, Joan Torro, John Parsch, Jorge Vieira, Jose Luis Olmo, Khalid Khfif, Krzysztof Wojciechowski, Lilian Madi-Ravazzi, Maaria Kankare, Mads F Schou, Emmanuel D Ladoukakis, M Josefa Gómez-Julián, M Luisa Espinosa-Jimenez, Maria Pilar Garcia Guerreiro, Maria-Eleni Parakatselaki, Marija Savic Veselinovic, Marija Tanaskovic, Marina Stamenkovic-Radak, Margot Paris, Marta Pascual, Michael G Ritchie, Michel Rera, Mihailo Jelić, Mina Hojat Ansari, Mina Rakic, Miriam Merenciano, Natalia Hernandes, Nazar Gora, Nicolas Rode, Omar Rota-Stabelli, Paloma Sepulveda, Patricia Gibert, Pau Carazo, Pinar Kohlmeier, Priscilla A Erickson, Renaud Vitalis, Jorge Roberto Torres, Sara Guirao-Rico, Sebastian E Ramos-Onsins, Silvana Castillo, Tânia F Paulo, Venera Tyukmaeva, Zahara Alonso, Vladimir E Alatortsev, Elena Pasyukova, Dmitry V Mukha, Dmitri A Petrov, Paul Schmidt, Thomas Flatt, Alan O Bergland, Josefa Gonzalez","doi":"10.1093/molbev/msaf132","DOIUrl":"10.1093/molbev/msaf132","url":null,"abstract":"<p><p>Large-scale genomic resources can place genetic variation into an ecologically informed context. To advance our understanding of the population genetics of the fruit fly Drosophila melanogaster, we present an expanded release of the community-generated population genomics resource Drosophila Evolution over Space and Time (DEST 2.0; https://dest.bio/). This release includes 530 high-quality pooled libraries from flies collected across six continents over more than a decade (2009 to 2021), most at multiple time points per year; 211 of these libraries are sequenced and shared here for the first time. We used this enhanced resource to elucidate several aspects of the species' demographic history and identify novel signs of adaptation across spatial and temporal dimensions. For example, we showed that the spatial genetic structure of populations is stable over time, but that drift due to seasonal contractions of population size causes populations to diverge over time. We identified signals of adaptation that vary between continents in genomic regions associated with xenobiotic resistance, consistent with independent adaptation to common pesticides. Moreover, by analyzing samples collected during spring and fall across Europe, we provide new evidence for seasonal adaptation related to loci associated with pathogen response. Furthermore, we have also released an updated version of the DEST genome browser. This is a useful tool for studying spatiotemporal patterns of genetic variation in this classic model system.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":"42 8","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-07-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12360290/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144874170","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}