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1. Identification of constrained sequence elements across 239 primate genomes

Author

Natural Environment Research Council (UK), UK Research and Innovation, National Human Genome Research Institute (US), Fundación la Caixa, Vienna Science and Technology Fund, European Commission, Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brasil), Fonds de la Recherche Scientifique (Fédération Wallonie-Bruxelles), Fundação de Amparo à Pesquisa do Estado do Amazonas, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brasil), German Research Foundation, Ministry of Science and Technology of Vietnam, Agencia Estatal de Investigación (España), Generalitat de Catalunya, Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Wenner-Gren Foundation, Leakey Foundation, National Science Foundation (US), National Geographic Society, National Institute on Aging (US), Swedish Research Council, National Research Foundation Singapore, European Research Council, Ministerio de Ciencia e Innovación (España), Ministerio de Ciencia, Innovación y Universidades (España), Kuderna, Lukas F. K. [0000-0002-9992-9295], Kuhlwilm, Martin [0000-0002-0115-1797], Valenzuela, Alejandro [0000-0001-6120-6246], Juan, David [0000-0003-1912-9667], Lizano, Esther [0000-0003-3304-9807], Navarro, Arcadi [0000-0003-2162-8246], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Kuderna, Lukas F. K., Ulirsch, Jacob C., Rashid, Sabrina, Ameen, Mohamed, Sundaram, Laksshman, Hickey, Glenn, Cox, Anthony J., Gao, Hong, Kumar, Arvind, Aguet, Francois, Christmas, Matthew J., Clawson, Hiram, Haeussler, Maximilian, Janiak, Mareike C., Kuhlwilm, Martin, Orkin, Joseph D., Bataillon, Thomas, Manu, Shivakumara, Valenzuela, Alejandro, Bergman, Juraj, Rousselle, Marjolaine, Silva, Felipe Ennes, Agueda, Lidia, Blanc, Julie, Gut, Marta, Vries, Dorien de, Goodhead, Ian, Harris, R. Alan, Raveendran, Muthuswamy, Jensen, Axel, Chuma, Idriss S., Horvath, Julie E., Hvilsom, Christina, Juan, David, Frandsen, Peter, Schraiber, Joshua G., Melo, Fabiano R. de, Bertuol, Fabrício, Byrne, Hazel, Sampaio, Iracilda, Farias, Izeni, Valsecchi, João, Messias, Malu, Silva, Maria N. F. da, Trivedi, Mihir, Rossi, Rogerio, Hrbek, Tomas, Andriaholinirina, Nicole, Rabarivola, Clément J., Zaramody, Alphonse, Jolly, Clifford J., Phillips-Conroy, Jane, Wilkerson, Gregory, Abee, Christian, Simmons, Joe H., Fernandez-Duque, Eduardo, Kanthaswamy, Sree, Shiferaw, Fekadu, Wu, Dongdong, Zhou, Long, Shao, Yong, Zhang, Guojie, Keyyu, Julius D., Knauf, Sascha, Le, Minh D., Lizano, Esther, Merker, Stefan, Navarro, Arcadi, Nadler, Tilo, Khor, Chiea Chuen, Lee, Jessica, Tan, Patrick, Lim, Weng Khong, Kitchener, Andrew C., Zinner, Dietmar, Gut, Ivo, Melin, Amanda D., Guschanski, Katerina, Schierup, Mikkel Heide, Beck, Robin M. D., Karakikes, Ioannis, Wang, Kevin C., Umapathy, Govindhaswamy, Roos, Christian, Boubli, Jean P., Siepel, Adam, Kundaje, Anshul, Paten, Benedict, Lindblad-Toh, Kerstin, Rogers, Jeffrey, Marqués-Bonet, Tomàs, Farh, Kyle Kai-How, Natural Environment Research Council (UK), UK Research and Innovation, National Human Genome Research Institute (US), Fundación la Caixa, Vienna Science and Technology Fund, European Commission, Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brasil), Fonds de la Recherche Scientifique (Fédération Wallonie-Bruxelles), Fundação de Amparo à Pesquisa do Estado do Amazonas, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brasil), German Research Foundation, Ministry of Science and Technology of Vietnam, Agencia Estatal de Investigación (España), Generalitat de Catalunya, Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Wenner-Gren Foundation, Leakey Foundation, National Science Foundation (US), National Geographic Society, National Institute on Aging (US), Swedish Research Council, National Research Foundation Singapore, European Research Council, Ministerio de Ciencia e Innovación (España), Ministerio de Ciencia, Innovación y Universidades (España), Kuderna, Lukas F. K. [0000-0002-9992-9295], Kuhlwilm, Martin [0000-0002-0115-1797], Valenzuela, Alejandro [0000-0001-6120-6246], Juan, David [0000-0003-1912-9667], Lizano, Esther [0000-0003-3304-9807], Navarro, Arcadi [0000-0003-2162-8246], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Kuderna, Lukas F. K., Ulirsch, Jacob C., Rashid, Sabrina, Ameen, Mohamed, Sundaram, Laksshman, Hickey, Glenn, Cox, Anthony J., Gao, Hong, Kumar, Arvind, Aguet, Francois, Christmas, Matthew J., Clawson, Hiram, Haeussler, Maximilian, Janiak, Mareike C., Kuhlwilm, Martin, Orkin, Joseph D., Bataillon, Thomas, Manu, Shivakumara, Valenzuela, Alejandro, Bergman, Juraj, Rousselle, Marjolaine, Silva, Felipe Ennes, Agueda, Lidia, Blanc, Julie, Gut, Marta, Vries, Dorien de, Goodhead, Ian, Harris, R. Alan, Raveendran, Muthuswamy, Jensen, Axel, Chuma, Idriss S., Horvath, Julie E., Hvilsom, Christina, Juan, David, Frandsen, Peter, Schraiber, Joshua G., Melo, Fabiano R. de, Bertuol, Fabrício, Byrne, Hazel, Sampaio, Iracilda, Farias, Izeni, Valsecchi, João, Messias, Malu, Silva, Maria N. F. da, Trivedi, Mihir, Rossi, Rogerio, Hrbek, Tomas, Andriaholinirina, Nicole, Rabarivola, Clément J., Zaramody, Alphonse, Jolly, Clifford J., Phillips-Conroy, Jane, Wilkerson, Gregory, Abee, Christian, Simmons, Joe H., Fernandez-Duque, Eduardo, Kanthaswamy, Sree, Shiferaw, Fekadu, Wu, Dongdong, Zhou, Long, Shao, Yong, Zhang, Guojie, Keyyu, Julius D., Knauf, Sascha, Le, Minh D., Lizano, Esther, Merker, Stefan, Navarro, Arcadi, Nadler, Tilo, Khor, Chiea Chuen, Lee, Jessica, Tan, Patrick, Lim, Weng Khong, Kitchener, Andrew C., Zinner, Dietmar, Gut, Ivo, Melin, Amanda D., Guschanski, Katerina, Schierup, Mikkel Heide, Beck, Robin M. D., Karakikes, Ioannis, Wang, Kevin C., Umapathy, Govindhaswamy, Roos, Christian, Boubli, Jean P., Siepel, Adam, Kundaje, Anshul, Paten, Benedict, Lindblad-Toh, Kerstin, Rogers, Jeffrey, Marqués-Bonet, Tomàs, and Farh, Kyle Kai-How

Abstract

Noncoding DNA is central to our understanding of human gene regulation and complex diseases1,2, and measuring the evolutionary sequence constraint can establish the functional relevance of putative regulatory elements in the human genome3,4,5,6,7,8,9. Identifying the genomic elements that have become constrained specifically in primates has been hampered by the faster evolution of noncoding DNA compared to protein-coding DNA10, the relatively short timescales separating primate species11, and the previously limited availability of whole-genome sequences12. Here we construct a whole-genome alignment of 239 species, representing nearly half of all extant species in the primate order. Using this resource, we identified human regulatory elements that are under selective constraint across primates and other mammals at a 5% false discovery rate. We detected 111,318 DNase I hypersensitivity sites and 267,410 transcription factor binding sites that are constrained specifically in primates but not across other placental mammals and validate their cis-regulatory effects on gene expression. These regulatory elements are enriched for human genetic variants that affect gene expression and complex traits and diseases. Our results highlight the important role of recent evolution in regulatory sequence elements differentiating primates, including humans, from other placental mammals.

Published
2024

2. Y chromosome sequence and epigenomic reconstruction across human populations

Author

Fundación la Caixa, European Research Council, European Commission, Ministerio de Ciencia e Innovación (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Kuderna, Lukas F. K. [0000-0002-9992-9295], Lizano, Esther [0000-0003-3304-9807], Juan, David [0000-0003-1912-9667], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Esteller-Cucala, Paula, Palmada-Flores, Marc, Kuderna, Lukas F. K., Fontsere, Claudia, Serres-Armero, Aitor, Dabad, Marc, Torralvo, María, Faella, Armida, Ferrández-Peral, Luis, Llovera, Laia, Fornas, Oscar, Julià, Eva, Ramírez, Erika, González, Irene, Hecht, Jochen, Lizano, Esther, Juan, David, Marqués-Bonet, Tomàs, Fundación la Caixa, European Research Council, European Commission, Ministerio de Ciencia e Innovación (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Kuderna, Lukas F. K. [0000-0002-9992-9295], Lizano, Esther [0000-0003-3304-9807], Juan, David [0000-0003-1912-9667], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Esteller-Cucala, Paula, Palmada-Flores, Marc, Kuderna, Lukas F. K., Fontsere, Claudia, Serres-Armero, Aitor, Dabad, Marc, Torralvo, María, Faella, Armida, Ferrández-Peral, Luis, Llovera, Laia, Fornas, Oscar, Julià, Eva, Ramírez, Erika, González, Irene, Hecht, Jochen, Lizano, Esther, Juan, David, and Marqués-Bonet, Tomàs

Abstract

Recent advances in long-read sequencing technologies have allowed the generation and curation of more complete genome assemblies, enabling the analysis of traditionally neglected chromosomes, such as the human Y chromosome (chrY). Native DNA was sequenced on a MinION Oxford Nanopore Technologies sequencing device to generate genome assemblies for seven major chrY human haplogroups. We analyzed and compared the chrY enrichment of sequencing data obtained using two different selective sequencing approaches: adaptive sampling and flow cytometry chromosome sorting. We show that adaptive sampling can produce data to create assemblies comparable to chromosome sorting while being a less expensive and time-consuming technique. We also assessed haplogroup-specific structural variants, which would be otherwise difficult to study using short-read sequencing data only. Finally, we took advantage of this technology to detect and profile epigenetic modifications among the considered haplogroups. Altogether, we provide a framework to study complex genomic regions with a simple, fast, and affordable methodology that could be applied to larger population genomics datasets.

Published
2023

3. Phylogenomic analyses provide insights into primate evolution

Author

Chinese Academy of Sciences, National Natural Science Foundation of China, Villum Fonden, Japan Society for the Promotion of Science, Hokkaido University, European Research Council, European Commission, Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Kuderna, Lukas F. K. [0000-0002-9992-9295], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Shao, Yong, Zhou, Long, Li, Fang, Zhao, Lan, Zhang, Bao-Lin, Shao, Feng, Chen, Jia-Wei, Chen, Chun-Yan, Bi, Xupeng, Zhuang, Xiao-Lin, Zhu, Hong-Liang, Hu, Jiang, Sun, Zongyi, Li, Xin, Wang, Depeng, Rivas-González, Iker, Wang, Sheng, Wang, Yun-Mei, Chen, Wu, Li, Gang, Lu, Hui-Meng, Liu, Yang, Kuderna, Lukas F. K., Farh, Kyle Kai-How, Fan, Peng-Fei, Yu, Li, Li, Ming, Liu, Zhi-Jin, Tiley, George P., Yoder, Anne D., Roos, Christian, Hayakawa, Takashi, Marqués-Bonet, Tomàs, Rogers, Jeffrey, Stenson, Peter D., Cooper, David N., Schierup, Mikkel Heide, Yao, Yong-Gang, Zhang, Ya-Ping, Wang, Wen, Qi, Xiao-Guang, Zhang, Guojie, Wu, Dong-Dong, Chinese Academy of Sciences, National Natural Science Foundation of China, Villum Fonden, Japan Society for the Promotion of Science, Hokkaido University, European Research Council, European Commission, Ministerio de Economía y Competitividad (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Kuderna, Lukas F. K. [0000-0002-9992-9295], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Shao, Yong, Zhou, Long, Li, Fang, Zhao, Lan, Zhang, Bao-Lin, Shao, Feng, Chen, Jia-Wei, Chen, Chun-Yan, Bi, Xupeng, Zhuang, Xiao-Lin, Zhu, Hong-Liang, Hu, Jiang, Sun, Zongyi, Li, Xin, Wang, Depeng, Rivas-González, Iker, Wang, Sheng, Wang, Yun-Mei, Chen, Wu, Li, Gang, Lu, Hui-Meng, Liu, Yang, Kuderna, Lukas F. K., Farh, Kyle Kai-How, Fan, Peng-Fei, Yu, Li, Li, Ming, Liu, Zhi-Jin, Tiley, George P., Yoder, Anne D., Roos, Christian, Hayakawa, Takashi, Marqués-Bonet, Tomàs, Rogers, Jeffrey, Stenson, Peter D., Cooper, David N., Schierup, Mikkel Heide, Yao, Yong-Gang, Zhang, Ya-Ping, Wang, Wen, Qi, Xiao-Guang, Zhang, Guojie, and Wu, Dong-Dong

Abstract

Comparative analysis of primate genomes within a phylogenetic context is essential for understanding the evolution of human genetic architecture and primate diversity. We present such a study of 50 primate species spanning 38 genera and 14 families, including 27 genomes first reported here, with many from previously less well represented groups, the New World monkeys and the Strepsirrhini. Our analyses reveal heterogeneous rates of genomic rearrangement and gene evolution across primate lineages. Thousands of genes under positive selection in different lineages play roles in the nervous, skeletal, and digestive systems and may have contributed to primate innovations and adaptations. Our study reveals that many key genomic innovations occurred in the Simiiformes ancestral node and may have had an impact on the adaptive radiation of the Simiiformes and human evolution.

Published
2023

4. A global catalog of whole-genome diversity from 233 primate species

Author

Fundación la Caixa, Vienna Science and Technology Fund, European Commission, Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brasil), International Primatological Society, Rufford Foundation, Margot Marsh Biodiversity Foundation, Primate Conservation, Fundação de Amparo à Pesquisa do Estado do Amazonas, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brasil), German Research Foundation, National Science Foundation (US), Ministry of Science and Technology of Vietnam, Ministerio de Ciencia e Innovación (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, European Research Council, Natural Environment Research Council (UK), UK Research and Innovation, Department of Biotechnology (India), San Diego Zoo Wildlife Alliance, Wenner-Gren Foundation, Leakey Foundation, National Geographic Society, National Institute on Aging (US), National Institutes of Health (US), Swedish Research Council, National Research Foundation Singapore, Government of Singapore, Kuderna, Lukas F. K. [0000-0002-9992-9295], Kuhlwilm, Martin [0000-0002-0115-1797], Orkin, Joseph D. [0000-0001-6922-2072], Valenzuela, Alejandro [0000-0001-6120-6246], Juan, David [0000-0003-1912-9667], Lizano, Esther [0000-0003-3304-9807], Navarro, Arcadi [0000-0003-2162-8246], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Kuderna, Lukas F. K., Gao, Hong, Janiak, Mareike C., Kuhlwilm, Martin, Orkin, Joseph D., Bataillon, Thomas, Manu, Shivakumara, Valenzuela, Alejandro, Bergman, Juraj, Rousselle, Marjolaine, Silva, Felipe Ennes, Agueda, Lidia, Blanc, Julie, Gut, Marta, Vries, Dorien de, Goodhead, Ian, Harris, R. Alan, Raveendran, Muthuswamy, Jensen, Axel, Chuma, Idrissa S., Horvath, Julie E., Hvilsom, Christina, Juan, David, Frandsen, Peter, Schraiber, Joshua G., Melo, Fabiano R. de, Bertuol, Fabrício, Byrne, Hazel, Sampaio, Iracilda, Farias, Izeni, Valsecchi, João, Messias, Malu, Silva, Maria N. F. da, Trivedi, Mihir, Rossi, Rogerio, Hrbek, Tomas, Andriaholinirina, Nicole, Rabarivola, Clément J., Zaramody, Alphonse, Jolly, Clifford J., Phillips-Conroy, Jane, Wilkerson, Gregory, Abee, Christian, Simmons, Joe H., Fernandez-Duque, Eduardo, Kanthaswamy, Sree, Shiferaw, Fekadu, Wu, Dongdong, Zhou, Long, Shao, Yong, Zhang, Guojie, Keyyu, Julius D., Knauf, Sascha, Le, Minh D., Lizano, Esther, Merker, Stefan, Navarro, Arcadi, Nadler, Tilo, Khor, Chiea Chuen, Lee, Jessica, Tan, Patrick, Lim, Weng Khong, Kitchener, Andrew C., Zinner, Dietmar, Gut, Ivo, Melin, Amanda D., Guschanski, Katerina, Schierup, Mikkel Heide, Beck, Robin M. D., Umapathy, Govindhaswamy, Roos, Christian, Boubli, Jean P., Rogers, Jeffrey, Farh, Kyle Kai-How, Marqués-Bonet, Tomàs, Fundación la Caixa, Vienna Science and Technology Fund, European Commission, Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brasil), International Primatological Society, Rufford Foundation, Margot Marsh Biodiversity Foundation, Primate Conservation, Fundação de Amparo à Pesquisa do Estado do Amazonas, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brasil), German Research Foundation, National Science Foundation (US), Ministry of Science and Technology of Vietnam, Ministerio de Ciencia e Innovación (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, European Research Council, Natural Environment Research Council (UK), UK Research and Innovation, Department of Biotechnology (India), San Diego Zoo Wildlife Alliance, Wenner-Gren Foundation, Leakey Foundation, National Geographic Society, National Institute on Aging (US), National Institutes of Health (US), Swedish Research Council, National Research Foundation Singapore, Government of Singapore, Kuderna, Lukas F. K. [0000-0002-9992-9295], Kuhlwilm, Martin [0000-0002-0115-1797], Orkin, Joseph D. [0000-0001-6922-2072], Valenzuela, Alejandro [0000-0001-6120-6246], Juan, David [0000-0003-1912-9667], Lizano, Esther [0000-0003-3304-9807], Navarro, Arcadi [0000-0003-2162-8246], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Kuderna, Lukas F. K., Gao, Hong, Janiak, Mareike C., Kuhlwilm, Martin, Orkin, Joseph D., Bataillon, Thomas, Manu, Shivakumara, Valenzuela, Alejandro, Bergman, Juraj, Rousselle, Marjolaine, Silva, Felipe Ennes, Agueda, Lidia, Blanc, Julie, Gut, Marta, Vries, Dorien de, Goodhead, Ian, Harris, R. Alan, Raveendran, Muthuswamy, Jensen, Axel, Chuma, Idrissa S., Horvath, Julie E., Hvilsom, Christina, Juan, David, Frandsen, Peter, Schraiber, Joshua G., Melo, Fabiano R. de, Bertuol, Fabrício, Byrne, Hazel, Sampaio, Iracilda, Farias, Izeni, Valsecchi, João, Messias, Malu, Silva, Maria N. F. da, Trivedi, Mihir, Rossi, Rogerio, Hrbek, Tomas, Andriaholinirina, Nicole, Rabarivola, Clément J., Zaramody, Alphonse, Jolly, Clifford J., Phillips-Conroy, Jane, Wilkerson, Gregory, Abee, Christian, Simmons, Joe H., Fernandez-Duque, Eduardo, Kanthaswamy, Sree, Shiferaw, Fekadu, Wu, Dongdong, Zhou, Long, Shao, Yong, Zhang, Guojie, Keyyu, Julius D., Knauf, Sascha, Le, Minh D., Lizano, Esther, Merker, Stefan, Navarro, Arcadi, Nadler, Tilo, Khor, Chiea Chuen, Lee, Jessica, Tan, Patrick, Lim, Weng Khong, Kitchener, Andrew C., Zinner, Dietmar, Gut, Ivo, Melin, Amanda D., Guschanski, Katerina, Schierup, Mikkel Heide, Beck, Robin M. D., Umapathy, Govindhaswamy, Roos, Christian, Boubli, Jean P., Rogers, Jeffrey, Farh, Kyle Kai-How, and Marqués-Bonet, Tomàs

Abstract

The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.

Published
2023

5. Eighty million years of rapid evolution of the primate Y chromosome

Author

Chinese Academy of Sciences, Villum Fonden, National Natural Science Foundation of China, Yunnan Province, Kuderna, Lukas F. K. [0000-0002-9992-9295], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Zhou, Yang, Zhan, Xiaoyu, Jin, Jiazheng, Zhou, Long, Bergman, Juraj, Li, Xuemei, Rousselle, Marjolaine, Riera, Meritxell, Zhao, Lan, Fang, Miaoquan, Chen, Jiawei, Fang, Qi, Kuderna, Lukas F. K., Marqués-Bonet, Tomàs, Kitayama, Haruka, Hayakawa, Takashi, Yao, Yong-Gang, Yang, Huanming, Cooper, David N., Qi, Xiaoguang, Wu, Dong-Dong, Schierup, Mikkel Heide, Zhang, Guojie, Chinese Academy of Sciences, Villum Fonden, National Natural Science Foundation of China, Yunnan Province, Kuderna, Lukas F. K. [0000-0002-9992-9295], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Zhou, Yang, Zhan, Xiaoyu, Jin, Jiazheng, Zhou, Long, Bergman, Juraj, Li, Xuemei, Rousselle, Marjolaine, Riera, Meritxell, Zhao, Lan, Fang, Miaoquan, Chen, Jiawei, Fang, Qi, Kuderna, Lukas F. K., Marqués-Bonet, Tomàs, Kitayama, Haruka, Hayakawa, Takashi, Yao, Yong-Gang, Yang, Huanming, Cooper, David N., Qi, Xiaoguang, Wu, Dong-Dong, Schierup, Mikkel Heide, and Zhang, Guojie

Abstract

The Y chromosome usually plays a critical role in determining male sex and comprises sequence classes that have experienced unique evolutionary trajectories. Here we generated 19 new primate sex chromosome assemblies, analysed them with 10 existing assemblies and report rapid evolution of the Y chromosome across primates. The pseudoautosomal boundary has shifted at least six times during primate evolution, leading to the formation of a Simiiformes-specific evolutionary stratum and to the independent start of young strata in Catarrhini and Platyrrhini. Different primate lineages experienced different rates of gene loss and structural and chromatin change on their Y chromosomes. Selection on several Y-linked genes has contributed to the evolution of male developmental traits across the primates. Additionally, lineage-specific expansions of ampliconic regions have further increased the diversification of the structure and gene composition of the Y chromosome. Overall, our comprehensive analysis has broadened our knowledge of the evolution of the primate Y chromosome.

Published
2023

6. Variation in predicted COVID-19 risk among lemurs and lorises

Author

Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Natural Environment Research Council (UK), Ministerio de Economía y Competitividad (España), Instituto de Salud Carlos III, European Commission, Generalitat de Catalunya, European Research Council, Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Howard Hughes Medical Institute, Obra Social la Caixa, Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], Arora, Paramjit S. [0000-0001-5315-401X], Higham, James P. [0000-0002-1133-2030], Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Valenzuela, Alejandro, Kuderna, Lukas F. K., Marrone, Frank, Ramangason, Hasinala, Horvath, Julie E., Roos, Christian, Kitchener, Andrew C., Khor, Chiea Chuen, Lim, Weng Khong, Lee, Jessica G. H., Tan, Patrick, Umapathy, Govindhaswamy, Raveendran, Muthuswamy, Harris, R. Alan, Gut, Ivo, Gut, Marta, Lizano, Esther, Nadler, Tilo, Zinner, Dietmar, Johnson, Steig E., Jarvis, Erich D., Fedrigo, Olivier, Wu, Dongdong, Zhang, Guojie, Farh, Kyle Kai-How, Rogers, Jeffrey, Marqués-Bonet, Tomàs, Navarro, Arcadi, Juan, David, Arora, Paramjit S., Higham, James P., Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Natural Environment Research Council (UK), Ministerio de Economía y Competitividad (España), Instituto de Salud Carlos III, European Commission, Generalitat de Catalunya, European Research Council, Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Howard Hughes Medical Institute, Obra Social la Caixa, Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], Arora, Paramjit S. [0000-0001-5315-401X], Higham, James P. [0000-0002-1133-2030], Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Valenzuela, Alejandro, Kuderna, Lukas F. K., Marrone, Frank, Ramangason, Hasinala, Horvath, Julie E., Roos, Christian, Kitchener, Andrew C., Khor, Chiea Chuen, Lim, Weng Khong, Lee, Jessica G. H., Tan, Patrick, Umapathy, Govindhaswamy, Raveendran, Muthuswamy, Harris, R. Alan, Gut, Ivo, Gut, Marta, Lizano, Esther, Nadler, Tilo, Zinner, Dietmar, Johnson, Steig E., Jarvis, Erich D., Fedrigo, Olivier, Wu, Dongdong, Zhang, Guojie, Farh, Kyle Kai-How, Rogers, Jeffrey, Marqués-Bonet, Tomàs, Navarro, Arcadi, Juan, David, Arora, Paramjit S., and Higham, James P.

Abstract

The novel coronavirus SARS-CoV-2, which in humans leads to the disease COVID-19, has caused global disruption and more than 1.5 million fatalities since it first emerged in late 2019. As we write, infection rates are currently at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary viral target is the cellular receptor angiotensin-converting enzyme2 (ACE2). Recent sequence analyses of the ACE2 gene predicts that many nonhuman primates are also likely to be highly susceptible to infection. However, the anticipated risk is not equal across the Order. Furthermore, some taxonomic groups show high ACE2 amino acid conservation, while others exhibit high variability at this locus. As an example of the latter, analyses of strepsirrhine primate ACE2 sequences to date indicate large variation among lemurs and lorises compared to other primate clades despite low sampling effort. Here, we report ACE2 gene and protein sequences for 71 individual strepsirrhines, spanning 51 species and 19 genera. Our study reinforces previous results and finds additional variability in other strepsirrhine species, and suggests several clades of lemurs have high potential susceptibility to SARS-CoV-2 infection. Troublingly, some species, including the rare and Endangered aye-aye (Daubentonia madagascariensis), as well as those in the genera Avahi and Propithecus, may be at high risk. Given that lemurs are endemic to Madagascar and among the primates at highest risk of extinction globally, further understanding of the potential threat of COVID-19 to their health should be a conservation priority. All feasible actions should be taken to limit their exposure to SARS-CoV-2.

Published
2021

7. Variation in predicted COVID-19 risk among lemurs and lorises

Author

Jeffrey Rogers, Dietmar Zinner, Tilo Nadler, Chiea Chuen Khor, Muthuswamy Raveendran, Weng Khong Lim, Tomas Marques-Bonet, Kyle Kai-How Farh, Frank Marrone, Alejandro E. J. Valenzuela, C. Rabarivola, Minh Duc Le, Erich D. Jarvis, Govindhaswamy Umapathy, Joseph D. Orkin, Hasinala Ramangason, Andrew C. Kitchener, Nicole Volasoa Andriaholinirina, Dong-Dong Wu, Paramjit S. Arora, Ivo Gut, Amanda D. Melin, Lukas F. K. Kuderna, Sivakumara Manu, Esther Lizano, Alphonse Zaramody, Olivier Fedrigo, Guojie Zhang, Mareike C Janiak, R. Alan Harris, Patrick Tan, Arcadi Navarro, Steig E. Johnson, David Juan, Christian Roos, James P. Higham, Marta Gut, Jessica G. H. Lee, Julie E. Horvath, Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Natural Environment Research Council (UK), Ministerio de Ciencia, Innovación y Universidades (España), Instituto de Salud Carlos III, Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), European Commission, Generalitat de Catalunya, Fundación 'la Caixa', Howard Hughes Medical Institute, National Institutes of Health (US), Rockefeller University, Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Valenzuela, Alejandro [0000-0002-2252-3887], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], Ramangason, Hasinala [0000-0003-4222-7476], Horvath, Julie E. [0000-0002-6426-035X], Roos, Christian [0000-0003-0190-4266], Kitchener, Andrew C. [0000-0003-2594-0827], Khor, Chiea Chuen [0000-0002-1128-4729], Lim, Weng Khong [0000-0003-4391-1130], Umapathy, Govindhaswamy [0000-0003-4086-7445], Raveendran, Muthuswamy [0000-0001-6185-4059], Harris, R. Alan [0000-0002-7333-4752], Gut, Ivo [0000-0001-7219-632X], Gut, Marta [0000-0002-4063-7159], Lizano, Esther 0000-0003-3304-9807], Zinner, Dietmar [0000-0003-3967-8014], Manu, Sivakumara [0000-0002-9114-8793], Johnson, Steig E. [0000-0003-2257-8949], Fedrigo, Olivier [0000-0002-6450-7551], Farh, Kyle Kai-How [0000-0001-6947-8537], Rogers, Jeffrey [0000-0002-7374-6490], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Navarro, Arcadi [0000-0003-2162-8246], Juan, David [0000-0003-1912-9667], Arora, Paramjit S. [0000-0001-5315-401X], Higham, James P. [0000-0002-1133-2030], Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Valenzuela, Alejandro, Kuderna, Lukas F. K., Marrone, Frank, Ramangason, Hasinala, Horvath, Julie E., Roos, Christian, Kitchener, Andrew C., Khor, Chiea Chuen, Lim, Weng Khong, Umapathy, Govindhaswamy, Raveendran, Muthuswamy, Harris, R. Alan, Gut, Ivo, Gut, Marta, Zinner, Dietmar, Manu, Sivakumara, Johnson, Steig E., Fedrigo, Olivier, Farh, Kyle Kai-How, Rogers, Jeffrey, Marqués-Bonet, Tomàs, Navarro, Arcadi, Juan, David, Arora, Paramjit S., and Higham, James P.

Subjects
0106 biological sciences, Propithecus, Endangered species, Lemur, Locus (genetics), COVID-19 (Malaltia), 010603 evolutionary biology, 01 natural sciences, Lèmurs, Article, Lorisidae, 03 medical and health sciences, 0302 clinical medicine, Risk Factors, biology.animal, Animals, 0501 psychology and cognitive sciences, Primate, 030212 general & internal medicine, Taxonomic rank, 050102 behavioral science & comparative psychology, Clade, Ecology, Evolution, Behavior and Systematics, Research Articles, 030304 developmental biology, 0303 health sciences, Extinction, biology, Lorísids, 05 social sciences, Primate Diseases, COVID-19, biology.organism_classification, Evolutionary biology, Animal Science and Zoology, Angiotensin-Converting Enzyme 2, Genètica, Research Article
Abstract

Versión preprint disponible en: http://hdl.handle.net/10261/229066, The novel coronavirus SARS‐CoV‐2, which in humans leads to the disease COVID‐19, has caused global disruption and more than 2 million fatalities since it first emerged in late 2019. As we write, infection rates are at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary target of SARS‐CoV‐2 is the cellular receptor angiotensin‐converting enzyme‐2 (ACE2). Recent sequence analyses of the ACE2 gene predict that many nonhuman primates are also likely to be highly susceptible to infection. However, the anticipated risk is not equal across the Order. Furthermore, some taxonomic groups show high ACE2 amino acid conservation, while others exhibit high variability at this locus. As an example of the latter, analyses of strepsirrhine primate ACE2 sequences to date indicate large variation among lemurs and lorises compared to other primate clades despite low sampling effort. Here, we report ACE2 gene and protein sequences for 71 individual strepsirrhines, spanning 51 species and 19 genera. Our study reinforces previous results while finding additional variability in other strepsirrhine species, and suggests several clades of lemurs have high potential susceptibility to SARS‐CoV‐2 infection. Troublingly, some species, including the rare and endangered aye‐aye (Daubentonia madagascariensis), as well as those in the genera Avahi and Propithecus, may be at high risk. Given that lemurs are endemic to Madagascar and among the primates at highest risk of extinction globally, further understanding of the potential threat of COVID‐19 to their health should be a conservation priority. All feasible actions should be taken to limit their exposure to SARS‐CoV‐2., ADM is supported bythe Natural Sciences and Engineering Research Council of Canada(NSERC Discovery Grant) and Canada Research Chairs Program.MCJ's postdoctoral appointment is supported by funding from theNatural Environment Research Council (NERC NE/T000341/1). IGand MG acknowledge the support of the Spanish Ministry of Scienceand Innovation through the Instituto de Salud Carlos III and the2014–2020 Smart Growth Operating Program, to the EMBL part-nership and cofinancing with the European Regional DevelopmentFund (MINECO/FEDER, BIO201571792P). We also acknowledgethe support of the Centro de Excelencia Severo Ochoa, and theGeneralitat de Catalunya through the Departament de Salut, De-partament d'Empresa i Coneixement and the CERCA Programme.TMB is supported by funding from the European Research Council(ERC) under the European Union's Horizon 2020 research and in-novation program (grant agreement No. 864203), BFU201786471P (MINECO/FEDER, UE), “Unidad de Excelencia María de Maeztu”,funded by the AEI (CEX2018000792M), Howard Hughes Interna-tional Early Career, Obra Social "La Caixa" and Secretaria d'Uni-versitats i Recerca and CERCA Programme del Departamentd'Economia i Coneixement de la Generalitat de Catalunya (GRC2017 SGR 880). PSA thanks the National Institutes of Health(R35GM130333) for financial support. EL is supported by CGL201782654P (MINECO/FEDER, UE). EDJ and OF's contributions weresupported by funds from Howard Hughes Medical Institute and theRockefeller University. Chris Smith drew the images for Figure 1. Theauthors would like to thank the Veterinary and Zoology staff atWildlife Reserves Singapore for their help in obtaining the tissuesamples, as well as the Lee Kong Chian Natural History Museum forstorage and provision of the tissue samples. Finally, we thank tworeviewers for quick and constructive comments, and Karen Bales forher supportive editorial oversight

Published
2021

8. Variation in predicted COVID-19 risk among lemurs and lorises

Author

Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Valenzuela, Alejandro, Kuderna, Lukas F. K., Marrone, Frank, Ramangason, Hasinala, Horvath, Julie E., Roos, Christian, Kitchener, Andrew C., Khor, Chiea Chuen, Lim, Weng Khong, Lee, Jessica G. H., Tan, Patrick, Umapathy, Govindhaswamy, Raveendran, Muthuswamy, Harris, R. Alan, Gut, Ivo, Gut, Marta, Lizano, Esther, Nadler, Tilo, Zinner, Dietmar, Johnson, Steig E., Jarvis, Erich D., Fedrigo, Olivier, Wu, Dongdong, Zhang, Guojie, Farh, Kyle Kai-How, Rogers, Jeffrey, Marqués-Bonet, Tomàs, Navarro, Arcadi, Juan, David, Arora, Paramjit S., Higham, James P., Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Natural Environment Research Council (UK), Ministerio de Economía y Competitividad (España), Instituto de Salud Carlos III, European Commission, Generalitat de Catalunya, European Research Council, Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Howard Hughes Medical Institute, Fundación 'la Caixa', Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], Arora, Paramjit S. [0000-0001-5315-401X], Higham, James P. [0000-0002-1133-2030], Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Kuderna, Lukas F. K., Marrone, Frank, Arora, Paramjit S., and Higham, James P.

Abstract

Versión editorial disponible en: http://hdl.handle.net/10261/239013, The novel coronavirus SARS-CoV-2, which in humans leads to the disease COVID-19, has caused global disruption and more than 1.5 million fatalities since it first emerged in late 2019. As we write, infection rates are currently at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary viral target is the cellular receptor angiotensin-converting enzyme2 (ACE2). Recent sequence analyses of the ACE2 gene predicts that many nonhuman primates are also likely to be highly susceptible to infection. However, the anticipated risk is not equal across the Order. Furthermore, some taxonomic groups show high ACE2 amino acid conservation, while others exhibit high variability at this locus. As an example of the latter, analyses of strepsirrhine primate ACE2 sequences to date indicate large variation among lemurs and lorises compared to other primate clades despite low sampling effort. Here, we report ACE2 gene and protein sequences for 71 individual strepsirrhines, spanning 51 species and 19 genera. Our study reinforces previous results and finds additional variability in other strepsirrhine species, and suggests several clades of lemurs have high potential susceptibility to SARS-CoV-2 infection. Troublingly, some species, including the rare and Endangered aye-aye (Daubentonia madagascariensis), as well as those in the genera Avahi and Propithecus, may be at high risk. Given that lemurs are endemic to Madagascar and among the primates at highest risk of extinction globally, further understanding of the potential threat of COVID-19 to their health should be a conservation priority. All feasible actions should be taken to limit their exposure to SARS-CoV-2., ADM is supported by the Natural Sciences and Engineering Research Council of Canada (NSERC Discovery Grant) and Canada Research Chairs Program. MCJ’s postdoctoral appointment is supported by funding from the Natural Environment Research Council (NERC NE/T000341/1). IG and MG acknowledge the support of the Spanish Ministry of Science and Innovation through the Instituto de Salud Carlos III and the 2014–2020 Smart Growth Operating Program, to the EMBL partnership and cofinancing with the European Regional Development Fund (MINECO/FEDER, BIO2015-71792-P). We also acknowledge the support of the Centro de Excelencia Severo Ochoa, and the Generalitat de Catalunya through the Departament de Salut, Departament d’Empresa i Coneixement and the CERCA Programme. TMB is supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 864203), BFU2017-86471-P (MINECO/FEDER, UE), “Unidad de Excelencia María de Maeztu”, funded by the AEI (CEX2018-000792-M), Howard Hughes International Early Career, Obra Social "La Caixa" and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880). PSA thanks the National Institutes of Health (R35GM130333) for financial support. E.L is supported by CGL2017- 82654-P (MINECO/FEDER,UE). EDJ and OF's contributions were supported by funds from Howard Hughes Medical Institute and the Rockefeller University. Chris Smith drew the images for Figure 1. The authors would like to thank the Veterinary and Zoology staff at Wildlife Reserves Singapore for their help in obtaining the tissue samples, as well as the Lee Kong Chian Natural History Museum for storage and provision of the tissue samples.

Published
2021

9. A comparative genomics multitool for scientific discovery and conservation

Author

Oliver A. Ryder, Jeremy Johnson, Ross Swofford, Wilfried Haerty, Jennifer R. S. Meadows, Gill Bejerano, Eva Murén, Jessica Alföldi, Marlys L. Houck, Katherine S. Pollard, David A. Ray, Emma C. Teeling, Robert Hubley, Leona G. Chemnick, Eric S. Lander, Vadim N. Gladyshev, Martin T. Nweeia, Federica Di Palma, Teemu Kivioja, Voichita D. Marinescu, Hyun Ji Noh, Joana Damas, Mark Diekhans, Mark S. Springer, Arian F.A. Smit, Nicholas R. Casewell, Benedict Paten, Lukas F. K. Kuderna, Manuel Garber, Bruce W. Birren, Joel Armstrong, Tomas Marques-Bonet, Aitor Serres, Jason Turner-Maier, Diane P. Genereux, Ian T. Fiddes, Elinor K. Karlsson, William J. Murphy, Will Nash, David Juan, Harris A. Lewin, Cynthia C. Steiner, Kerstin Lindblad-Toh, Linda Goodman, Andreas R. Pfenning, Beth Shapiro, Klaus-Peter Koepfli, Jussi Taipale, National Institutes of Health (US), Swedish Research Council, Knut and Alice Wallenberg Foundation, Uppsala University, European Commission, Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Howard Hughes Medical Institute, European Research Council, Fundación 'la Caixa', Wellcome Trust, Royal Society (UK), Ministerio de Economía y Competitividad (España), Fondation Prince Albert II de Monaco, Smithsonian Institution, Irish Research Council, Medical Research Council (UK), National Science Foundation (US), Academy of Finland, Research Programs Unit, ATG - Applied Tumor Genomics, University of Helsinki, Department of Pathology, Jussi Taipale / Principal Investigator, Armstrong, Joel [0000-0003-2077-4671], Juan, David [0000-0003-1912-9667], Bejerano, Gill [0000-0001-5179-3635], Casewell, Nicholas R. [0000-0002-8035-4719], Garber, Manuel [0000-0001-8732-1293], Kivioja, Teemu [0000-0002-7732-2177], Kuderna, Lukas F. K. [0000-0002-9992-9295], Lander, Eric S. [0000-0003-2662-4631], Noh, Hyun Ji [0000-0002-6634-0599], Nweeia, Martin [0000-0001-7079-4123], Pfenning, Andreas R. [0000-0002-3447-9801], Pollard, Katherine S. [0000-0002-9870-6196], Shapiro, Beth [0000-0002-2733-7776], Teeling, Emma C. [0000-0002-3309-1346], Alfoldi, Jessica [0000-0001-9713-6200], Ryder, Oliver A. [0000-0003-2427-763X], Lewin, Harris A. [0000-0002-1043-7287], Paten, Benedict [0000-0001-8863-3539], Marques-Bonet, Tomas [0000-0002-5597-3075], Karlsson, Elinor K. [0000-0002-4343-3776], and Apollo - University of Cambridge Repository

Subjects
0106 biological sciences, Biomedical Research, Zoonomia Consortium, Loss of Heterozygosity, Genome informatics, 01 natural sciences, Evolutionsbiologi, Neoplasms, HISTORY, Glucose homeostasis, Phylogeny, 0303 health sciences, Multidisciplinary, BROWN ADIPOSE-TISSUE, Eutheria, ALGORITHMS, 1184 Genetics, developmental biology, physiology, Ecological genetics, Genomics, Biodiversity, Extinction, Knowledge Discovery, Phylogenetics, EXTINCTION, Biotechnology, Conservation of Natural Resources, Medicina -- Investigació, Life on Land, Evolution, Genetic Speciation, General Science & Technology, Scientific discovery, Computational biology, Biology, Extinction, Biological, Infections, 010603 evolutionary biology, Descobriments científics, Risk Assessment, Evolutionary genetics, Evolution, Molecular, 03 medical and health sciences, Species Specificity, Genetic, Genetics, Animals, Humans, Selection, Genetic, Genetik, Selection, 030304 developmental biology, Comparative genomics, Evolutionary Biology, Human evolutionary genetics, Venoms, Human Genome, Molecular, Genetic Variation, 15. Life on land, FRAMEWORK, Biological, Genòmica, Biodiversitat -- Conservació, GLUCOSE-HOMEOSTASIS, Sequence Alignment, human activities, Mamífers, Analysis
Abstract

The Zoonomia Project is investigating the genomics of shared and specialized traits in eutherian mammals. Here we provide genome assemblies for 131 species, of which all but 9 are previously uncharacterized, and describe a whole-genome alignment of 240 species of considerable phylogenetic diversity, comprising representatives from more than 80% of mammalian families. We find that regions of reduced genetic diversity are more abundant in species at a high risk of extinction, discern signals of evolutionary selection at high resolution and provide insights from individual reference genomes. By prioritizing phylogenetic diversity and making data available quickly and without restriction, the Zoonomia Project aims to support biological discovery, medical research and the conservation of biodiversity., This project was funded by NIH NHGRI R01HG008742 (E.K.K., B.B., D.P.G., R.S., J.T.-M., J.J., H.J.N., B.P. and J. Armstrong), Swedish Research Council Distinguished Professor Award (K.L.-T., V.D.M., E.M. and J.R.S.M.), Swedish Research Council grant 2018-05973 (K.L.-T.), Knut and Alice Wallenberg Foundation (K.L.-T., V.D.M., E.M. and J.R.S.M.), Uppsala University (K.L.-T., V.D.M., E.M., J.R.S.M., J.J., J. Alfoldi and L.G.), Broad Institute Next10 (L.G.), Gladstone Institutes (K.S.P.), NIH NHGRI 5R01HG002939 (A.F.A.S. and R.H.), NIH NHGRI 5U24HG010136 (A.F.A.S. and R.H.), NIH NHGRI 5R01HG010485 (B.P. and M.D.), NIH NHGRI 2U41HG007234 (B.P., M.D. and J. Armstrong), NIH NIA 5PO1AG047200 (V.N.G.), NIH NIA 1UH2AG064706 (V.N.G.), BFU2017-86471-P MINECO/FEDER, UE (T.M.-B.), Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya GRC 2017 SGR 880 (T.M.-B.), Howard Hughes International Early Career (T.M.-B.), European Research Council Horizon 2020 no. 864203 (T.M.-B.), Obra Social ‘La Caixa’ (T.M.-B.), BBSRC BBS/E/T/000PR9818, BBS/E/T/ 000PR9783 (W.H. and W.N.), BBSRC Core Strategic Programme Grant BB/P016774/1 (W.H., W.N. and F.D.), Sir Henry Dale Fellowship 200517/Z/16/Z jointly funded by the Wellcome Trust and the Royal Society (N.R.C.), FJCI-2016-29558 MICINN (D.J.), Prince Albert II Foundation of Monaco and Canada, Global Genome Initiative, Smithsonian Institution (M.N.), European Research Council Research Grant ERC-2012-StG311000 (E.C.T.), Irish Research Council Laureate Award (E.C.T.), UK Medical Research Council MR/P026028/1 (W.H. and W.N.), National Science Foundation DEB-1457735 (M.S.S.), National Science Foundation DEB-1753760 (W.J.M.), National Science Foundation IOS-2029774 (E.K.K. and D.P.G.), Robert and Rosabel Osborne Endowment (H.A.L. and J.D.), Swedish Research Council, FORMAS 221-2012-1531 (J.R.S.M.), NSF RoL: FELS: EAGER: DEB 1838283 (D.A.R.) and Academy of Finland grant to Center of Excellence in Tumor Genetics Research no. 312042 (T.K. and J.T.).

Published
2020

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