Evolutionary constraint and innovation across hundreds of placental mammals
[INTRODUCTION] A major challenge in genomics is discerning which bases among billions alter organismal phenotypes and affect health and disease risk. Evidence of past selective pressure on a base, whether highly conserved or fast evolving, is a marker of functional importance. Bases that are unchanged in all mammals may shape phenotypes that are essential for organismal health. Bases that are evolving quickly in some species, or changed only in species that share an adaptive trait, may shape phenotypes that support survival in specific niches. Identifying bases associated with exceptional capacity for cellular recovery, such as in species that hibernate, could inform therapeutic discovery.
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2023-04-28
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[INTRODUCTION] A major challenge in genomics is discerning which bases among billions alter organismal phenotypes and affect health and disease risk. Evidence of past selective pressure on a base, whether highly conserved or fast evolving, is a marker of functional importance. Bases that are unchanged in all mammals may shape phenotypes that are essential for organismal health. Bases that are evolving quickly in some species, or changed only in species that share an adaptive trait, may shape phenotypes that support survival in specific niches. Identifying bases associated with exceptional capacity for cellular recovery, such as in species that hibernate, could inform therapeutic discovery. |
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National Institutes of Health (US) Christmas, Matthew J. Kaplow, Irene M. Genereux, Diane P. Dong, Michael X. Hughes, Graham M. Li, Xue Sullivan, Patrick F. Hindle, Allyson G. Andrews,Gregory Armstrong, Joel C. Bianchi, Matteo Breit, Ana M. Diekhans, Mark Fanter, Cornelia Foley, Nicole M. Goodman, Daniel B. Goodman, Linda Keough, Kathleen C. Kirilenko, Bogdan Kowalczyk, Amanda Lawless, Colleen Lind, Abigail L. Meadows, Jennifer R. S. Moreira, Lucas R. Redlich, Ruby W. Ryan, Louise Swofford, Ross Valenzuela, Alejandro Wagner, Franziska Wallerman, Ola Brown, Ashley R. Damas, Joana Fan, Kaili Gatesy, John Grimshaw, Jenna Johnson, Jeremy Kozyrev, Sergey V. Lawler, Alyssa J. Marinescu, Voichita D. Morrill, Kathleen M. Osmanski, Austin Paulat, Nicole S. Phan, Badoi N. Reilly, Steven K. Schäffer, Daniel E. Steiner, Cynthia Supple, Megan A. Wilder, Aryn P. Wirthlin, Morgan E. Xue, James R. Zoonomia Consortium Birren, Bruce W. Gazal, Steven Hubley, Robert M. Koepfli, Klaus-Peter Marqués-Bonet, Tomàs Meyer, Wynn K. Nweeia, Martin Sabeti, Pardis C. Shapiro, Beth Smit, Arian F. A. Springer, Mark S. Teeling, Emma C. Weng, Zhiping Hiller, Michael Levesque, Danielle L. Lewin, Harris A. Murphy, William J. Navarro, Arcadi Paten, Benedict Pollard, Katherine S. Ray, David A. Ruf, Irina Ryder, Oliver A. Pfenning , Andreas R. Lindblad-Toh, Kerstin Karlsson, Elinor K. |
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Christmas, Matthew J. Kaplow, Irene M. Genereux, Diane P. Dong, Michael X. Hughes, Graham M. Li, Xue Sullivan, Patrick F. Hindle, Allyson G. Andrews,Gregory Armstrong, Joel C. Bianchi, Matteo Breit, Ana M. Diekhans, Mark Fanter, Cornelia Foley, Nicole M. Goodman, Daniel B. Goodman, Linda Keough, Kathleen C. Kirilenko, Bogdan Kowalczyk, Amanda Lawless, Colleen Lind, Abigail L. Meadows, Jennifer R. S. Moreira, Lucas R. Redlich, Ruby W. Ryan, Louise Swofford, Ross Valenzuela, Alejandro Wagner, Franziska Wallerman, Ola Brown, Ashley R. Damas, Joana Fan, Kaili Gatesy, John Grimshaw, Jenna Johnson, Jeremy Kozyrev, Sergey V. Lawler, Alyssa J. Marinescu, Voichita D. Morrill, Kathleen M. Osmanski, Austin Paulat, Nicole S. Phan, Badoi N. Reilly, Steven K. Schäffer, Daniel E. Steiner, Cynthia Supple, Megan A. Wilder, Aryn P. Wirthlin, Morgan E. Xue, James R. Zoonomia Consortium Birren, Bruce W. Gazal, Steven Hubley, Robert M. Koepfli, Klaus-Peter Marqués-Bonet, Tomàs Meyer, Wynn K. Nweeia, Martin Sabeti, Pardis C. Shapiro, Beth Smit, Arian F. A. Springer, Mark S. Teeling, Emma C. Weng, Zhiping Hiller, Michael Levesque, Danielle L. Lewin, Harris A. Murphy, William J. Navarro, Arcadi Paten, Benedict Pollard, Katherine S. Ray, David A. Ruf, Irina Ryder, Oliver A. Pfenning , Andreas R. Lindblad-Toh, Kerstin Karlsson, Elinor K. |
spellingShingle |
Christmas, Matthew J. Kaplow, Irene M. Genereux, Diane P. Dong, Michael X. Hughes, Graham M. Li, Xue Sullivan, Patrick F. Hindle, Allyson G. Andrews,Gregory Armstrong, Joel C. Bianchi, Matteo Breit, Ana M. Diekhans, Mark Fanter, Cornelia Foley, Nicole M. Goodman, Daniel B. Goodman, Linda Keough, Kathleen C. Kirilenko, Bogdan Kowalczyk, Amanda Lawless, Colleen Lind, Abigail L. Meadows, Jennifer R. S. Moreira, Lucas R. Redlich, Ruby W. Ryan, Louise Swofford, Ross Valenzuela, Alejandro Wagner, Franziska Wallerman, Ola Brown, Ashley R. Damas, Joana Fan, Kaili Gatesy, John Grimshaw, Jenna Johnson, Jeremy Kozyrev, Sergey V. Lawler, Alyssa J. Marinescu, Voichita D. Morrill, Kathleen M. Osmanski, Austin Paulat, Nicole S. Phan, Badoi N. Reilly, Steven K. Schäffer, Daniel E. Steiner, Cynthia Supple, Megan A. Wilder, Aryn P. Wirthlin, Morgan E. Xue, James R. Zoonomia Consortium Birren, Bruce W. Gazal, Steven Hubley, Robert M. Koepfli, Klaus-Peter Marqués-Bonet, Tomàs Meyer, Wynn K. Nweeia, Martin Sabeti, Pardis C. Shapiro, Beth Smit, Arian F. A. Springer, Mark S. Teeling, Emma C. Weng, Zhiping Hiller, Michael Levesque, Danielle L. Lewin, Harris A. Murphy, William J. Navarro, Arcadi Paten, Benedict Pollard, Katherine S. Ray, David A. Ruf, Irina Ryder, Oliver A. Pfenning , Andreas R. Lindblad-Toh, Kerstin Karlsson, Elinor K. Evolutionary constraint and innovation across hundreds of placental mammals |
author_sort |
Christmas, Matthew J. |
title |
Evolutionary constraint and innovation across hundreds of placental mammals |
title_short |
Evolutionary constraint and innovation across hundreds of placental mammals |
title_full |
Evolutionary constraint and innovation across hundreds of placental mammals |
title_fullStr |
Evolutionary constraint and innovation across hundreds of placental mammals |
title_full_unstemmed |
Evolutionary constraint and innovation across hundreds of placental mammals |
title_sort |
evolutionary constraint and innovation across hundreds of placental mammals |
publisher |
American Association for the Advancement of Science |
publishDate |
2023-04-28 |
url |
http://hdl.handle.net/10261/348077 |
work_keys_str_mv |
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dig-ibe-es-10261-3480772024-02-23T09:49:37Z Evolutionary constraint and innovation across hundreds of placental mammals Christmas, Matthew J. Kaplow, Irene M. Genereux, Diane P. Dong, Michael X. Hughes, Graham M. Li, Xue Sullivan, Patrick F. Hindle, Allyson G. Andrews,Gregory Armstrong, Joel C. Bianchi, Matteo Breit, Ana M. Diekhans, Mark Fanter, Cornelia Foley, Nicole M. Goodman, Daniel B. Goodman, Linda Keough, Kathleen C. Kirilenko, Bogdan Kowalczyk, Amanda Lawless, Colleen Lind, Abigail L. Meadows, Jennifer R. S. Moreira, Lucas R. Redlich, Ruby W. Ryan, Louise Swofford, Ross Valenzuela, Alejandro Wagner, Franziska Wallerman, Ola Brown, Ashley R. Damas, Joana Fan, Kaili Gatesy, John Grimshaw, Jenna Johnson, Jeremy Kozyrev, Sergey V. Lawler, Alyssa J. Marinescu, Voichita D. Morrill, Kathleen M. Osmanski, Austin Paulat, Nicole S. Phan, Badoi N. Reilly, Steven K. Schäffer, Daniel E. Steiner, Cynthia Supple, Megan A. Wilder, Aryn P. Wirthlin, Morgan E. Xue, James R. Zoonomia Consortium Birren, Bruce W. Gazal, Steven Hubley, Robert M. Koepfli, Klaus-Peter Marqués-Bonet, Tomàs Meyer, Wynn K. Nweeia, Martin Sabeti, Pardis C. Shapiro, Beth Smit, Arian F. A. Springer, Mark S. Teeling, Emma C. Weng, Zhiping Hiller, Michael Levesque, Danielle L. Lewin, Harris A. Murphy, William J. Navarro, Arcadi Paten, Benedict Pollard, Katherine S. Ray, David A. Ruf, Irina Ryder, Oliver A. Pfenning , Andreas R. Lindblad-Toh, Kerstin Karlsson, Elinor K. National Institutes of Health (US) National Science Foundation (US) European Research Council European Commission Ministerio de Ciencia e Innovación (España) Agencia Estatal de Investigación (España) Ministerio de Ciencia, Innovación y Universidades (España) Science Foundation Ireland Irish Research Council Swedish Research Council Carnegie Mellon University Roddenberry Foundation Gladstone Institutes LOEWE Center for Insect Biotechnology & Bioresources Robert and Rosabel Osborne Endowment SFI Research Centre in Applied Geosciences (Ireland) Alfred P. Sloan Foundation UMaine Institute of Medicine University College Dublin Knut and Alice Wallenberg Foundation Lehigh University Valenzuela, Alejandro [0000-0001-6120-6246] Marqués-Bonet, Tomàs [0000-0002-5597-3075] Navarro, Arcadi [0000-0003-2162-8246] [INTRODUCTION] A major challenge in genomics is discerning which bases among billions alter organismal phenotypes and affect health and disease risk. Evidence of past selective pressure on a base, whether highly conserved or fast evolving, is a marker of functional importance. Bases that are unchanged in all mammals may shape phenotypes that are essential for organismal health. Bases that are evolving quickly in some species, or changed only in species that share an adaptive trait, may shape phenotypes that support survival in specific niches. Identifying bases associated with exceptional capacity for cellular recovery, such as in species that hibernate, could inform therapeutic discovery. [RATIONALE] The power and resolution of evolutionary analyses scale with the number and diversity of species compared. By analyzing genomes for hundreds of placental mammals, we can detect which individual bases in the genome are exceptionally conserved (constrained) and likely to be functionally important in both coding and noncoding regions. By including species that represent all orders of placental mammals and aligning genomes using a method that does not require designating humans as the reference species, we explore unusual traits in other species. [RESULTS] Zoonomia’s mammalian comparative genomics resources are the most comprehensive and statistically well-powered produced to date, with a protein-coding alignment of 427 mammals and a whole-genome alignment of 240 placental mammals representing all orders. We estimate that at least 10.7% of the human genome is evolutionarily conserved relative to neutrally evolving repeats and identify about 101 million significantly constrained single bases (false discovery rate < 0.05). We cataloged 4552 ultraconserved elements at least 20 bases long that are identical in more than 98% of the 240 placental mammals. Many constrained bases have no known function, illustrating the potential for discovery using evolutionary measures. Eighty percent are outside protein-coding exons, and half have no functional annotations in the Encyclopedia of DNA Elements (ENCODE) resource. Constrained bases tend to vary less within human populations, which is consistent with purifying selection. Species threatened with extinction have few substitutions at constrained sites, possibly because severely deleterious alleles have been purged from their small populations. By pairing Zoonomia’s genomic resources with phenotype annotations, we find genomic elements associated with phenotypes that differ between species, including olfaction, hibernation, brain size, and vocal learning. We associate genomic traits, such as the number of olfactory receptor genes, with physical phenotypes, such as the number of olfactory turbinals. By comparing hibernators and nonhibernators, we implicate genes involved in mitochondrial disorders, protection against heat stress, and longevity in this physiologically intriguing phenotype. Using a machine learning–based approach that predicts tissue-specific cis-regulatory activity in hundreds of species using data from just a few, we associate changes in noncoding sequence with traits for which humans are exceptional: brain size and vocal learning. [CONCLUSION] Large-scale comparative genomics opens new opportunities to explore how genomes evolved as mammals adapted to a wide range of ecological niches and to discover what is shared across species and what is distinctively human. High-quality data for consistently defined phenotypes are necessary to realize this potential. Through partnerships with researchers in other fields, comparative genomics can address questions in human health and basic biology while guiding efforts to protect the biodiversity that is essential to these discoveries. This work was funded by National Institutes of Health (NIH) grant R37CA218570; NIH grant R01HG008742; NIH grant R01HG010485; NIH grant RO1-HG002939; NIH grant U01HG010961; NIH grant U24-HG010136; NIH grant U24HG009446; NIH grant U41HG002371; NIH grant U41HG007234; NIH grant U19AG057377; NIH grant DP1DA046585; NIH grant F30DA053020; NIH grant R24OD018250; National Science Foundation (NSF) grant DEB-1753760; NSF grant DEB-2150664; NSF grant DBI-2046550; NSF grant DEB 1838283; NSF grant DEB-1457735; NSF grant DGE-1252522; NSF grant DGE-1745016; NSF grant IOS-2032006; NSF grant IOS-1929592; NSF grant IOS-2022007; NSF grant IOS-2029774; NSF grant TG-BIO200055; NSF grant ACI-1548562; NSF Postdoctoral Fellowship in Biology 2011038 (C.F.); European Research Council under the European Union’s Horizon 2020 research and innovation program grant 864203 (T.M.-B.); MINECO/FEDER, UE grant PID2021-126004NB-100 (T.M.-B.); FEDER/UE grant AEI-PGC2018-101927-BI00 704 (A.N.C.), AEI grant CEX2018-000792-M (A.N.C. and T.M.-B.), Science Foundation Ireland 19/FFP/6790 (E.C.T.); Irish Research Council Laureate grant (E.C.T.); Distinguished professorship from the Swedish Research Council (K.L.-T.); Swedish Research Council Vetenskapsrådet grant D0886501 (P.F.S.); Carnegie Mellon University Computational Biology Department Lane Postdoctoral Fellowship (I.M.K.); Carnegie Mellon University SURF grant (D.E.S.); Gift from Ed and Pam Taft, Roddenberry Foundation, Gladstone Institutes (K.S.P.); LOEWE-Centre for Translational Biodiversity Genomics (M.H.); Robert and Rosabel Osborne Endowment, UC Davis (H.A.L.); SFI Centre for Research Training in Genomics Data Science grant 18/CRT/6214 (L.R.); Sloan Foundation grant (A.R.P.); UMaine Institute of Medicine Seed Grant (D.L.L.); University College Dublin Ad Astra Fellowship (G.M.H.); Knut and Alice Wallenberg Foundation (K.L.-T.); NSF grant 2019035 (Lehigh University Research Computing Infrastructure); NSF grant TG-BIO200055 [The Extreme Science and Engineering Discovery Environment (XSEDE)]; and Swedish Research Council grant 2018-05973 [Swedish National Infrastructure for Computing (SNIC) at UPPMAX]. With funding from the Spanish government through the ‘María de Maeztu Unit of Excelence’ accreditation (CEX2018-000792-M). No 2024-02-23T07:58:58Z 2024-02-23T07:58:58Z 2023-04-28 artículo Science 380(6643): eabn3943 (2023) 0036-8075 CEX2018-000792-M http://hdl.handle.net/10261/348077 10.1126/science.abn3943 1095-9203 en #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/H2020/864203 info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-126004NB-I00/ES/LA INTERACCION ENTRE LA EPIGENOMICA Y LA DIVERGENCIA GENOMICA EN LA EVOLUCION RECIENTE DE PRIMATES Y MAMIFEROS/ info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-101927-B-I00/ES/LAS CAUSAS EVOLUTIVAS Y MECANICAS DE LA SENESCENCIA Y SUS FENOTIPOS RELACIONADOS EN VERTEBRADOS: UNA APROXIMACION DE GENOMICA COMPARADA/ info:eu-repo/grantAgreement/AEI//CEX2018-000792-M https://doi.org/10.1126/science.abn3943 Sí none American Association for the Advancement of Science |