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.

doi:10.1126/science.abn3943

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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, Marques-Bonet, Tomas, 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., Andrews, Gregory, Armstrong, Joel C., Bianchi, Matteo, Birren, Bruce W., Bredemeyer, Kevin R., Breit, Ana M., Christmas, Matthew J., Clawson, Hiram, Damas, Joana, Di Palma, Federica, Diekhans, Mark, Dong, Michael X., Eizirik, Eduardo, Fan, Kaili, Fanter, Cornelia, Foley, Nicole M., Forsberg-Nilsson, Karin, Garcia, Carlos J., Gatesy, John, Gazal, Steven, Genereux, Diane P., Goodman, Linda, Grimshaw, Jenna, Halsey, Michaela K., Harris, Andrew J., Hickey, Glenn, Hiller, Michael, Hindle, Allyson G., Hubley, Robert M., Hughes, Graham M., Johnson, Jeremy, Juan, David, Kaplow, Irene M., Karlsson, Elinor K., Keough, Kathleen C., Kirilenko, Bogdan, Koepfli, Klaus-Peter, Korstian, Jennifer M., Kowalczyk, Amanda, Kozyrev, Sergey V., Lawler, Alyssa J., Lawless, Colleen, Lehmann, Thomas, Levesque, Danielle L., Lewin, Harris A., Li, Xue, Lind, Abigail, Lindblad-Toh, Kerstin, Mackay-Smith, Ava, Marinescu, Voichita D., Marques-Bonet, Tomas, Mason, Victor C., Meadows, Jennifer R. S., Meyer, Wynn K., Moore, Jill E., Moreira, Lucas R., Moreno-Santillan, Diana D., Morrill, Kathleen M., Muntané, Gerard, Murphy, William J., Navarro, Arcadi, Nweeia, Martin, Ortmann, Sylvia, Osmanski, Austin, Paten, Benedict, Paulat, Nicole S., Pfenning, Andreas R., Phan, BaDoi N., Pollard, Katherine S., Pratt, Henry E., Ray, David A., Reilly, Steven K., Rosen, Jeb R., Ruf, Irina, Ryan, Louise, Ryder, Oliver A., Sabeti, Pardis C., Schäffer, Daniel E., Serres, Aitor, Shapiro, Beth, Smit, Arian F. A., Springer, Mark, Srinivasan, Chaitanya, Steiner, Cynthia, Storer, Jessica M., Sullivan, Kevin A. M., Sullivan, Patrick F., Sundström, Elisabeth, Supple, Megan A., Swofford, Ross, Talbot, Joy-El, Teeling, Emma, Turner-Maier, Jason, Valenzuela, Alejandro, Wagner, Franziska, Wallerman, Ola, Wang, Chao, Wang, Juehan, Weng, Zhiping, Wilder, Aryn P., Wirthlin, Morgan E., Xue, James R., Zhang, Xiaomeng·2023·Science

DOI 10.1126/science.abn3943PMC PMC10250106

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Abstract

Zoonomia is the largest comparative genomics resource for mammals produced to date. By aligning genomes for 240 species, we identify bases that, when mutated, are likely to affect fitness and alter disease risk. At least 332 million bases (~10.7%) in the human genome are unusually conserved across species (evolutionarily constrained) relative to neutrally evolving repeats, and 4552 ultraconserved elements are nearly perfectly conserved. Of 101 million significantly constrained single bases, 80% are outside protein-coding exons and half have no functional annotations in the Encyclopedia of DNA Elements (ENCODE) resource. Changes in genes and regulatory elements are associated with exceptional mammalian traits, such as hibernation, that could inform therapeutic development. Earth’s vast and imperiled biodiversity offers distinctive power for identifying genetic variants that affect genome function and organismal phenotypes.

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Studies in mammals and birds have shown that highly conserved elements are enriched for transcriptional regulation and organ development pathways.
“studies in both mammals and birds have shown that highly conserved elements are enriched for transcriptional regulation and organ development pathways.9,29”
From A genomic compendium of hundreds of teleost fishes reveals their evolutionary landscape (2026) · cites this paper as [9]
Genome-wide alignments have proved effective for identifying conserved genomic regions in birds, mammals, and primates.
“Genome-wide alignments have proved effective for identifying conserved genomic regions in birds,8 mammals,9 and primates,28”
From A genomic compendium of hundreds of teleost fishes reveals their evolutionary landscape (2026) · cites this paper as [9]
Although genes are commonly considered the most strongly constrained sequences, most constrained and conserved regions are located in non-coding DNA.
“although genes are commonly considered the most strongly constrained sequences, most constrained and conserved regions are located in non-coding.9”
From A genomic compendium of hundreds of teleost fishes reveals their evolutionary landscape (2026) · cites this paper as [9]
Accelerated genes in mammals are linked to immunity, skin development, and certain sensory capabilities.
“Previous studies indicate that these accelerated genes are linked to mammalian immunity, skin development, and certain sensory capabilities.9”
From A genomic compendium of hundreds of teleost fishes reveals their evolutionary landscape (2026) · cites this paper as [9]

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Authors: Christmas, M. J., Kaplow, I. M., Genereux, D. P., Dong, M. X., Hughes, G. M., Li, X., Sullivan, P. F., Hindle, A. G., Andrews, G., Armstrong, J. C., Bianchi, M., Breit, A. M., Diekhans, M., Fanter, C., Foley, N. M., Goodman, D. B., Goodman, L., Keough, K. C., Kirilenko, B., Kowalczyk, A., Lawless, C., Lind, A. L., Meadows, J. R. S., Moreira, L. R., Redlich, R. W., Ryan, L., Swofford, R., Valenzuela, A., Wagner, F., Wallerman, O., Brown, A. R., Damas, J., Fan, K., Gatesy, J., Grimshaw, J., Johnson, J., Kozyrev, S. V., Lawler, A. J., Marinescu, V. D., Morrill, K. M., Osmanski, A., Paulat, N. S., Phan, B. N., Reilly, S. K., Schäffer, D. E., Steiner, C., Supple, M. A., Wilder, A. P., Wirthlin, M. E., Xue, J. R., Zoonomia Consortium§, Birren, B. W., Gazal, S., Hubley, R. M., Koepfli, K.-P., Marques-Bonet, T., Meyer, W. K., Nweeia, M., Sabeti, P. C., Shapiro, B., Smit, A. F. A., Springer, M. S., Teeling, E. C., Weng, Z., Hiller, M., Levesque, D. L., Lewin, H. A., Murphy, W. J., Navarro, A., Paten, B., Pollard, K. S., Ray, D. A., Ruf, I., Ryder, O. A., Pfenning, A. R., Lindblad-Toh, K., Karlsson, E. K., Andrews, G., Armstrong, J. C., Bianchi, M., Birren, B. W., Bredemeyer, K. R., Breit, A. M., Christmas, M. J., Clawson, H., Damas, J., Di Palma, F., Diekhans, M., Dong, M. X., Eizirik, E., Fan, K., Fanter, C., Foley, N. M., Forsberg-Nilsson, K., Garcia, C. J., Gatesy, J., Gazal, S., Genereux, D. P., Goodman, L., Grimshaw, J., Halsey, M. K., Harris, A. J., Hickey, G., Hiller, M., Hindle, A. G., Hubley, R. M., Hughes, G. M., Johnson, J., Juan, D., Kaplow, I. M., Karlsson, E. K., Keough, K. C., Kirilenko, B., Koepfli, K.-P., Korstian, J. M., Kowalczyk, A., Kozyrev, S. V., Lawler, A. J., Lawless, C., Lehmann, T., Levesque, D. L., Lewin, H. A., Li, X., Lind, A., Lindblad-Toh, K., Mackay-Smith, A., Marinescu, V. D., Marques-Bonet, T., Mason, V. C., Meadows, J. R. S., Meyer, W. K., Moore, J. E., Moreira, L. R., Moreno-Santillan, D. D., Morrill, K. M., Muntané, G., Murphy, W. J., Navarro, A., Nweeia, M., Ortmann, S., Osmanski, A., Paten, B., Paulat, N. S., Pfenning, A. R., Phan, B. N., Pollard, K. S., Pratt, H. E., Ray, D. A., Reilly, S. K., Rosen, J. R., Ruf, I., Ryan, L., Ryder, O. A., Sabeti, P. C., Schäffer, D. E., Serres, A., Shapiro, B., Smit, A. F. A., Springer, M., Srinivasan, C., Steiner, C., Storer, J. M., Sullivan, K. A. M., Sullivan, P. F., Sundström, E., Supple, M. A., Swofford, R., Talbot, J.-E., Teeling, E., Turner-Maier, J., Valenzuela, A., Wagner, F., Wallerman, O., Wang, C., Wang, J., Weng, Z., Wilder, A. P., Wirthlin, M. E., Xue, J. R., & Zhang, X.
Affiliations: Department of Microbiology and Immunology, University of California San Francisco, San Francisco, CA 94143, USA.
Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA 94158, USA.
Department of Biological Sciences, Mellon College of Science, Carnegie Mellon University, Pittsburgh, PA 15213, USA.
Department of Computational Biology, School of Computer Science, Carnegie Mellon University, Pittsburgh, PA 15213, USA.
Department of Evolution, Ecology and Organismal Biology, University of California Riverside, Riverside, CA 92521, USA.
School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland.
ORCID: Goodman, Daniel B.
Lind, Abigail L.
Brown, Ashley R.
Springer, Mark S.
Teeling, Emma C.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2023-04-28
Volume: 380
Issue: 6643
ISSN: 0036-8075
1095-9203
DOI: 10.1126/science.abn3943
PMC: PMC10250106
Cited by: 292
References: 30
Language: en

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Evolutionary constraint and innovation across hundreds of placental mammals

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