Genetic diversity loss in the Anthropocene

Exposito-Alonso, Moises; Booker, Tom R.; Czech, Lucas; Gillespie, Lauren; Hateley, Shannon; Kyriazis, Christopher C.; Lang, Patricia L.  M.; Leventhal, Laura; Nogues-Bravo, David; Pagowski, Veronica; Ruffley, Megan; Spence, Jeffrey P.; Toro Arana, Sebastian E.; Weiß, Clemens L.; Zess, Erin

doi:10.1126/science.abn5642

Genetic diversity loss in the Anthropocene

Journal Article · Fri Sep 23 04:00:00 EDT 2022 · Science

DOI:https://doi.org/10.1126/science.abn5642· OSTI ID:1980743

^[1]; ^[2]; ^[3]; ^[4]; ^[3]; Kyriazis, Christopher C. ^[5]; ^[6]; ^[7]; ^[8]; Pagowski, Veronica ^[6]; ^[3]; ^[9]; ^[7]; ^[9]; ^[3]

Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.; Department of Biology, Stanford University, Stanford, CA 94305, USA.; Department of Global Ecology, Carnegie Institution for Science, Stanford, CA 94305, USA.; OSTI
Department of Zoology, University of British Columbia, Vancouver, Canada.; Biodiversity Research Centre, University of British Columbia, Vancouver, Canada.
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.; Department of Computer Science, Stanford University, Stanford, CA 94305, USA.
Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA.
Department of Biology, Stanford University, Stanford, CA 94305, USA.
Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.; Department of Biology, Stanford University, Stanford, CA 94305, USA.
Center for Macroecology, Evolution and Climate, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
Department of Genetics, Stanford University, Stanford, CA 94305, USA.

Anthropogenic habitat loss and climate change are reducing species’ geographic ranges, increasing extinction risk and losses of species’ genetic diversity. Although preserving genetic diversity is key to maintaining species’ adaptability, we lack predictive tools and global estimates of genetic diversity loss across ecosystems. We introduce a mathematical framework that bridges biodiversity theory and population genetics to understand the loss of naturally occurring DNA mutations with decreasing habitat. By analyzing genomic variation of 10,095 georeferenced individuals from 20 plant and animal species, we show that genome-wide diversity follows a mutations-area relationship power law with geographic area, which can predict genetic diversity loss from local population extinctions. We estimate that more than 10% of genetic diversity may already be lost for many threatened and nonthreatened species, surpassing the United Nations’ post-2020 targets for genetic preservation.

Research Organization:: Illinois State University (ISU), Normal, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0021286

OSTI ID:: 1980743

Journal Information:: Science, Journal Name: Science Journal Issue: 6613 Vol. 377; ISSN 0036-8075

Publisher:: AAAS

Country of Publication:: United States

Language:: English

References (74)

Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s Paradox Buffalo, Vince eLife, Vol. 10 https://doi.org/10.7554/eLife.67509	journal	August 2021
Ecological and Evolutionary Responses to Recent Climate Change Parmesan, Camille Annual Review of Ecology, Evolution, and Systematics, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.ecolsys.37.091305.110100	journal	December 2006
Spontaneous Mutation Accumulation Studies in Evolutionary Genetics Halligan, Daniel L.; Keightley, Peter D. Annual Review of Ecology, Evolution, and Systematics, Vol. 40, Issue 1 https://doi.org/10.1146/annurev.ecolsys.39.110707.173437	journal	December 2009
Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass Lovell, John T.; MacQueen, Alice H.; Mamidi, Sujan Nature, Vol. 590, Issue 7846 https://doi.org/10.1038/s41586-020-03127-1	journal	January 2021
Pervasive human-driven decline of life on Earth points to the need for transformative change Díaz, Sandra; Settele, Josef; Brondízio, Eduardo S. Science, Vol. 366, Issue 6471 https://doi.org/10.1126/science.aax3100	journal	December 2019
Mutation Accumulation and the Extinction of Small Populations Lynch, Michael; Conery, John; Burger, Reinhard The American Naturalist, Vol. 146, Issue 4 https://doi.org/10.1086/285812	journal	October 1995
Universal species–area and endemics–area relationships at continental scales Storch, David; Keil, Petr; Jetz, Walter Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11226	journal	June 2012
The Commonness, And Rarity, of Species Preston, F. W. Ecology, Vol. 29, Issue 3 https://doi.org/10.2307/1930989	journal	July 1948
Evolutionary biochemistry: revealing the historical and physical causes of protein properties Harms, Michael J.; Thornton, Joseph W. Nature Reviews Genetics, Vol. 14, Issue 8 https://doi.org/10.1038/nrg3540	journal	July 2013
Rivets and Redundancy Ehrlich, Paul; Walker, Brian BioScience, Vol. 48, Issue 5 https://doi.org/10.2307/1313377	journal	May 1998
Linking climate niches across seasons to assess population vulnerability in a migratory bird Ruegg, Kristen; Anderson, Eric C.; Somveille, Marius Global Change Biology, Vol. 27, Issue 15 https://doi.org/10.1111/gcb.15639	journal	May 2021
Efficient pedigree recording for fast population genetics simulation Kelleher, Jerome; Thornton, Kevin R.; Ashander, Jaime PLOS Computational Biology, Vol. 14, Issue 11 https://doi.org/10.1371/journal.pcbi.1006581	journal	November 2018
Harmonization of global land use change and management for the period 850–2100 (LUH2) for CMIP6 Hurtt, George C.; Chini, Louise; Sahajpal, Ritvik Geoscientific Model Development, Vol. 13, Issue 11 https://doi.org/10.5194/gmd-13-5425-2020	journal	January 2020
Rebuilding community ecology from functional traits Mcgill, B.; Enquist, B.; Weiher, E. Trends in Ecology & Evolution, Vol. 21, Issue 4 https://doi.org/10.1016/j.tree.2006.02.002	journal	April 2006
No saturation in the accumulation of alien species worldwide Seebens, Hanno; Blackburn, Tim M.; Dyer, Ellie E. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14435	journal	February 2017
Sampling Hubbell's neutral theory of biodiversity: Sampling neutral theory Alonso, David; McKane, Alan J. Ecology Letters, Vol. 7, Issue 10 https://doi.org/10.1111/j.1461-0248.2004.00640.x	journal	August 2004
Whole‐genome analyses provide no evidence for dog introgression in Fennoscandian wolf populations Smeds, Linnéa; Aspi, Jouni; Berglund, Jonas Evolutionary Applications, Vol. 14, Issue 3 https://doi.org/10.1111/eva.13151	journal	November 2020
sars: an R package for fitting, evaluating and comparing species–area relationship models Matthews, Thomas J.; Triantis, Kostas A.; Whittaker, Robert J. Ecography, Vol. 42, Issue 8 https://doi.org/10.1111/ecog.04271	journal	April 2019
Extinction risk from climate change Thomas, Chris D.; Cameron, Alison; Green, Rhys E. Nature, Vol. 427, Issue 6970 https://doi.org/10.1038/nature02121	journal	January 2004
Changes in plant species richness due to land use and nitrogen deposition across the globe Gallego‐Zamorano, Juan; Huijbregts, Mark A. J.; Schipper, Aafke M. Diversity and Distributions, Vol. 28, Issue 4 https://doi.org/10.1111/ddi.13476	journal	January 2022
The crucial role of genome-wide genetic variation in conservation Kardos, Marty; Armstrong, Ellie E.; Fitzpatrick, Sarah W. Proceedings of the National Academy of Sciences, Vol. 118, Issue 48 https://doi.org/10.1073/pnas.2104642118	journal	November 2021
Population genomic and historical analysis suggests a global invasion by bridgehead processes in Mimulus guttatus Vallejo-Marín, Mario; Friedman, Jannice; Twyford, Alex D. Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-01795-x	journal	March 2021
Genomic signals of selection predict climate-driven population declines in a migratory bird Bay, Rachael A.; Harrigan, Ryan J.; Underwood, Vinh Le Science, Vol. 359, Issue 6371 https://doi.org/10.1126/science.aan4380	journal	January 2018
Drivers of linkage disequilibrium across a species’ geographic range Lucek, Kay; Willi, Yvonne PLOS Genetics, Vol. 17, Issue 3 https://doi.org/10.1371/journal.pgen.1009477	journal	March 2021
Countryside Species–Area Relationship as a Valid Alternative to the Matrix‐Calibrated Species–Area Model Pereira, Henrique Miguel; Ziv, Guy; Miranda, Murilo Conservation Biology, Vol. 28, Issue 3 https://doi.org/10.1111/cobi.12289	journal	March 2014
The Canonical Distribution of Commonness and Rarity: Part I Preston, F. W. Ecology, Vol. 43, Issue 2 https://doi.org/10.2307/1931976	journal	April 1962
Tree‐sequence recording in SLiM opens new horizons for forward‐time simulation of whole genomes Haller, Benjamin C.; Galloway, Jared; Kelleher, Jerome Molecular Ecology Resources, Vol. 19, Issue 2 https://doi.org/10.1111/1755-0998.12968	journal	February 2019
The ultimate and proximate mechanisms driving the evolution of long tails in forest deer mice Kingsley, Evan P.; Kozak, Krzysztof M.; Pfeifer, Susanne P. Evolution, Vol. 71, Issue 2 https://doi.org/10.1111/evo.13150	journal	December 2016
Genetic Diversity–Area Relationships across Bird Species Fan (樊海英), Haiying; Zhang (张清臣), Qingchen; Rao (饶娟娟), Juanjuan The American Naturalist, Vol. 194, Issue 5 https://doi.org/10.1086/705346	journal	November 2019
The Relation Between the Number of Species and the Number of Individuals in a Random Sample of an Animal Population Fisher, R. A.; Corbet, A. Steven; Williams, C. B. The Journal of Animal Ecology, Vol. 12, Issue 1 https://doi.org/10.2307/1411	journal	May 1943
Planetary boundaries: Guiding human development on a changing planet Steffen, W.; Richardson, K.; Rockstrom, J. Science, Vol. 347, Issue 6223 https://doi.org/10.1126/science.1259855	journal	January 2015
Climate-Related Local Extinctions Are Already Widespread among Plant and Animal Species Wiens, John J. PLOS Biology, Vol. 14, Issue 12 https://doi.org/10.1371/journal.pbio.2001104	journal	December 2016
Species–area relationships always overestimate extinction rates from habitat loss He, Fangliang; Hubbell, Stephen P. Nature, Vol. 473, Issue 7347 https://doi.org/10.1038/nature09985	journal	May 2011
A Roadmap for Understanding the Evolutionary Significance of Structural Genomic Variation Mérot, Claire; Oomen, Rebekah A.; Tigano, Anna Trends in Ecology & Evolution, Vol. 35, Issue 7 https://doi.org/10.1016/j.tree.2020.03.002	journal	July 2020
No consistent effects of humans on animal genetic diversity worldwide Millette, Katie L.; Fugère, Vincent; Debyser, Chloé Ecology Letters, Vol. 23, Issue 1 https://doi.org/10.1111/ele.13394	journal	October 2019
The qtn Program and the Alleles that Matter for Evolution: all That'S gold does not Glitter Rockman, Matthew V. Evolution, Vol. 66, Issue 1 https://doi.org/10.1111/j.1558-5646.2011.01486.x	journal	November 2011
Drosophila Evolution over Space and Time (DEST): A New Population Genomics Resource Kapun, Martin; Nunez, Joaquin C. B.; Bogaerts-Márquez, María Molecular Biology and Evolution, Vol. 38, Issue 12 https://doi.org/10.1093/molbev/msab259	journal	September 2021
Population genetics of the coral Acropora millepora : Toward genomic prediction of bleaching Fuller, Zachary L.; Mocellin, Veronique J. L.; Morris, Luke A. Science, Vol. 369, Issue 6501 https://doi.org/10.1126/science.aba4674	journal	July 2020
Population genomics of divergence within an obligate pollination mutualism: Selection maintains differences between Joshua tree species Royer, Anne M.; Streisfeld, Matthew A.; Smith, Christopher Irwin American Journal of Botany, Vol. 103, Issue 10 https://doi.org/10.3732/ajb.1600069	journal	September 2016
Estimated six per cent loss of genetic variation in wild populations since the industrial revolution Leigh, Deborah M.; Hendry, Andrew P.; Vázquez‐Domínguez, Ella Evolutionary Applications, Vol. 12, Issue 8 https://doi.org/10.1111/eva.12810	journal	June 2019
Modeling Biodiversity Dynamics in Countryside Landscapes Pereira, Henrique M.; Daily, Gretchen C. Ecology, Vol. 87, Issue 8 https://doi.org/10.1890/0012-9658(2006)87[1877:MBDICL]2.0.CO;2	journal	August 2006
Natural selection on the Arabidopsis thaliana genome in present and future climates Exposito-Alonso, Moises; Burbano, Hernán A.; Bossdorf, Oliver Nature, Vol. 573, Issue 7772 https://doi.org/10.1038/s41586-019-1520-9	journal	August 2019
Landscape genomic prediction for restoration of a Eucalyptus foundation species under climate change Supple, Megan Ann; Bragg, Jason G.; Broadhurst, Linda M. eLife, Vol. 7 https://doi.org/10.7554/eLife.31835	journal	April 2018
Efficient Coalescent Simulation and Genealogical Analysis for Large Sample Sizes Kelleher, Jerome; Etheridge, Alison M.; McVean, Gilean PLOS Computational Biology, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pcbi.1004842	journal	May 2016
Post-2020 goals overlook genetic diversity Laikre, Linda; Hoban, Sean; Bruford, Michael W. Science, Vol. 367, Issue 6482 https://doi.org/10.1126/science.abb2748	journal	March 2020
Global trade will accelerate plant invasions in emerging economies under climate change Seebens, Hanno; Essl, Franz; Dawson, Wayne Global Change Biology, Vol. 21, Issue 11 https://doi.org/10.1111/gcb.13021	journal	September 2015
Estimation of levels of gene flow from DNA sequence data. Hudson, R. R.; Slatkin, M.; Maddison, W. P. Genetics, Vol. 132, Issue 2 https://doi.org/10.1093/genetics/132.2.583	journal	October 1992
A population genetic interpretation of GWAS findings for human quantitative traits Simons, Yuval B.; Bullaughey, Kevin; Hudson, Richard R. PLOS Biology, Vol. 16, Issue 3 https://doi.org/10.1371/journal.pbio.2002985	journal	March 2018
A unified model of species abundance, genetic diversity, and functional diversity reveals the mechanisms structuring ecological communities Overcast, Isaac; Ruffley, Megan; Rosindell, James Molecular Ecology Resources, Vol. 21, Issue 8 https://doi.org/10.1111/1755-0998.13514	journal	October 2021
Epistasis and environmental heterogeneity in the speciation process Campos, Paulo R. A.; de Oliveira, Viviane M.; Rosas, Alexandre Ecological Modelling, Vol. 221, Issue 21 https://doi.org/10.1016/j.ecolmodel.2010.07.023	journal	October 2010
The coalescent Kingman, J. F. C. Stochastic Processes and their Applications, Vol. 13, Issue 3 https://doi.org/10.1016/0304-4149(82)90011-4	journal	September 1982
Exposure of mammal genetic diversity to mid‐21st century global change Theodoridis, Spyros; Rahbek, Carsten; Nogues‐Bravo, David Ecography, Vol. 44, Issue 6 https://doi.org/10.1111/ecog.05588	journal	March 2021
The Future of Biodiversity Pimm, S. L.; Russell, G. J.; Gittleman, J. L. Science, Vol. 269, Issue 5222 https://doi.org/10.1126/science.269.5222.347	journal	July 1995
1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana Alonso-Blanco, Carlos; Andrade, Jorge; Becker, Claude Cell, Vol. 166, Issue 2 https://doi.org/10.1016/j.cell.2016.05.063	journal	July 2016
Targeted capture and resequencing of 1040 genes reveal environmentally driven functional variation in grey wolves Schweizer, Rena M.; Robinson, Jacqueline; Harrigan, Ryan Molecular Ecology, Vol. 25, Issue 1 https://doi.org/10.1111/mec.13467	journal	December 2015
Set ambitious goals for biodiversity and sustainability Díaz, Sandra; Zafra-Calvo, Noelia; Purvis, Andy Science, Vol. 370, Issue 6515 https://doi.org/10.1126/science.abe1530	journal	October 2020
Do bottlenecks increase additive genetic variance? Taft, Heather R.; Roff, Derek A. Conservation Genetics, Vol. 13, Issue 2 https://doi.org/10.1007/s10592-011-0285-y	journal	November 2011
A global reference for human genetic variation Consortium, The 1000 Genomes Project; Auton, Adam; Abecasis, Gonçalo R. Nature, Vol. 526, Issue 7571, p. 68-74 https://doi.org/10.1038/nature15393	journal	January 2015
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe The American Journal of Human Genetics, Vol. 81, Issue 3 https://doi.org/10.1086/519795	journal	September 2007
Global habitat loss and extinction risk of terrestrial vertebrates under future land-use-change scenarios Powers, Ryan P.; Jetz, Walter Nature Climate Change, Vol. 9, Issue 4 https://doi.org/10.1038/s41558-019-0406-z	journal	March 2019
Species and Area Arrhenius, Olof The Journal of Ecology, Vol. 9, Issue 1 https://doi.org/10.2307/2255763	journal	September 1921
Isolation by Distance Wright, Sewall Genetics, Vol. 28, Issue 2 https://doi.org/10.1093/genetics/28.2.114	journal	March 1943
Multiple modes of convergent adaptation in the spread of glyphosate-resistant Amaranthus tuberculatus Kreiner, Julia M.; Giacomini, Darci Ann; Bemm, Felix Proceedings of the National Academy of Sciences, Vol. 116, Issue 42 https://doi.org/10.1073/pnas.1900870116	journal	September 2019
The rate and potential relevance of new mutations in a colonizing plant lineage Exposito-Alonso, Moises; Becker, Claude; Schuenemann, Verena J. PLOS Genetics, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pgen.1007155	journal	February 2018
Conserving biodiversity under climate change: the rear edge matters: Rear edges and climate change Hampe, Arndt; Petit, Rémy J. Ecology Letters, Vol. 8, Issue 5 https://doi.org/10.1111/j.1461-0248.2005.00739.x	journal	March 2005
Most species are not driven to extinction before genetic factors impact them Spielman, D.; Brook, B. W.; Frankham, R. Proceedings of the National Academy of Sciences, Vol. 101, Issue 42 https://doi.org/10.1073/pnas.0403809101	journal	October 2004
XVII.—The Distribution of Gene Ratios for Rare Mutations Fisher, R. A. Proceedings of the Royal Society of Edinburgh, Vol. 50 https://doi.org/10.1017/S0370164600044886	journal	January 1931
Interpreting principal component analyses of spatial population genetic variation Novembre, John; Stephens, Matthew Nature Genetics, Vol. 40, Issue 5 https://doi.org/10.1038/ng.139	journal	April 2008
Niche Apportionment or Random Assortment: Species Abundance Patterns Revisited Tokeshi, Mutsunori The Journal of Animal Ecology, Vol. 59, Issue 3 https://doi.org/10.2307/5036	journal	October 1990
The age of a mutation in a general coalescent tree Griffiths, R. C.; Tavaré, Simon Communications in Statistics. Stochastic Models, Vol. 14, Issue 1-2 https://doi.org/10.1080/15326349808807471	journal	January 1998
SLiM 3: Forward Genetic Simulations Beyond the Wright–Fisher Model Haller, Benjamin C.; Messer, Philipp W. Molecular Biology and Evolution, Vol. 36, Issue 3 https://doi.org/10.1093/molbev/msy228	journal	January 2019
Geographic patterns of genomic diversity and structure in the C4 grass Panicum hallii across its natural distribution Palacio-Mejía, Juan Diego; Grabowski, Paul P.; Ortiz, Edgardo M. AoB PLANTS, Vol. 13, Issue 2 https://doi.org/10.1093/aobpla/plab002	journal	January 2021
Genomic insights into the conservation status of the world’s last remaining Sumatran rhinoceros populations von Seth, Johanna; Dussex, Nicolas; Díez-del-Molino, David Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-22386-8	journal	April 2021
Genome-wide shifts in climate-related variation underpin responses to selective breeding in a widespread conifer MacLachlan, Ian R.; McDonald, Tegan K.; Lind, Brandon M. Proceedings of the National Academy of Sciences, Vol. 118, Issue 10 https://doi.org/10.1073/pnas.2016900118	journal	March 2021

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