Abstract
The 2019 United Nations Global assessment report on biodiversity and ecosystem services estimated that approximately 1 million species are at risk of extinction. This primarily human-driven loss of biodiversity has unprecedented negative consequences for ecosystems and people. Classic and emerging approaches in genetics and genomics have the potential to dramatically improve these outcomes. In particular, the study of interactions among genetic loci within and between species will play a critical role in understanding the adaptive potential of species and communities, and hence their direct and indirect effects on biodiversity, ecosystems and people. We explore these population and community genomic contexts in the hope of finding solutions for maintaining and improving ecosystem services and nature’s contributions to people.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Scheffers, B. R. et al. The broad footprint of climate change from genes to biomes to people. Science 354, aaf7671 (2016).
Cadotte, M. W., Carscadden, K. & Mirotchnick, N. Beyond species: functional diversity and the maintenance of ecological processes and services. J. Appl. Ecol. 48, 1079–1087 (2011).
Faith, D. P. et al. Evosystem services: an evolutionary perspective on the links between biodiversity and human well-being. Curr. Opin. Environ. Sustain. 2, 66–74 (2010).
Mimura, M. et al. Understanding and monitoring the consequences of human impacts on intraspecific variation. Evol. Appl. 10, 121–139 (2017).
Rudman, S. M. et al. What genomic data can reveal about eco-evolutionary dynamics. Nat. Ecol. Evol. 2, 9–15 (2018).
Des Roches, S. et al. The ecological importance of intraspecific variation. Nat. Ecol. Evol. 2, 57–64 (2018).
Therkildsen, N. O. et al. Contrasting genomic shifts underlie parallel phenotypic evolution in response to fishing. Science 365, 487–490 (2019).
Crutsinger, G. M. et al. Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313, 966–968 (2006).
Leigh, D. M., Hendry, A. P., Vázquez-Domínguez, E. & Friesen, V. L. Estimated six per cent loss of genetic variation in wild populations since the industrial revolution. Evol. Appl. 12, 1505–1512 (2019).
Boeuf, G. Marine biodiversity characteristics. C. R. Biol. 334, 435–440 (2011).
Loss, S. R., Terwilliger, L. A. & Peterson, A. C. Assisted colonization: integrating conservation strategies in the face of climate change. Biol. Conserv. 144, 92–100 (2011).
Aitken, S. N. & Whitlock, M. C. Assisted gene flow to facilitate local adaptation to climate change. Annu. Rev. Ecol. Evol. Syst. 44, 367–388 (2013).
Witzenberger, K. A. & Hochkirch, A. Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers. Conserv. 20, 1843–1861 (2011).
Novak, B. J. De-extinction. Genes 9, 548 (2018).
Muir, W. M. et al. Genome-wide assessment of worldwide chicken SNP genetic diversity indicates significant absence of rare alleles in commercial breeds. Proc. Natl Acad. Sci. USA 105, 17312–17317 (2008).
Beck, M. W. et al. The global flood protection savings provided by coral reefs. Nat. Commun 9, 2186 (2018).
Millennium Ecosystem Assessment. Ecosystems and Human Well-Being: Synthesis (Island Press, 2005).
Díaz, S. et al. The IPBES conceptual framework — connecting nature and people. Curr. Opin. Environ. Sustain. 14, 1–16 (2015).
Hendry, A. P. Eco-evolutionary Dynamics (Princeton Univ. Press, 2017).
Whitham, T. G. et al. Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84, 559–573 (2003).
Larkin, A. A. & Martiny, A. C. Microdiversity shapes the traits, niche space, and biogeography of microbial taxa. Environ. Microbiol. Rep. 9, 55–70 (2017).
Rodríguez-Verdugo, A., Buckley, J. & Stapley, J. The genomic basis of eco-evolutionary dynamics. Mol. Ecol. 26, 1456–1464 (2017).
Chen, E., Huang, X., Tian, Z., Wing, R. A. & Han, B. The genomics of oryza species provides insights into rice domestication and heterosis. Annu. Rev. Plant. Biol. 70, 639–665 (2019).
Bailey, J. K. et al. Beavers as molecular geneticists: a genetic basis to the foraging of an ecosystem engineer. Ecology 85, 603–608 (2004).
Whitham, T. G. et al. A framework for community and ecosystem genetics: from genes to ecosystems. Nat. Rev. Genet. 7, 510–523 (2006).
Lee, S. M., Jellison, T. & Alper, H. S. Systematic and evolutionary engineering of a xylose isomerase-based pathway in Saccharomyces cerevisiae for efficient conversion yields. Biotechnol. Biofuels 7, 1–8 (2014).
Gleizer, S. et al. Conversion of Escherichia coli to generate all biomass carbon from CO2. Cell 179, 1255–1263.e12 (2019).
Zhu, Y. et al. Genetic diversity and disease control in rice. Nature 406, 718–722 (2000).
King, K. C. & Lively, C. M. Does genetic diversity limit disease spread in natural host populations. Heredity 109, 199–203 (2012).
Robinson, S. J., Samuel, M. D., Johnson, C. J., Adams, M. & McKenzie, D. I. Emerging prion disease drives host selection in a wildlife population. Ecol. Appl. 22, 1050–1059 (2012).
Springbett, A. J., MacKenzie, K., Woolliams, J. A. & Bishop, S. C. The contribution of genetic diversity to the spread of infectious diseases in livestock populations. Genetics 165, 1465–1474 (2003).
McGranahan, N. & Swanton, C. Clonal heterogeneity and tumor evolution: past, present, and the future. Cell 168, 613–628 (2017).
Heap, I. M. The occurrence of herbicide-resistant weeds worldwide. Pestic. Sci. 51, 235–243 (1997).
Whalon, M. E., Mota-Sanchez, D. & Hollingworth, R. M. Global Pesticide Resistance in Arthropods (CABI, 2008).
Hartley, C. J. et al. Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance. Proc. Natl Acad. Sci. USA 103, 8757–8762 (2006).
Dunlop, E. S., Eikeset, A. M. & Stenseth, N. C. From genes to populations: how fisheries-induced evolution alters stock productivity. Ecol. Appl. 25, 1860–1868 (2015).
Waples, R. S. & Audzijonyte, A. Fishery-induced evolution provides insights into adaptive responses of marine species to climate change. Front. Ecol. Environ. 14, 217–224 (2016).
Food and Agriculture Organization of the United Nations. Review of the state of world marine fishery resources (FAO, 2011).
Darimont, C. T. et al. Human predators outpace other agents of trait change in the wild. Proc. Natl Acad. Sci. USA 106, 952–954 (2009).
Philipp, D. P. et al. Fisheries-induced evolution in Largemouth Bass: linking vulnerability to angling, parental care, and fitness. Am. Fish. Soc. Symp. 82, 223–234 (2015).
Philipp, D. P. et al. Selection for vulnerability to angling in largemouth bass. Trans. Am. Fish. Soc. 138, 189–199 (2009).
Pigeon, G., Festa-Bianchet, M., Coltman, D. W. & Pelletier, F. Intense selective hunting leads to artificial evolution in horn size. Evol. Appl. 9, 521–530 (2016).
Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).
Carlson, S. M., Cunningham, C. J. & Westley, P. A. H. Evolutionary rescue in a changing world. Trends Ecol. Evol. 29, 521–530 (2014).
Hendry, A. P., Schoen, D. J., Wolak, M. E. & Reid, J. M. The contemporary evolution of fitness. Annu. Rev. Ecol. Evol. Syst. 49, 457–476 (2018).
Dakos, V. et al. Ecosystem tipping points in an evolving world. Nat. Ecol. Evol. 3, 355–362 (2019).
Souza, F. F. C. et al. Uncovering prokaryotic biodiversity within aerosols of the pristine Amazon forest. Sci. Total Environ. 688, 83–86 (2019).
Suffredini, I. B., Barradas Paciencia, M. L., Varella, A. D. & Younes, R. N. Antibacterial activity of Brazilian Amazon plant extracts. Braz. J. Infect. Dis. 10, 400–402 (2006).
Blanco-Salas, J., Gutiérrez-García, L., Labrador-Moreno, J. & Ruiz-Téllez, T. Wild plants potentially used in human food in the protected area ‘Sierra Grande de Hornachos’ of Extremadura (Spain). Sustainability 11, 456 (2019).
Sam Ma, Z., Li, L. & Zhang, Y. P. Defining individual-level genetic diversity and similarity profiles. Sci. Rep. 10, 5805 (2020).
Avolio, M. L., Beaulieu, J. M., Lo, E. Y. Y. & Smith, M. D. Measuring genetic diversity in ecological studies. Plant. Ecol. 213, 1105–1115 (2012).
Günther, T. & Coop, G. Robust identification of local adaptation from allele frequencies. Genetics 195, 205–220 (2013).
Booker, T. R., Jackson, B. C. & Keightley, P. D. Detecting positive selection in the genome. BMC Biol. 15, 1–10 (2017).
Dawkins, R. The Extended Phenotype – The Gene as the Unit of Selection (Oxford Univ. Press, 1983).
Shuster, S. M., Lonsdorf, E. V., Wimp, G. M., Bailey, J. K. & Whitham, T. G. Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. Evolution 60, 991–1003 (2006).
Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, 1998).
Doudna, J. A. & Charpentier, E. The new frontier of genome engineering with CRISPR-Cas9. Science 346, 1258096 (2014).
Knott, G. J. & Doudna, J. A. CRISPR-Cas guides the future of genetic engineering. Science 361, 866–869 (2018).
Skovmand, L. H. et al. Keystone genes. Trends Ecol. Evol. 33, 689–700 (2018).
Pregitzer, C. C., Bailey, J. K., Hart, S. C. & Schweitzer, J. A. Soils as agents of selection: feedbacks between plants and soils alter seedling survival and performance. Evol. Ecol. 24, 1045–1059 (2010).
Bailey, J. K. et al. From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Phil. Trans. R. Soc. B 364, 1607–1616 (2009).
Davies, C., Ellis, C. J., Iason, G. R. & Ennos, R. A. Genotypic variation in a foundation tree (Populus tremula L.) explains community structure of associated epiphytes. Biol. Lett. 10, 20140190 (2014).
Thompson, T. Q. et al. Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations. Proc. Natl Acad. Sci. USA 116, 177–186 (2019).
Ford, M. D. et al. Reviewing and synthesizing the state of the science regarding associations between adult run timing and specific genotypes in Chinook salmon and steelhead (US Department of Commerce, 2020).
Leroy, C. J. et al. Salmon carcasses influence genetic linkages between forests and streams. Can. J. Fish. Aquat. Sci. 73, 910–920 (2016).
Crutsinger, G. M. et al. Testing a ‘genes-to-ecosystems’ approach to understanding aquatic-terrestrial linkages. Mol. Ecol. 23, 5888–5903 (2014).
Lewontin, R. C. The Genetic Basis of Evolutionary Change (Columbia Univ. Press, 1974).
Csilléry, K., Rodríguez-Verdugo, A., Rellstab, C. & Guillaume, F. Detecting the genomic signal of polygenic adaptation and the role of epistasis in evolution. Mol. Ecol. 27, 606–612 (2018).
Zytynska, S. E., Fleming, S., Tétard-Jones, C., Kertesz, M. A. & Preziosi, R. F. Community genetic interactions mediate indirect ecological effects between a parasitoid wasp and rhizobacteria. Ecology 91, 1563–1568 (2010).
Carroll, S. P., Dingle, H. & Famula, T. R. Rapid appearance of epistasis during adaptive divergence following colonization. Proc. R. Soc. Lond. B 270, S80–S83 (2003).
Carroll, S. P. et al. And the beak shall inherit - evolution in response to invasion. Ecol. Lett. 8, 944–951 (2005).
Doust, A. N. et al. Beyond the single gene: how epistasis and gene-byenvironment effects influence crop domestication. Proc. Natl Acad. Sci. USA 111, 6178–6183 (2014).
Wellenreuther, M., Mérot, C., Berdan, E. & Bernatchez, L. Going beyond SNPs: the role of structural genomic variants in adaptive evolution and species diversification. Mol. Ecol. 28, 1203–1209 (2019).
Ayala, D. et al. Association mapping desiccation resistance within chromosomal inversions in the African malaria vector Anopheles gambiae. Mol. Ecol. 28, 1333–1342 (2019).
Christmas, M. J. et al. Chromosomal inversions associated with environmental adaptation in honeybees. Mol. Ecol. 28, 1358–1374 (2019).
Kess, T. et al. A migration-associated supergene reveals loss of biocomplexity in Atlantic cod. Sci. Adv. 5, eaav2461 (2019).
Berg, P. R. et al. Trans-oceanic genomic divergence of Atlantic cod ecotypes is associated with large inversions. Heredity 119, 418–428 (2017).
Frank, K. T., Petrie, B., Choi, J. S. & Leggett, W. C. Ecology: trophic cascades in a formerly cod-dominated ecosystem. Science 308, 1621–1623 (2005).
Prunier, J. et al. Gene copy number variations involved in balsam poplar (Populus balsamifera L.) adaptive variations. Mol. Ecol. 28, 1476–1490 (2019).
Youngson, N. A. & Whitelaw, E. Transgenerational epigenetic effects. Annu. Rev. Genomics Hum. Genet. 9, 233–257 (2008).
Miura, K. et al. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545–549 (2010).
Ong-Abdullah, M. et al. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525, 533–537 (2015).
Le Luyer, J. et al. Parallel epigenetic modifications induced by hatchery rearing in a Pacific salmon. Proc. Natl Acad. Sci. USA 114, 12964–12969 (2017).
Baerwald, M. R. et al. Migration-related phenotypic divergence is associated with epigenetic modifications in rainbow trout. Mol. Ecol. 25, 1785–1800 (2016).
Oke, K. B. et al. Recent declines in salmon body size impact ecosystems and fisheries. Nat. Commun. 11, 4155 (2020).
Davies, T. J., Urban, M. C., Rayfield, B., Cadotte, M. W. & Peres-Neto, P. R. Deconstructing the relationships between phylogenetic diversity and ecology: a case study on ecosystem functioning. Ecology 97, 2212–2222 (2016).
Cadotte, M. W. Phylogenetic diversity-ecosystem function relationships are insensitive to phylogenetic edge lengths. Funct. Ecol. 29, 718–723 (2015).
Cadotte, M. W. Experimental evidence that evolutionarily diverse assemblages result in higher productivity. Proc. Natl Acad. Sci. USA 110, 8996–9000 (2013).
MacIvor, J. S. et al. Manipulating plant phylogenetic diversity for green roof ecosystem service delivery. Evol. Appl. 11, 2014–2024 (2018).
Clark, J. S., Scher, C. L. & Swift, M. The emergent interactions that govern biodiversity change. Proc. Natl Acad. Sci. USA 117, 17074–17083 (2020).
Crutsinger, G. M. A community genetics perspective: opportunities for the coming decade. N. Phytol. 210, 65–70 (2016).
Zuppinger-Dingley, D. et al. Selection for niche differentiation in plant communities increases biodiversity effects. Nature 515, 108–111 (2014).
van Moorsel, S. J. et al. Community evolution increases plant productivity at low diversity. Ecol. Lett. 21, 128–137 (2018).
Wade, M. J. The co-evolutionary genetics of ecological communities. Nat. Rev. Genet. 8, 185–195 (2007).
Genung, M. A., Bailey, J. K. & Schweitzer, J. A. Welcome to the neighbourhood: Interspecific genotype by genotype interactions in Solidago influence above- and belowground biomass and associated communities. Ecol. Lett. 15, 65–73 (2012).
Genung, M. A., Bailey, J. K. & Schweitzer, J. A. The afterlife of interspecific indirect genetic effects: genotype interactions alter litter quality with consequences for decomposition and nutrient dynamics. PLoS ONE 8, e53718 (2013).
Lankau, R. A. & Nodurft, R. N. An exotic invader drives the evolution of plant traits that determine mycorrhizal fungal diversity in a native competitor. Mol. Ecol. 22, 5472–5485 (2013).
Lankau, R. A., Nuzzo, V., Spyreas, G. & Davis, A. S. Evolutionary limits ameliorate the negative impact of an invasive plant. Proc. Natl Acad. Sci. USA 107, 1253 (2010).
Lankau, R. A. Coevolution between invasive and native plants driven by chemical competition and soil biota. Proc. Natl Acad. Sci. USA 109, 11240–11245 (2012).
Lankau, R. A., Bauer, J. T., Anderson, M. R. & Anderson, R. C. Long-term legacies and partial recovery of mycorrhizal communities after invasive plant removal. Biol. Invasions 16, 1979–1990 (2014).
Miller, E. T., Svanbäck, R. & Bohannan, B. J. M. Microbiomes as metacommunities: understanding host-associated microbes through metacommunity ecology. Trends Ecol. Evol. 33, 926–935 (2018).
Pearse, D. E., Miller, M. R., Abadía-Cardoso, A. & Garza, J. C. Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout. Proc. R. Soc. B 281, 20140012 (2014).
Narum, S. R., Genova, A. D., Micheletti, S. J. & Maass, A. Genomic variation underlying complex life-history traits revealed by genome sequencing in Chinook salmon. Proc. R. Soc. B 285, 20180935 (2018).
Prince, D. J. et al. The evolutionary basis of premature migration in Pacific salmon highlights the utility of genomics for informing conservation. Sci. Adv. 3, e1603198 (2017).
Rey, O. et al. Linking epigenetics and biological conservation: towards a conservation epigenetics perspective. Funct. Ecol. 34, 414–427 (2020).
Hu, J. & Barrett, R. D. H. Epigenetics in natural animal populations. J. Evol. Biol. 30, 1612–1632 (2017).
Herrera, C. M., Medrano, M., Pérez, R., Bazaga, P. & Alonso, C. Within-plant heterogeneity in fecundity and herbivory induced by localized DNA hypomethylation in the perennial herb Helleborus foetidus. Am. J. Bot. 106, 798–806 (2019).
Cohen, S. N., Chang, A. C. Y., Boyer, H. W. & Helling, R. B. Construction of biologically functional bacterial plasmids in vitro (R factor/restriction enzyme/transformation/endonuclease/antibiotic resistance). Proc. Natl Acad. Sci. USA 70, 3240–3244 (1973).
Porteus, M. H. & Carroll, D. Gene targeting using zinc finger nucleases. Nat. Biotechnol. 23, 967–973 (2005).
Urnov, F. D., Rebar, E. J., Holmes, M. C., Zhang, H. S. & Gregory, P. D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11, 636–646 (2010).
Joung, J. K. & Sander, J. D. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 14, 49–55 (2013).
Burt, A. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. R. Soc. Lond. B 270, 921–928 (2003).
Zhang, Y., Massel, K., Godwin, I. D. & Gao, C. Applications and potential of genome editing in crop improvement. Genome Biol. 19, 210 (2018).
Charu, V. & Kaplan, D. L. Silk as a biomaterial. Prog. Polym. Sci. 100, 130–134 (2012).
Mosa, K. A., Saadoun, I., Kumar, K., Helmy, M. & Dhankher, O. P. Potential biotechnological strategies for the cleanup of heavy metals and metalloids. Front. Plant Sci. 7, 303 (2016).
Champer, J., Buchman, A. & Akbari, O. S. Cheating evolution: engineering gene drives to manipulate the fate of wild populations. Nat. Rev. Genet. 17, 146–159 (2016).
Rode, N. O., Estoup, A., Bourguet, D., Courtier-Orgogozo, V. & Débarre, F. Population management using gene drive: molecular design, models of spread dynamics and assessment of ecological risks. Conserv. Genet. 20, 671–690 (2019).
Esvelt, K. M. & Gemmell, N. J. Conservation demands safe gene drive. PLoS Biol. 15, 1–8 (2017).
Phuc, H. et al. Late-acting dominant lethal genetic systems and mosquito control. BMC Biol. 5, 11 (2007).
Campbell, K. J. et al. in Island Invasives: Scaling up to Meet the Challenge (eds Veitch, C. R., Clout, M. N., Martin, A. R., Russel, J. C. & West, C. J.) 6–14 (IUCN, 2019).
Sherkow, J. S. & Greely, H. T. What if extinction is not forever? Science 340, 32–33 (2013).
Otoupal, P. B., Cordell, W. T., Bachu, V., Sitton, M. J. & Chatterjee, A. Multiplexed deactivated CRISPR-Cas9 gene expression perturbations deter bacterial adaptation by inducing negative epistasis. Commun. Biol. 1, 129 (2018).
Kraft, K. et al. Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in mice. Cell Rep. 10, 833–839 (2015).
Springer, N. M. & Schmitz, R. J. Exploiting induced and natural epigenetic variation for crop improvement. Nat. Rev. Genet. 18, 563–575 (2017).
Reinders, J. et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23, 939–950 (2009).
Carrière, Y., Crowder, D. W. & Tabashnik, B. E. Evolutionary ecology of insect adaptation to Bt crops. Evol. Appl. 3, 561–573 (2010).
Fish, D. & Carpenter, S. R. Leaf litter and larval mosquito dynamics in tree-hole ecosystems. Ecology 63, 283–288 (1982).
Kraus, J. M. & Vonesh, J. R. Fluxes of terrestrial and aquatic carbon by emergent mosquitoes: a test of controls and implications for cross-ecosystem linkages. Oecologia 170, 1111–1122 (2012).
Sheehan, S. & Song, Y. S. Deep learning for population genetic inference. PLoS Comput. Biol. 12, e1004845 (2016).
Schrider, D. R. & Kern, A. D. Supervised machine learning for population genetics: a new paradigm. Trends Genet. 34, 301–312 (2018).
Christin, S., Hervet, É. & Lecomte, N. Applications for deep learning in ecology. Methods Ecol. Evol. 10, 1632–1644 (2019).
Desjardins-Proulx, P., Laigle, I., Poisot, T. & Gravel, D. Ecological interactions and the Netflix problem. PeerJ 2017, e3644 (2017).
Ruffley, M., Peterson, K., Week, B., Tank, D. C. & Harmon, L. J. Identifying models of trait-mediated community assembly using random forests and approximate Bayesian computation. Dep. Biol. Sci. https://doi.org/10.1002/ece3.5773 (2019).
Laikre, L. et al. Neglect of genetic diversity in implementation of the convention on biological diversity: conservation in practice and policy. Conserv. Biol. 24, 86–88 (2010).
Hoban, S. et al. Genetic diversity targets and indicators in the CBD post-2020 Global Biodiversity Framework must be improved. Biol. Conserv. 248, 108654 (2020).
Meyer, P. et al. Endogenous and environmental factors influence 35S promoter methylation of a maize A1 gene construct in transgenic petunia and its colour phenotype. Mol. Gen. Genet. 231, 345–352 (1992).
Morandin, L. A. & Winston, M. L. Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol. Appl. 15, 871–881 (2005).
Axelsson, E. P. et al. Leaf litter from insect-resistant transgenic trees causes changes in aquatic insect community composition. J. Appl. Ecol. 48, 1472–1479 (2011).
Axelsson, E. P., Hjältén, J. & LeRoy, C. J. Performance of insect-resistant Bacillus thuringiensis (Bt)-expressing aspens under semi-natural field conditions including natural herbivory in Sweden. For. Ecol. Manage. 264, 167–171 (2012).
Sundström, L. F., Lõhmus, M., Tymchuk, W. E. & Devlin, R. H. Gene-environment interactions influence ecological consequences of transgenic animals. Proc. Natl Acad. Sci. USA 104, 3889–3894 (2007).
Sundström, L. F., Lôhmus, M., Johnsson, J. I. & Devlin, R. H. Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proc. R. Soc. Lond. B 271, 350–352 (2004).
Bodbyl Roels, S. A. & Kelly, J. K. Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65, 2541–2552 (2011).
Cheptou, P. O., Carrue, O., Rouifed, S. & Cantarel, A. Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc. Natl Acad. Sci. USA 105, 3796–3799 (2008).
Polymenakou, P. N. Atmosphere: a source of pathogenic or beneficial microbes? Atmosphere 3, 87–102 (2012).
Collins, S. Many possible worlds: expanding the ecological scenarios in experimental evolution. Evol. Biol. 38, 3–14 (2011).
Archer, D. et al. Atmospheric lifetime of fossil fuel carbon dioxide. Annu. Rev. Earth Planet. Sci. 37, 117–134 (2009).
Sunday, J. M. et al. Evolution in an acidifying ocean. Trends Ecol. Evol. 29, 117–125 (2014).
Harmon, L. J. et al. Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458, 1167–1170 (2009).
Hairston, N. G. et al. Rapid evolution revealed by dormant eggs. Nature 401, 446–446 (1999).
Bothe, H. & Słomka, A. Divergent biology of facultative heavy metal plants. J. Plant Physiol. 219, 45–61 (2017).
Reusch, T. B. H., Ehlers, A., Hammerli, A. & Worm, B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl Acad. Sci. USA 102, 2826–2831 (2005).
Crutsinger, G. M., Souza, L. & Sanders, N. J. Intraspecific diversity and dominant genotypes resist plant invasions. Ecol. Lett. 11, 16–23 (2008).
Pelz, H. J. et al. The genetic basis of resistance to anticoagulants in rodents. Genetics 170, 1839–1847 (2005).
National Research Council. Materials Research to Meet 21st Century Defense Needs (National Academies Press, 2003).
Hutchison, W. D. et al. Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330, 222–225 (2010).
Leale, A. M. & Kassen, R. The emergence, maintenance, and demise of diversity in a spatially variable antibiotic regime. Evol. Lett. 2, 134–143 (2018).
Grant, P. R. & Grant, B. R. Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296, 707–711 (2002).
Grant, P. R. & Grant, B. R. Evolution of character displacement in Darwin’ s finches. Science 313, 224–226 (2006).
Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).
Constantino, V. Instinct extinct: the great pacific flyway. Leonardo 52, 5–11 (2018).
Lewis, B., Grant, W. S., Brenner, R. E. & Hamazaki, T. Changes in size and age of chinook salmon Oncorhynchus tshawytscha returning to Alaska. PLoS ONE 10, 132872 (2015).
Schweitzer, J. A. et al. From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems 11, 1005–1020 (2008).
Díaz, S. et al. Assessing nature’s contributions to people. Science 359, 270–272 (2018). Introduction to the key concept of NCP.
Acknowledgements
The authors thank S. Rudman, V. Glynn, S. van Moorsel, the anonymous reviewers, I. Porth and R. Waples for comments on an earlier version of the manuscript.
Author information
Authors and Affiliations
Contributions
The authors contributed equally to all aspects of the article.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information
Nature Reviews Genetics thanks I. Porth, R. Waples and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Related links
Convention on Biological Diversity Aichi Biodiversity Targets: https://www.cbd.int/sp/targets/
Earth BioGenome Project: https://www.earthbiogenome.org
EpiDiverse European Training Network: https://epidiverse.eu/
Genetic Biocontrol of Invasive Rodents (GBIRd): https://www.geneticbiocontrol.org/
Genome 10K Project: https://genome10k.soe.ucsc.edu
Group on Earth Observations Biodiversity Observation Networks: https://geobon.org/
Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) Global Assessment on Biodiversity and Ecosystem Services: https://www.ipbes.net/global-assessment-report-biodiversity-ecosystem-services
Revive & Restore projects: https://reviverestore.org/projects/
Sustainable Development Goals: https://www.un.org/sustainabledevelopment/sustainable-development-goals/
Vertebrate Genomes Project: https://vertebrategenomesproject.org
Glossary
- Intraspecific genetic variation
-
Variation in alleles of genes within and among populations of the same species.
- Genetic diversity
-
Interspecific and intraspecific genetic variation.
- Contemporary evolution
-
(Also known as rapid evolution). Natural selection that drives adaptive evolution in populations on timescales of less than a few hundred years.
- Gene flow
-
Transfer of genetic variation from one population to another usually via migrating individuals.
- Mutation
-
Change in the DNA sequence.
- Genetic drift
-
Stochastic process altering the genetic variation in a population, usually reducing genetic diversity.
- Population genetics
-
The study of genetic variation and evolutionary history within species using single-gene markers (population genetics) and multigene markers up to full genomes for consideration of structural and epigenetic variation (population genomics).
- Community genetics
-
A community is the sum of populations formed by different species within a particular geographical area. Community genetics and genomics studies the effects of interactions among genomic variation between interacting species. Such interactions are mediated through phenotypes that are determined by heritable genetic variation and environmental influences.
- Extended phenotypes
-
Phenotypes that include effects of genes on the environment, such as an organism’s behaviour or life history, or ecosystem.
- Keystone species
-
A species with a disproportionate ecological effect in an ecosystem. Removal of that species would lead to a drastic change in the ecosystem.
- Evolvability
-
The ability to evolve (that is, to produce genetic diversity on which selection can act).
- Heterozygosity
-
Proportion of sites on the chromosome at which two randomly chosen copies differ in DNA sequence.
- Additive genetic variance
-
The independent genetic effect of an allele on the phenotype of an individual organism resulting in deviation from the population mean phenotype. Additive genetic variance contributes to the evolvability of a population.
- Dominance
-
A genetic interaction between the two alleles at a locus, such that the phenotype of heterozygotes deviates from the average of the two homozygotes.
- Epistasis
-
Non-additive gene–gene interaction. A given allele might function well in one genetic background but poorly in another genetic background. We also refer to interspecific epistasis, in which alleles in different species interact (for example, gene–gene interactions between a native host and a parasite perform differently from an invasive host and the parasite genotype).
- Biocontrol agent
-
In contrast to chemical control agents, biocontrol agents are natural predators or parasites of a pest.
- Epialleles
-
Alternative chromatin states at a given locus, defined with respect to individuals in the population for a given time point and tissue type.
- Population dynamics
-
A population is the sum of all individuals of the same species within a defined geographical area. Its dynamics are described as changes in the demographics of a given population (for example, age, composition or size) driven by biological and environmental factors.
- Character displacement
-
Phenotypically (in a trait or ecological niche) similar but geographically or temporally co-occurring species diverge in the trait to minimize interspecific competition.
- Allelopathic compound
-
As part of a plant’s defence mechanism, lethal biochemical compounds are released into the soil to suppress neighbouring organisms.
- Mycorrhizal
-
A term describing the symbiotic interaction between a fungus and a plant’s rhizosphere.
- Microbiome
-
The totality of microorganisms, their genetic information and the milieu in which they interact to perform a specific function.
- Gene drives
-
Genetically engineered, synthetic genetic elements designed to increase in frequency over time in a population to propagate a certain gene variant.
- Deep learning
-
A subdiscipline of machine learning, with the difference that no training data set is needed. The artificial neural network recognizes patterns from coarse to fine scale in multiple steps, so-called hidden layers, which compute increasingly more complex features by taking the results of preceding operations as input.
Rights and permissions
About this article
Cite this article
Stange, M., Barrett, R.D.H. & Hendry, A.P. The importance of genomic variation for biodiversity, ecosystems and people. Nat Rev Genet 22, 89–105 (2021). https://doi.org/10.1038/s41576-020-00288-7
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41576-020-00288-7
This article is cited by
-
Genomics for monitoring and understanding species responses to global climate change
Nature Reviews Genetics (2024)
-
Haplotype-resolved assemblies and variant benchmark of a Chinese Quartet
Genome Biology (2023)
-
Performance analysis of conventional and AI-based variant callers using short and long reads
BMC Bioinformatics (2023)
-
Global determinants of insect mitochondrial genetic diversity
Nature Communications (2023)
-
Ecosystem services provided by fungi in freshwaters: a wake-up call
Hydrobiologia (2023)