Over two thousand plant species have been modified morphologically through cultivation and human use. Here, we review three aspects of crop domestication that are currently undergoing marked revisions, due to analytical advancements and their application to whole genome resequencing (WGS) data. We begin by discussing the duration and demographic history of domestication. There has been debate as to whether domestication occurred quickly or slowly. The latter is tentatively supported both by fossil data and application of WGS data to sequentially Markovian coalescent methods that infer the history of effective population size. This history suggests the possibility of extended human impacts on domesticated lineages prior to their purposeful cultivation. We also make the point that demographic history matters, because it shapes patterns and levels of extant genetic diversity. We illustrate this point by discussing the evolutionary processes that contribute to the empirical observation that most crops examined to date have more putatively deleterious alleles than their wild relatives. These deleterious alleles may contribute to genetic load within crops and may be fitting targets for crop improvement. Finally, the same demographic factors are likely to shape the spectrum of structural variants (SVs) within crops. SVs are known to underlie many of the phenotypic changes associated with domestication and crop improvement, but we currently lack sufficient knowledge about the mechanisms that create SVs, their rates of origin, their population frequencies and their phenotypic effects.
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Gaut, B. S., Díez, C. M. & Morrell, P. L. Genomics and the contrasting dynamics of annual and perennial domestication. Trends Genet. 31, 709–719 (2015).
Hammer, K. Das domestikationssyndrom. Kulturpflanze 32, 11–34 (1984).
Gerbault, P. et al. Storytelling and story testing in domestication. Proc. Natl. Acad. Sci. USA 111, 6159–6164 (2014).
Lu, J. et al. The accumulation of deleterious mutations in rice genomes: a hypothesis on the cost of domestication. Trends Genet. 22, 126–131 (2006).
Meyer, R. S. & Purugganan, M. D. Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 840–852 (2013).
Miller, A. J. & Gross, B. L. From forest to field: perennial fruit crop domestication. Am. J. Bot. 98, 1389–1414 (2011).
Doebley, J. in Isozymes in plant biology (eds Soltis, D. E. & Soltis, P. S.) 165–191 (Chapman and Hall, London, 1989).
Eyre-Walker, A., Gaut, R. L., Hilton, H., Feldman, D. L. & Gaut, B. S. Investigation of the bottleneck leading to the domestication of maize. Proc. Natl. Acad. Sci. USA 95, 4441–4446 (1998).
Hillman, G. C. & Davies, M. S. Domestication rates in wild-type wheats and barley under primitive cultivation. Biol. J. Linn. Soc. 39, 39–78 (1990).
Ladizinsky, G. Pulse domestication before cultivation. Econ. Bot. 41, 60–65 (1987).
Harlan, J. R., de Wet, J. M. J. & Price, E. G. Comparative evolution of cereals. Evolution 27, 311–325 (1973).
Hillman, G. C. & Davies, M. S. Measured domestication rates in wild wheats and barley under primative cultivation and their archaelogical implications. J. World Prehist. 4, 157–222 (1990).
Zhang, L. B. et al. Selection on grain shattering genes and rates of rice domestication. New Phytol. 184, 708–720 (2009).
Li, C., Zhou, A. & Sang, T. Rice domestication by reducing shattering. Science 311, 1936–1939 (2006).
Wright, S. I. et al. The effects of artificial selection on the maize genome. Science 308, 1310–1314 (2005).
Zhu, Q., Zheng, X., Luo, J., Gaut, B. S. & Ge, S. Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol. Biol. Evol. 24, 875–888 (2007).
Molina, J. et al. Molecular evidence for a single evolutionary origin of domesticated rice. Proc. Natl. Acad. Sci. USA 108, 8351–8356 (2011).
Beissinger, T. M. et al. Recent demography drives changes in linked selection across the maize genome. Nat. Plants 2, 16084 (2016).
Caicedo, A. L. et al. Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet. 3, 1745–1756 (2007).
Purugganan, M. D. & Fuller, D. Q. The nature of selection during plant domestication. Nature 457, 843–848 (2009).
Purugganan, M. D. & Fuller, D. Q. Archaeological data reveal slow rates of evolution during plant domestication. Evolution 65, 171–183 (2011).
Allaby, R. G., Stevens, C., Lucas, L., Maeda, O. & Fuller, D. Q. Geographic mosaics and changing rates of cereal domestication. Philos. T. Roy. Soc. B 372, 20160429 (2017).
Ishikawa, R. et al. Allelic interaction at seed-shattering loci in the genetic backgrounds of wild and cultivated rice species. Genes Genet. Syst. 85, 265–271 (2010).
Ishii, T. et al. OsLG1 regulates a closed panicle trait in domesticated rice. Nat. Genet. 45, 462–465 (2013).
Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011).
Schiffels, S. & Durbin, R. Inferring human population size and separation history from multiple genome sequences. Nat. Genet. 46, 919–925 (2014).
Terhorst, J., Kamm, J. A. & Song, Y. S. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat. Genet. 49, 303–309 (2017).
Velasco, D., Hough, J., Aradhya, M. & Ross-Ibarra, J. Evolutionary genomics of peach and almond domestication. G3-Genes Genom. Genet. 6, 3985–3993 (2016).
Wang, L. et al. The interplay of demography and selection during maize domestication and expansion. Genome Biol. 18, 215 (2017).
Meyer, R. S. et al. Domestication history and geographical adaptation inferred from a SNP map of African rice. Nat. Genet. 48, 1083–1088 (2016).
Zhou, Y., Massonnet, M., Sanjak, J. S., Cantu, D. & Gaut, B. S. Evolutionary genomics of grape (Vitis vinifera ssp. vinifera) domestication. Proc. Natl. Acad. Sci. USA 114, 11715–11720 (2017).
Adler, D. S. & Tushabramishvili, N. in Settlement Dynamics of the Middle Palaeolithic and Middle Stone Age Vol. 2 (ed. Conard, N. J.) Ch. 5 (Kerns Verlag, Tubingen, 2004).
Nielsen, R. & Beaumont, M. A. Statistical inferences in phylogeography. Mol. Ecol. 18, 1034–1047 (2009).
Mazet, O., Rodríguez, W., Grusea, S., Boitard, S. & Chikhi, L. On the importance of being structured: instantaneous coalescence rates and human evolution–lessons for ancestral population size inference. Heredity 116, 362–371 (2016).
Schrider, D. R., Shanku, A. G. & Kern, A. D. Effects of linked selective sweeps on demographic inference and model selection. Genetics 204, 1207–1223 (2016).
Roberts, P., Hunt, C., Arroyo-Kalin, M., Evans, D. & Boivin, N. The deep human prehistory of global tropical forests and its relevance for modern conservation. Nat. Plants 3, 17093 (2017).
Boivin, N. L. et al. Ecological consequences of human niche construction: Examining long-term anthropogenic shaping of global species distributions. Proc. Natl. Acad. Sci. USA 113, 6388–6396 (2016).
Moyers, B. T., Morrell, P. L. & McKay, J. K. Genetic costs of domestication and improvement. J. Hered. 109, 103–116 (2017).
Hedrick, P. W. & Garcia-Dorado, A. Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol. Evol. 31, 940–952 (2016).
Charlesworth, D. & Willis, J. H. The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796 (2009).
Chun, S. & Fay, J. C. Evidence for hitchhiking of deleterious mutations within the human genome. PLoS Genet. 7, e1002240 (2011).
Charlesworth, B. The role of background selection in shaping patterns of molecular evolution and variation: evidence from variability on the Drosophila X chromosome. Genetics 191, 233–246 (2012).
Eyre-Walker, A. & Keightley, P. D. The distribution of fitness effects of new mutations. Nat. Rev. Genet. 8, 610–618 (2007).
Liu, Q., Zhou, Y., Morrell, P. L. & Gaut, B. S. Deleterious variants in Asian rice and the potential cost of domestication. Mol. Biol. Evol. 34, 908–924 (2017).
Arunkumar, R., Ness, R. W., Wright, S. I. & Barrett, S. C. The evolution of selfing is accompanied by reduced efficacy of selection and purging of deleterious mutations. Genetics 199, 817–829 (2015).
Ohta, T. The nearly neutral model of molecular evolution. Annu. Rev. Ecol. Syst. 23, 263–286 (1992).
Casals, F. et al. Whole-exome sequencing reveals a rapid change in the frequency of rare functional variants in a founding population of humans. PLoS Genet 9, e1003815 (2013).
Lohmueller, K. E. The distribution of deleterious genetic variation in human populations. Curr. Opin. Genet. Dev. 29, 139–146 (2014).
Lohmueller, K. E. et al. Proportionally more deleterious genetic variation in European than in African populations. Nature 451, 994–997 (2008).
Simons, Y. B., Turchin, M. C., Pritchard, J. K. & Sella, G. The deleterious mutation load is insensitive to recent population history. Nat. Genet. 46, 220–224 (2014).
Marsden, C. D. et al. Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs. Proc. Natl. Acad. Sci. USA 113, 152–157 (2016).
Balick, D. J., Do, R., Cassa, C. A., Reich, D. & Sunyaev, S. R. Dominance of deleterious alleles controls the response to a population bottleneck. PLoS Genet. 11, e1005436 (2015).
Choi, Y., Sims, G. E., Murphy, S., Miller, J. R. & Chan, A. P. Predicting the functional effect of amino acid substitutions and indels. PLoS ONE 7, e46688 (2012).
Ng, P. C. & Henikoff, S. SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res. 31, 3812–3814 (2003).
Davydov, E. V. et al. Identifying a high fraction of the human genome to be under selective constraint using GERP++. PLoS Comput. Biol. 6, e1001025 (2010).
Kono, T. J. Y. et al. Comparative genomics approaches accurately predict deleterious variants in plants. bioRxiv https://doi.org/10.1101/112318 (2018).
Kono, T. J. et al. The role of deleterious substitutions in crop genomes. Mol. Biol. Evol. 33, 2307–2317 (2016).
Renaut, S. & Rieseberg, L. H. The accumulation of deleterious mutations as a consequence of domestication and improvement in sunflowers and other composite crops. Mol. Biol. Evol. 32, 2273–2283 (2015).
Ramu, P. et al. Cassava haplotype map highlights fixation of deleterious mutations during clonal propagation. Nat. Genet. 49, 959–963 (2017).
Brandvain, Y. & Wright, S. I. The limits of natural selection in a nonequilibrium world. Trends Genet. 32, 201–210 (2016).
Kirkpatrick, M. & Jarne, P. The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155, 154–167 (2000).
Henn, B. M. et al. Distance from sub-Saharan Africa predicts mutational load in diverse human genomes. Proc. Natl. Acad. Sci. USA 113, 440–449 (2016).
Morrell, P. L., Buckler, E. S. & Ross-Ibarra, J. Crop genomics: advances and applications. Nat. Rev. Genet. 13, 85–96 (2011).
Kremling, K. A. G. et al. Dysregulation of expression correlates with rare-allele burden and fitness loss in maize. Nature 555, 520–523 (2018).
Mezmouk, S. & Ross-Ibarra, J. The pattern and distribution of deleterious mutations in maize. G3-Genes Genom. Genet. 4, 163–171 (2014).
Yang, J. et al. Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize. PLoS Genet. 13, e1007019 (2017).
Rodgers-Melnick, E. et al. Recombination in diverse maize is stable, predictable, and associated with genetic load. Proc. Natl. Acad. Sci. USA 112, 3823–3828 (2015).
Wang, H., Vieira, F. G., Crawford, J. E., Chu, C. & Nielsen, R. Asian wild rice is a hybrid swarm with extensive gene flow and feralization from domesticated rice. Genome Res. 27, 1029–1038 (2017).
Diez, C. M. et al. Olive domestication and diversification in the Mediterranean Basin. New Phytol. 206, 436–447 (2015).
Cornille, A. et al. New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genet. 8, e1002703 (2012).
Duan, N. et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat. Commun. 8, 249 (2017).
Hufford, M. B. et al. The genomic signature of crop-wild introgression in maize. PLoS Genet. 9, e1003477 (2013).
Swarts, K. et al. Genomic estimation of complex traits reveals ancient maize adaptation to temperate North America. Science 357, 512–515 (2017).
Wang, M. et al. Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication. Nat. Genet. 49, 579–587 (2017).
Cheng, F. et al. Genome resequencing and comparative variome analysis in a Brassica rapa and Brassica oleracea collection. Sci. Data 3, 160119 (2016).
Cao, K. et al. Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol. 15, 415 (2014).
Hazzouri, K. M. et al. Whole genome re-sequencing of date palms yields insights into diversification of a fruit tree crop. Nat. Commun. 6, 8824 (2015).
Swanson-Wagner, R. A. et al. Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res. 20, 1689–1699 (2010).
Stein, J. C. et al. Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat. Genet. 50, 285–296 (2018).
Zhou, Z. et al. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat. Biotechnol. 33, 408–414 (2015).
Zhang, Z. et al. Genome-wide mapping of structural variations reveals a copy number variant that determines reproductive morphology in cucumber. Plant Cell 27, 1595–1604 (2015).
Chia, J. M. et al. Maize HapMap2 identifies extant variation from a genome in flux. Nat. Genet. 44, 803–807 (2012).
Sudmant, P. H. et al. An integrated map of structural variation in 2,504 human genomes. Nature 526, 75–81 (2015).
Stuart, T. et al. Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation. eLife 5, e20777 (2016).
Vigouroux, Y. et al. Rate and pattern of mutation at microsatellite loci in maize. Mol. Biol. Evol. 19, 1251–1260 (2002).
Gaut, B., Yang, L., Takuno, S. & Eguiarte, L. E. The patterns and causes of variation in plant nucleotide substitution rates. Annu. Rev. Ecol. Evol. S. 42, 245–266 (2011).
Gordon, S. P. et al. Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. Nat. Commun. 8, 2184 (2017).
Walbot, V. Saturation mutagenesis using maize transposons. Curr. Opin. Plant Biol. 3, 103–107 (2000).
Naito, K. et al. Dramatic amplification of a rice transposable element during recent domestication. Proc. Natl. Acad. Sci. USA 103, 17620–17625 (2006).
Lisch, D. Epigenetic regulation of transposable elements in plants. Annu. Rev. Plant Biol. 60, 43–66 (2009).
Diez, C. M. et al. Genome size variation in wild and cultivated maize along altitudinal gradients. New Phytol. 199, 264–276 (2013).
Szathmáry, E., Jordán, F. & Pál, C. Molecular biology and evolution. Can genes explain biological complexity. Science 292, 1315–1316 (2001).
Panchy, N., Lehti-Shiu, M. & Shiu, S. H. Evolution of gene duplication in plants. Plant Physiol. 171, 2294–2316 (2016).
Lockton, S. & Gaut, B. S. Plant conserved non-coding sequences and paralogue evolution. Trends Genet. 21, 60–65 (2005).
Wang, Y., Wang, X. & Paterson, A. H. Genome and gene duplications and gene expression divergence: a view from plants. Ann. NY Acad. Sci. 1256, 1–14 (2012).
Yu, J. et al. PTGBase: an integrated database to study tandem duplicated genes in plants. Database 2015, bav017 (2015).
Dong, J. et al. Analysis of tandem gene copies in maize chromosomal regions reconstructed from long sequence reads. Proc. Natl. Acad. Sci. USA 113, 7949–7956 (2016).
Jelesko, J. G., Carter, K., Thompson, W., Kinoshita, Y. & Gruissem, W. Meiotic recombination between paralogous RBCSB genes on sister chromatids of Arabidopsis thaliana. Genetics 166, 947–957 (2004).
Zhang, L. & Gaut, B. S. Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome. Genome Res. 13, 2533–2540 (2003).
Gaut, B. S., Wright, S. I., Rizzon, C., Dvorak, J. & Anderson, L. K. Recombination: an underappreciated factor in the evolution of plant genomes. Nat. Rev. Genet. 8, 77–84 (2007).
Alkan, C., Coe, B. P. & Eichler, E. E. Genome structural variation discovery and genotyping. Nat. Rev. Genet. 12, 363–376 (2011).
Tattini, L., D’Aurizio, R. & Magi, A. Detection of genomic structural variants from next-generation sequencing data. Front Bioeng. Biotechnol. 3, 92 (2015).
Maretty, L. et al. Sequencing and de novo assembly of 150 genomes from Denmark as a population reference. Nature 548, 87–91 (2017).
Zhao, Q. et al. Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat. Genet. 50, 278–284 (2018).
Chakraborty, M. et al. Hidden genetic variation shapes the structure of functional elements in Drosophila. Nat. Genet. 50, 20–25 (2018).
Sedlazeck, F. J. et al. Accurate detection of complex structural variations using single-molecule sequencing. Nat. Methods 15, 461–468 (2018).
Yao, W. et al. Exploring the rice dispensable genome using a metagenome-like assembly strategy. Genome Biol. 16, 187 (2015).
Gymrek, M. et al. Abundant contribution of short tandem repeats to gene expression variation in humans. Nat. Genet. 48, 22–29 (2016).
Olsen, K. M. & Wendel, J. F. A bountiful harvest: genomic insights into crop domestication phenotypes. Annu. Rev. Plant Biol. 64, 47–70 (2013).
Studer, A., Zhao, Q., Ross-Ibarra, J. & Doebley, J. Identification of a functional transposon insertion in the maize domestication gene tb1. Nat. Genet. 43, 1160–1163 (2011).
Xu, K. et al. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442, 705–708 (2006).
Shomura, A. et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nat. Genet. 40, 1023–1028 (2008).
Kawase, M., Fukunaga, K. & Kato, K. Diverse origins of waxy foxtail millet crops in East and Southeast Asia mediated by multiple transposable element insertions. Mol. Genet. Genom. 274, 131–140 (2005).
Kobayashi, S., Goto-Yamamoto, N. & Hirochika, H. Retrotransposon-induced mutations in grape skin color. Science 304, 982 (2004).
Butelli, E. et al. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24, 1242–1255 (2012).
Fuller, D. Q. Long and attenuated: comparative trends in the domestication of tree fruits. Veg. Hist. Archaeobot. 27, 165–176 (2017).
Rogers, R. L. et al. Landscape of standing variation for tandem duplications in Drosophila yakuba and Drosophila simulans. Mol. Biol. Evol. 31, 1750–1766 (2014).
The authors thank two anonymous reviewers, A. Muyle, E. Solares and T. Batarseh for comments. BSG is supported by NSF grants 1741627 and 1655808. DKS is supported by an NSF Postdoctoral Research Fellowship in Biology (1609024). QL is supported by the National Natural Science Foundation of China (grant no. 31471431) and the Training Program for Outstanding Young Talents of Zhejiang A&F University. YZ is supported by Y.Z. is supported by the International Postdoctoral Exchange Fellowship Program, China.
The authors declare no competing interests.
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Gaut, B.S., Seymour, D.K., Liu, Q. et al. Demography and its effects on genomic variation in crop domestication. Nature Plants 4, 512–520 (2018). https://doi.org/10.1038/s41477-018-0210-1
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