Population bottleneck
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A population bottleneck, also called a genetic bottleneck, is a sharp fall in the size of a population that lasts at least one generation. The population that follows descends from the individuals that passed through the fall and carries only the variation they held.[1] The loss is genetic drift at a small effective population size. Later growth in numbers does not restore it, except through new mutation.[2] Rare alleles go first, so a population can keep much of its heterozygosity while losing many of its alleles. Soybean cultivars retained 72 per cent of the sequence diversity of the Asian landraces behind them and lost 79 per cent of the landraces' rare alleles.[3]
A past bottleneck leaves traces in allele frequencies and genome sequences that statistical tests can read. Reduced diversity alone does not show one. The sharp domestication bottleneck long assumed for crops is now disputed.[4]
In Cannabis, the best-fitting of 18 demographic models has the ancestors of hemp and drug-type plants pass through an effective size of about 190 after they split from other cannabis about 12,000 years ago.[5] A microsatellite test of 199 accessions gave a bottleneck signal under two mutation models and none under a third.[6] Bottlenecks proposed for hemp and drug-type breeding lines have been inferred from low diversity and from breeding history.[7]: 310[8]
Size and length of the fall
A bottleneck is measured by how few individuals remain and for how many generations. Measures of variation respond to both.[9] In the ideal model a population of N loses 1/(2N) of its heterozygosity in a generation: a tenth at five individuals and 1 per cent at 50.[10] Masatoshi Nei, Takeo Maruyama and Ranajit Chakraborty computed the effects of bottlenecks in 1975.[2][11] A severe fall brings a rapid loss of heterozygosity.[4]
In maize, sequence diversity at the Adh1 gene fits a bottleneck of short length and very small size, for example 20 founding individuals over ten generations.[12] Over a longer span, the generations spent at a small size weigh more heavily in the effective size than their number suggests.[13] The founding of a new population by a few individuals has the same effects.[14]
Rare alleles and heterozygosity
N diploid plants carry 2N copies of a gene into the next generation.[15] A sample of that size misses an allele at frequency p with probability (1 − p)2N. With ten plants, an allele held by 1 per cent of gene copies is missed about four times in five and one held by 20 per cent about once in 90. Heterozygosity falls by 5 per cent.
Alleles therefore fall faster than heterozygosity. For a time after the fall, a population has more heterozygosity at neutral loci than its number of alleles would predict at equilibrium between mutation and drift.[16] Among the alleles that survive, those below a frequency of 0.1 become scarcer than those in an intermediate class.[17]
A bottleneck also changes the burden of harmful mutations. In models of outcrossing populations, inbreeding depression drops at once and goes on falling for some generations as highly recessive mutations are purged. The genetic load rises at once and then declines. For bottlenecks of ten or more individuals the changes are usually a few percentage points, unless lethal mutations arise very often and numbers recover very slowly.[18] Most crops examined carry more putatively harmful alleles than their wild relatives.[19] In maize landraces the excess is most pronounced in Andean maize, which went through a more severe founder event than other maize.[20]
Reading a bottleneck from genes
Several methods read a past fall in size from samples taken in the present.
| Method | What it reads | Reach | What limits it |
|---|---|---|---|
| Heterozygosity excess | Heterozygosity against the number of alleles[16] | A limited number of generations, until a new equilibrium[16] | Needs a mutation model. Markers under the infinite-allele model are the most useful[16] |
| Mode shift | The share of alleles below a frequency of 0.1 against an intermediate class[17] | A few dozen generations[17] | Likely to detect a fall to 20 or fewer breeding individuals, with 8 to 10 microsatellite loci and about 30 plants[17] |
| M ratio | Number of alleles against the range of allele sizes at microsatellite loci[9] | More than 100 generations in simulations[9] | Microsatellites only. Separates a recent fall from a population small for a long time[9] |
| Tajima's D | Segregating sites against average differences between sequences. Segregating sites follow current size more closely and average differences original size[21] | Depends on the time since the change: a contraction reads differently once a population has expanded again[22] | Devised as a test of neutrality, so it also responds to selection[23] |
| Sequential coalescent (PSMC) | Times to the common ancestor of the two gene copies in one genome. Coalescence is faster while a population is small[24][25] | About 10,000 to a million years in human genomes[24] | Population structure can produce a false signal of change in size[26] |
| Fitting models by simulation | Whole-genome data against a set of proposed histories[5] | About 12,000 years to 54 years ago in cannabis[5] | Under a wrong model, data can give precise estimates of a bottleneck that means nothing[26] |
A review of vertebrate studies found that microsatellite tests often miss bottlenecks in populations known to have declined. Simulations traced this largely to small samples. Common assumptions about how microsatellites mutate also underestimate multi-step mutations by about half, so that the tests can report bottlenecks in stable populations more often than their significance level implies.[27]
A selective sweep lowers diversity near a selected gene with no fall in population size.[28] In maize, 2 to 4 per cent of 774 genes showed selection and the rest retained the signature of a bottleneck.[29] Ren and colleagues combined three statistics to tell sweeps from background divergence caused by bottlenecks.[5]
The domestication bottleneck
Crops generally hold less diversity than their wild progenitors. The usual explanation is a sharp fall at domestication, as early farmers took a small part of the wild population and then selected within it.[4] Cultivated maize holds 75 per cent of the variation of its progenitor at Adh1.[12] In soybean, sequencing of populations from before and after each stage found that domestication halved a diversity already low in the wild species and removed 81 per cent of rare alleles. Later losses, in simulations, came mostly from the small number of landraces introduced to North America and little from selective breeding.[3]
Robin Allaby and colleagues tested the idea on ancient genomes of barley, maize and sorghum. None showed the expected dip in heterozygosity near domestication. In sorghum heterozygosity fell in a straight line over time. The authors proposed a continuing erosion through many small founder events. They concluded that lower diversity in a crop should not be taken as evidence of a domestication bottleneck.[4] Other work supports a long process. Resequencing of 31 maize landraces and four wild plants points to a protracted bottleneck followed by serial founder effects as the crop spread.[20] A 2018 review found slow domestication tentatively supported by fossil data and sequential coalescent methods.[19]
In cannabis
Demographic models
Guangpeng Ren and colleagues analysed 110 genomes and compared 18 models of bottlenecks and growth, treating feral and cultivated drug-type plants as one group. In the best-fitting model, the ancestors of hemp and drug types split from the basal group about 12,000 years ago (95 per cent interval 6,458 to 15,728) at an effective size of about 190. That lineage later grew and divided into hemp and drug types. Each of those grew again in the last few centuries. The basal group stayed above a million until the last 54 years. The authors note that their groups are not panmictic populations.[5]
| Group | Years ago | Effective size |
|---|---|---|
| Ancestors of hemp and drug types | 11,992 to 6,751 | 190 |
| Ancestors of hemp and drug types | 6,751 to 3,889 | 22,600 |
| Hemp | 3,889 to 321 | 979 |
| Hemp | 321 to present | 5,270 |
| Drug type, feral and cultivated | 3,889 to 563 | 11,900 |
| Drug type, feral and cultivated | 563 to present | 47,300 |
| Basal group | 11,992 to 54 | 1,660,000 |
| Basal group | 54 to present | 824 |
Patrick Woods and colleagues found Tajima's D positive at 7,540 single-copy genes in every group they compared, lowest in Asian plants and highest in feral American and drug-type plants. They took this to mean that all the groups except the Asian one had contracted recently without time to expand again.[22] A study of five chloroplast regions in 645 plants found Tajima's D and Fu's Fs not significant for any group and read this as stable populations.[30] Among 68 plants from Iran and Afghanistan, mean D was 0.007, which the authors attributed to balancing selection.[31]
A microsatellite test
Jiangjiang Zhang and colleagues tested 199 accessions, grouped by region of origin into nine sets, at 72 microsatellite loci. The sign test for heterozygosity excess was significant in all nine sets under the infinite-allele model, in eight under the two-phase model and in none under the stepwise model. The allele frequency distribution showed a mode shift in three sets and the normal L-shape in six. The authors concluded that a recent bottleneck had occurred in all the populations.[6]
Bottlenecks inferred from other evidence
Robert Clarke and Mark Merlin wrote that the drug-type gene pool had reached a genetic bottleneck through breeding between close relatives, selfing, selection for potency and vegetative propagation. They traced most European hemp cultivars to the same few single-plant selections.[7]: 310 Surveys of diversity have proposed bottlenecks in particular groups. Dufresnes and colleagues suggested that positive inbreeding coefficients in hemp varieties might reflect bottlenecks from current breeding practice.[8] Soler and colleagues took a low number of alleles per locus in some indica cultivars, in some cases only two, to indicate a bottleneck during their development.[32] Henry and colleagues judged that a cluster of cannabidiol-rich resin hemp had likely gone through a bottleneck while its chemotype was stabilised.[33]
Heterozygosity was lower in 16 fibre accessions than in other groups in one study, which suggested a bottleneck from recent selection for fibre. A survey of 43 fibre and 81 marijuana varieties found it lower in marijuana.[34][35]
Clarke and Merlin hold that people moving cannabis to new settlements most likely carried only a few seeds and sometimes raised parents from a single female, giving founder effects in the populations that became local landraces. Their example from drug-type breeding is the Afghan broad-leaflet landraces brought to Europe and North America in the late 1970s and early 1980s, of which a handful of plants were selected and crossed.[7]: 297 From the distribution of fossil pollen, John McPartland argued that European cannabis went through repeated bottlenecks as its range contracted.[36]
Seed collections and small populations
Each regrowing of a stored accession passes it through the plants that grow and set seed that year. Allelic variation may decline with each cycle.[34] At the Vavilov Institute in the 1990s, lack of space and of viable seed often made the minimum of 1,000 plants impossible. Several accessions had to be multiplied from very few seeds.[37]
One aim of regeneration is to keep at least one copy of every allele. For outbreeding crops, 160 to 210 plants give a 90 to 95 per cent chance of keeping alleles at a frequency of 0.05 or more at each of 150 loci.[38] Under mass selection, a field from which most male plants are removed before they shed pollen breeds from few fathers, which narrows the next generation.[39]
Law-enforcement seizures, agricultural accidents and the culling of unprofitable clones also reduce diversity in cannabis, according to Clarke and Merlin.[7]: 310–311 These losses are one form of genetic erosion. Regrowing stored seed is part of ex situ conservation.
See also
References
- ↑ Davinack, D. (2024). Molecular Ecology & Evolution: An Introduction. Norton, Massachusetts: Wheaton College. pp. 113–115.
- ↑ 2.0 2.1 Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. pp. 289–290.
- ↑ 3.0 3.1 Hyten, D.L.; Song, Q.; Zhu, Y.; Choi, I.Y.; Nelson, R.L.; Costa, J.M.; et al. (2006). "Impacts of genetic bottlenecks on soybean genome diversity". Proceedings of the National Academy of Sciences. 103 (45): 16666–16671. doi:10.1073/pnas.0604379103.
- ↑ 4.0 4.1 4.2 4.3 Allaby, R.G.; Ware, R.L.; Kistler, L. (2019). "A re-evaluation of the domestication bottleneck from archaeogenomic evidence". Evolutionary Applications. 12 (1): 29–37. doi:10.1111/eva.12680.
- ↑ 5.0 5.1 5.2 5.3 5.4 Ren, G.; Zhang, X.; Li, Y.; Ridout, K.; Serrano-Serrano, M.L.; Yang, Y.; Liu, A.; Ravikanth, G.; Nawaz, M.A.; Mumtaz, A.S.; Salamin, N.; Fumagalli, L. (2021). "Large-scale whole-genome resequencing unravels the domestication history of Cannabis sativa". Science Advances. 7 (29) eabg2286. doi:10.1126/sciadv.abg2286.
- ↑ 6.0 6.1 Zhang, J.; Yan, J.; Huang, S.; Pan, G.; Chang, L.; Li, J.; et al. (2020). "Genetic diversity and population structure of Cannabis based on the genome-wide development of simple sequence repeat markers". Frontiers in Genetics. 11 958. doi:10.3389/fgene.2020.00958.
- ↑ 7.0 7.1 7.2 7.3 Clarke, Robert C.; Merlin, Mark D. (2016). "Cannabis domestication, breeding history, present-day genetic diversity, and future prospects". Critical Reviews in Plant Sciences. 35 (5–6): 293–327. doi:10.1080/07352689.2016.1267498.
- ↑ 8.0 8.1 Dufresnes, C.; Jan, C.; Bienert, F.; Goudet, J.; Fumagalli, L. (2017). "Broad-scale genetic diversity of Cannabis for forensic applications". PLoS ONE. 12 (1) e0170522. doi:10.1371/journal.pone.0170522.
- ↑ 9.0 9.1 9.2 9.3 Garza, J.C.; Williamson, E.G. (2001). "Detection of reduction in population size using data from microsatellite loci". Molecular Ecology. 10 (2): 305–318. doi:10.1046/j.1365-294x.2001.01190.x.
- ↑ Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. pp. 254–256.
- ↑ Nei, M.; Maruyama, T.; Chakraborty, R. (1975). "The bottleneck effect and genetic variability in populations". Evolution. 29 (1): 1–10. doi:10.1111/j.1558-5646.1975.tb00807.x.
- ↑ 12.0 12.1 Eyre-Walker, A.; Gaut, R.L.; Hilton, H.; Feldman, D.L.; Gaut, B.S. (1998). "Investigation of the bottleneck leading to the domestication of maize". Proceedings of the National Academy of Sciences. 95 (8): 4441–4446. doi:10.1073/pnas.95.8.4441.
- ↑ Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. pp. 269–270.
- ↑ Davinack, D. (2024). Molecular Ecology & Evolution: An Introduction. Norton, Massachusetts: Wheaton College. pp. 121–122.
- ↑ Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. pp. 256–258.
- ↑ 16.0 16.1 16.2 16.3 Cornuet, J.M.; Luikart, G. (1996). "Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data". Genetics. 144 (4): 2001–2014. doi:10.1093/genetics/144.4.2001.
- ↑ 17.0 17.1 17.2 17.3 Luikart, G. (1998). "Distortion of allele frequency distributions provides a test for recent population bottlenecks". Journal of Heredity. 89 (3): 238–247. doi:10.1093/jhered/89.3.238.
- ↑ Kirkpatrick, M.; Jarne, P. (2000). "The effects of a bottleneck on inbreeding depression and the genetic load". The American Naturalist. 155 (2): 154–167. doi:10.1086/303312.
- ↑ 19.0 19.1 Gaut, B.S.; Seymour, D.K.; Liu, Q.; Zhou, Y. (2018). "Demography and its effects on genomic variation in crop domestication". Nature Plants. 4 (8): 512–520. doi:10.1038/s41477-018-0210-1.
- ↑ 20.0 20.1 Wang, L.; Beissinger, T.M.; Lorant, A.; Ross-Ibarra, C.; Ross-Ibarra, J.; Hufford, M.B. (2017). "The interplay of demography and selection during maize domestication and expansion". Genome Biology. 18 (1) 215. doi:10.1186/s13059-017-1346-4.
- ↑ Tajima, F. (1989). "The effect of change in population size on DNA polymorphism". Genetics. 123 (3): 597–601. doi:10.1093/genetics/123.3.597.
- ↑ 22.0 22.1 Woods, P.; Price, N.; Matthews, P.; McKay, J.K. (2023). "Genome-wide polymorphism and genic selection in feral and domesticated lineages of Cannabis sativa". G3. 13 (2) jkac209. doi:10.1093/g3journal/jkac209.
- ↑ Tajima, F. (1989). "Statistical method for testing the neutral mutation hypothesis by DNA polymorphism". Genetics. 123 (3): 585–595. doi:10.1093/genetics/123.3.585.
- ↑ 24.0 24.1 Li, H.; Durbin, R. (2011). "Inference of human population history from individual whole-genome sequences". Nature. 475 (7357): 493–496. doi:10.1038/nature10231.
- ↑ Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. p. 470.
- ↑ 26.0 26.1 Mazet, O.; Rodríguez, W.; Grusea, S.; Boitard, S.; Chikhi, L. (2016). "On the importance of being structured: instantaneous coalescence rates and human evolution: lessons for ancestral population size inference?". Heredity. 116 (4): 362–371. doi:10.1038/hdy.2015.104.
- ↑ Peery, M.Z.; Kirby, R.; Reid, B.N.; Stoelting, R.; Doucet‐Bëer, E.; Robinson, S.; et al. (2012). "Reliability of genetic bottleneck tests for detecting recent population declines". Molecular Ecology. 21 (14): 3403–3418. doi:10.1111/j.1365-294x.2012.05635.x.
- ↑ Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. pp. 273–275.
- ↑ Wright, S.I.; Bi, I.V.; Schroeder, S.G.; Yamasaki, M.; Doebley, J.F.; McMullen, M.D.; Gaut, B.S. (2005). "The effects of artificial selection on the maize genome". Science. 308 (5726): 1310–1314. doi:10.1126/science.1107891.
- ↑ Zhang, Q.; Chen, X.; Guo, H.; Trindade, L.M.; Salentijn, E.M.J.; Guo, R.; Guo, M.; Xu, Y.; Yang, M. (2018). "Latitudinal adaptation and genetic insights into the origins of Cannabis sativa L." Frontiers in Plant Science. 9 1876. doi:10.3389/fpls.2018.01876.
- ↑ Soorni, A.; Fatahi, R.; Haak, D.C.; Salami, S.A.; Bombarely, A. (2017). "Assessment of genetic diversity and population structure in Iranian Cannabis germplasm". Scientific Reports. 7 (1) 15668. doi:10.1038/s41598-017-15816-5.
- ↑ Soler, S.; Gramazio, P.; Figàs, M.R.; Vilanova, S.; Rosa, E.; Llosa, E.R.; et al. (2017). "Genetic structure of Cannabis sativa var. indica cultivars based on genomic SSR (gSSR) markers: implications for breeding and germplasm management". Industrial Crops and Products. 104: 171–178. doi:10.1016/j.indcrop.2017.04.043.
- ↑ Henry, P.; Khatodia, S.; Kapoor, K.; Gonzales, B.; Middleton, A.; Hong, K.; et al. (2020). "A single nucleotide polymorphism assay sheds light on the extent and distribution of genetic diversity, population structure and functional basis of key traits in cultivated north American cannabis". Journal of Cannabis Research. 2 (1) 26. doi:10.1186/s42238-020-00036-y.
- ↑ 34.0 34.1 Welling, M.T.; Shapter, T.; Rose, T.J.; Liu, L.; Stanger, R.; King, G.J. (2016). "A belated green revolution for Cannabis: virtual genetic resources to fast-track cultivar development". Frontiers in Plant Science. 7 1113. doi:10.3389/fpls.2016.01113.
- ↑ Sawler, Jason; Stout, Jake M.; Gardner, Kyle M.; Hudson, Darryl; Vidmar, John; Butler, Laura; Page, Jonathan E.; Myles, Sean (2015). "The genetic structure of marijuana and hemp". PLOS ONE. 10 (8) e0133292. doi:10.1371/journal.pone.0133292.
- ↑ McPartland, J.M. (2018). "Cannabis systematics at the levels of family, genus, and species". Cannabis and Cannabinoid Research. 3 (1): 203–212. doi:10.1089/can.2018.0039.
- ↑ Clarke, R.C. (1998). "Maintenance of Cannabis germplasm in the Vavilov Research Institute Gene Bank: five year report". Journal of the International Hemp Association. 5 (2): 75–79.
- ↑ Crossa, J.; Hernandez, C.M.; Bretting, P.; Eberhart, S.A.; Taba, S. (1993). "Statistical genetic considerations for maintaining germ plasm collections". Theoretical and Applied Genetics. 86 (6): 673–678. doi:10.1007/bf00222655.
- ↑ Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. pp. 266–268.