×

Testing for population decline using maximal linkage disequilibrium blocks. (English) Zbl 1516.92030

Summary: Only 6% of known species have a conservation status. Methods that assess conservation statuses are often based on individual counts and are thus too laborious to be generalized to all species. Population genomics methods that infer past variations in population size are easy to use but limited to the relatively distant past. Here we propose a population genomics approach that tests for recent population decline and may be used to assess species conservation statuses. More specifically, we study maximal recombination free (MRF) blocks, that are segments of a sequence alignment inherited from a common ancestor without recombination. MRF blocks are relatively longer in small than in large populations. We use the distribution of MRF block lengths rescaled by their mean to test for recent population decline. However, because MRF blocks are difficult to detect, we also consider maximal linkage disequilibrium (MLD) blocks, which are runs of single nucleotide polymorphisms compatible with a single tree. We develop a new method capable of inferring a very recent decline (e.g. with a detection power of 50% for populations whose size was halved to \(N\), \(0.05 \times N\) generations ago) from rescaled MLD block lengths. Our framework could serve as a basis for quantitative tools to assess conservation status in a wide range of species.

MSC:

92D10 Genetics and epigenetics
92D15 Problems related to evolution
62P10 Applications of statistics to biology and medical sciences; meta analysis

Software:

PLINK
PDFBibTeX XMLCite
Full Text: DOI DOI

References:

[1] Adams, A. M.; Hudson, R. R., Maximum-likelihood estimation of demographic parameters using the frequency spectrum of unlinked single-nucleotide polymorphisms, Genetics, 168, 3, 1699-1712 (2004)
[2] Alonso-Blanco, C.; Andrade, J.; Becker, C.; Bemm, F.; Bergelson, J.; Borgwardt, K. M.; Cao, J.; Chae, E.; Dezwaan, T. M.; Ding, W.; Ecker, J. R.; Exposito-Alonso, M.; Farlow, A.; Fitz, J.; Gan, X.; Grimm, D. G.; Hancock, A. M.; Henz, S. R.; Holm, S.; Horton, M.; Jarsulic, M.; Kerstetter, R. A.; Korte, A.; Korte, P.; Lanz, C.; Lee, C.-R.; Meng, D.; Michael, T. P.; Mott, R.; Muliyati, N. W.; Nägele, T.; Nagler, M.; Nizhynska, V.; Nordborg, M.; Novikova, P. Y.; Picó, F. X.; Platzer, A.; Rabanal, F. A.; Rodriguez, A.; Rowan, B. A.; Salomé, P. A.; Schmid, K. J.; Schmitz, R. J.; Seren, Ü.; Sperone, F. G.; Sudkamp, M.; Svardal, H.; Tanzer, M. M.; Todd, D.; Volchenboum, S. L.; Wang, C.; Wang, G.; Wang, X.; Weckwerth, W.; Weigel, D.; Zhou, X., 1,135 genomes reveal the global pattern of polymorphism in arabidopsis thaliana, Cell, 166, 2, 481-491 (2016)
[3] Ball, F.; Stefanov, V. T., Evaluation of identity-by-descent probabilities for half-sibs on continuous genome, Math. Biosci., 196, 2, 215-225 (2005) · Zbl 1070.92035
[4] Barnosky, A. D.; Matzke, N.; Tomiya, S.; Wogan, G. O.U.; Swartz, B.; Quental, T. B.; Marshall, C.; McGuire, J. L.; Lindsey, E. L.; Maguire, K. C.; Mersey, B.; Ferrer, E. A., Has the earth’s sixth mass extinction already arrived?, Nature, 471, 7336, 51-57 (2011)
[5] Beichman, A. C.; Huerta-Sanchez, E.; Lohmueller, K. E., Using genomic data to infer historic population dynamics of nonmodel organisms, Annu. Rev. Ecol. Evol. Syst., 49, 1, 433-456 (2018)
[6] Browning, S. R.; Browning, B. L., High-resolution detection of identity by descent in unrelated individuals, Am. J. Hum. Genet., 86, 4, 526-539 (2010)
[7] Browning, B. L.; Browning, S. R., Improving the accuracy and efficiency of identity-by-descent detection in population data, Genetics, 194, 2, 459-471 (2013)
[8] Browning, S. R.; Browning, B. L., Accurate non-parametric estimation of recent effective population size from segments of identity by descent, Am. J. Hum. Genet., 97, 3, 404-418 (2015)
[9] Carmi, S.; Wilton, P. R.; Wakeley, J.; Pe’er, I., A renewal theory approach to IBD sharing, Theor. Popul. Biol., 97, 35-48 (2014) · Zbl 1303.92068
[10] Ceballos, G.; Ehrlich, P. R.; Dirzo, R., Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines, Proc. Natl. Acad. Sci., 114, 30, E6089-E6096 (2017)
[11] Chapman, N. H.; Thompson, E. A., A model for the length of tracts of identity by descent in finite random mating populations, Theor. Popul. Biol., 64, 2, 141-150 (2003) · Zbl 1103.92030
[12] Chikhi, L.; Rodríguez, W.; Grusea, S.; Santos, P.; Boitard, S.; Mazet, O., The IICR (inverse instantaneous coalescence rate) as a summary of genomic diversity: insights into demographic inference and model choice, Heredity, 120, 1, 13-24 (2018)
[13] Donnelly, K. P., The probability that related individuals share some section of genome identical by descent, Theor. Popul. Biol., 23, 1, 34-63 (1983) · Zbl 0521.92011
[14] Excoffier, L.; Dupanloup, I.; Huerta-Sánchez, E.; Sousa, V. C.; Foll, M., Robust demographic inference from genomic and SNP data, PLoS Genet., 9, 10, Article e1003905 pp. (2013)
[15] Fu, Y. X., Statistical properties of segregating sites, Theor. Popul. Biol., 48, 2, 172-197 (1995) · Zbl 0854.92014
[16] Gibbs, R. A.; Boerwinkle, E.; Doddapaneni, H.; Han, Y.; Korchina, V.; Kovar, C.; Lee, S.; Muzny, D.; Reid, J. G., A global reference for human genetic variation, Nature, 526, 7571, 68-74 (2015)
[17] Gordon, D.; Huddleston, J.; Chaisson, M. J.P.; Hill, C. M.; Kronenberg, Z. N.; Munson, K. M.; Malig, M.; Raja, A.; Fiddes, I.; Hillier, L. W.; Dunn, C.; Baker, C.; Armstrong, J.; Diekhans, M.; Paten, B.; Shendure, J.; Wilson, R. K.; Haussler, D.; Chin, C.-S.; Eichler, E. E., Long-read sequence assembly of the gorilla genome, Science, 352, 6281 (2016)
[18] Griffiths, R.; Marjoram, P., An ancestral recombination graph, (Progress in Population Genetics and Human Evolution (1997), Springer), 257-270 · Zbl 0893.92020
[19] Grusea, S.; Rodríguez, W.; Pinchon, D.; Chikhi, L.; Boitard, S.; Mazet, O., Coalescence times for three genes provide sufficient information to distinguish population structure from population size changes, J. Math. Biol., 78, 1-2, 189-224 (2019) · Zbl 1410.92066
[20] Gusev, A.; Lowe, J. K.; Stoffel, M.; Daly, M. J.; Altshuler, D.; Breslow, J. L.; Friedman, J. M.; Pe’er, I., Whole population, genome-wide mapping of hidden relatedness, Genome Res., 19, 2, 318-326 (2009)
[21] Gutenkunst, R. N.; Hernandez, R. D.; Williamson, S. H.; Bustamante, C. D., Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data, PLoS Genet., 5, 10, Article e1000695 pp. (2009)
[22] Harris, K.; Nielsen, R., Inferring demographic history from a spectrum of shared haplotype lengths, PLoS Genet., 9, 6, Article e1003521 pp. (2013)
[23] Hayes, B. J.; Visscher, P. M.; McPartlan, H. C.; Goddard, M. E., Novel multilocus measure of linkage disequilibrium to estimate past effective population size, Genome Res., 13, 4, 635-643 (2003)
[24] Hey, J.; Wakeley, J., A coalescent estimator of the population recombination rate, Genetics, 145, 3, 833-846 (1997)
[25] Hill, W. G.; Robertson, A., Linkage disequilibrium in finite populations, Theor. Appl. Genet., 38, 6, 226-231 (1968)
[26] Hollenbeck, C. M.; Portnoy, D. S.; Gold, J. R., A method for detecting recent changes in contemporary effective population size from linkage disequilibrium at linked and unlinked loci, Heredity, 117, 4, 207-216 (2016)
[27] Hudson, R. R.; Kaplan, N., Statistical properties of the number of recombination events in the history of a sample of DNA sequences, Genetics, 111, 1, 147-164 (1985)
[28] Kelleher, J.; Etheridge, A. M.; McVean, G., Efficient coalescent simulation and genealogical analysis for large sample sizes, PLoS Comput. Biol., 12, 5, Article e1004842 pp. (2016)
[29] Kingman, J. F.C., The coalescent, Stochastic Process. Appl., 13, 3, 235-248 (1982) · Zbl 0491.60076
[30] Lapierre, M.; Lambert, A.; Achaz, G., Accuracy of demographic inferences from the site frequency spectrum: the case of the yoruba population, Genetics, 206, 1, 439-449 (2017)
[31] Lewontin, R. C.; ichi Kojima, K., The evolutionary dynamics of complex polymorphisms, Evolution, 14, 4, 458-472 (1960)
[32] Li, H.; Durbin, R., Inference of human population history from individual whole-genome sequences, Nature, 475, 7357, 493-496 (2011)
[33] MacLeod, I. M.; Larkin, D. M.; Lewin, H. A.; Hayes, B. J.; Goddard, M. E., Inferring demography from runs of homozygosity in whole-genome sequence, with correction for sequence errors, PLoS Comput. Biol., 30, 9, 2209-2223 (2013)
[34] MacLeod, I. M.; Meuwissen, T. H.E.; Hayes, B.; Goddard, M. E., A novel predictor of multilocus haplotype homozygosity: comparison with existing predictors, Genet. Res., 91, 6, 413-426 (2009)
[35] Maddison, W. P., Gene trees in species trees, Syst. Biol., 46, 3, 523-536 (1997)
[36] Marjoram, P.; Wall, J. D., Fast “coalescent” simulation, BMC Genet., 7, 16 (2006)
[37] Marth, G. T.; Czabarka, E.; Murvai, J.; Sherry, S. T., The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations, Genetics, 166, 1, 351-372 (2004)
[38] Mazet, O.; Rodríguez, W.; Chikhi, L., Demographic inference using genetic data from a single individual: Separating population size variation from population structure, Theor. Popul. Biol., 104, 46-58 (2015) · Zbl 1342.91033
[39] 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, 4, 362-371 (2016)
[40] McVean, G. A.T.; Cardin, N. J., Approximating the coalescent with recombination, Philos. Trans. R Soc. London [Biol.], 360, 1459, 1387-1393 (2005)
[41] Díez-del Molino, D.; Sánchez-Barreiro, F.; Barnes, I.; Gilbert, M. T.P.; Dalén, L., Quantifying temporal genomic erosion in endangered species, Trends Ecol. Evol., 33, 3, 176-185 (2018)
[42] Palamara, P. F.; Lencz, T.; Darvasi, A.; Pe’er, I., Length distributions of identity by descent reveal fine-scale demographic history, Am. J. Hum. Genet., 91, 5, 809-822 (2012)
[43] Patin, E.; Siddle, K. J.; Laval, G.; Quach, H.; Harmant, C.; Becker, N.; Froment, A.; Régnault, B.; Lemée, L.; Gravel, S., The impact of agricultural emergence on the genetic history of African rainforest hunter-gatherers and agriculturalists, Nature Commun., 5, 1 (2014)
[44] Prado-Martinez, J.; Sudmant, P. H.; Kidd, J. M.; Li, H.; Kelley, J. L.; Lorente-Galdos, B.; Veeramah, K. R.; Woerner, A. E.; O’Connor, T. D.; Santpere, G., Great ape genetic diversity and population history, Nature, 499, 7459, 471-475 (2013)
[45] Purcell, S.; Neale, B.; Todd-Brown, K.; Thomas, L.; Ferreira, M. A.R.; Bender, D.; Maller, J.; Sklar, P.; de Bakker, P. I.W.; Daly, M. J.; Sham, P. C., PLINK: A tool set for whole-genome association and population-based linkage analyses, Am. J. Hum. Genet., 81, 3, 559-575 (2007)
[46] Régnier, C.; Achaz, G.; Lambert, A.; Cowie, R. H.; Bouchet, P.; Fontaine, B., Mass extinction in poorly known taxa, Proc. Natl. Acad. Sci., 112, 25, 7761-7766 (2015)
[47] Ringbauer, H.; Coop, G.; Barton, N. H., Inferring recent demography from isolation by distance of long shared sequence blocks, Genetics, 205, 3, 1335-1351 (2017)
[48] Rodrigues, A. S.L.; Pilgrim, J. D.; Lamoreux, J. F.; Hoffmann, M.; Brooks, T. M., The value of the IUCN Red List for conservation, Trends Ecol. Evolut., 21, 2, 71-76 (2006)
[49] Rodríguez, W.; Mazet, O.; Grusea, S.; Arredondo, A.; Corujo, J. M.; Boitard, S.; Chikhi, L., The IICR and the non-stationary structured coalescent: towards demographic inference with arbitrary changes in population structure, Heredity, 121, 6, 663-678 (2018)
[50] Sánchez-Bayo, F.; Wyckhuys, K. A.G., Worldwide decline of the entomofauna: A review of its drivers, Biol. Cons., 232, 8-27 (2019)
[51] Schiffels, S.; Durbin, R., Inferring human population size and separation history from multiple genome sequences, Nature Genet., 46, 8, 919-925 (2014)
[52] Sheehan, S.; Harris, K.; Song, Y. S., Estimating variable effective population sizes from multiple genomes: A sequentially Markov conditional sampling distribution approach, Genetics, 194, 3, 647-662 (2013)
[53] Stam, P., The distribution of the fraction of the genome identical by descent in finite random mating populations, Genet. Res., 35, 2, 131-155 (1980)
[54] Stefanov, V. T., Distribution of genome shared identical by descent by two individuals in grandparent-type relationship, Genetics, 156, 3, 1403-1410 (2000)
[55] Terhorst, J.; Kamm, J. A.; Song, Y. S., Robust and scalable inference of population history from hundreds of unphased whole genomes, Nature Genet., 49, 2, 303-309 (2017)
[56] Tiret, M.; Hospital, F., Blocks of chromosomes identical by descent in a population: Models and predictions, Plos One, 12, 11, Article e0187416 pp. (2017)
[57] van der Valk, T.; Díez-del Molino, D.; Marques-Bonet, T.; Guschanski, K.; Dalén, L., Historical genomes reveal the genomic consequences of recent population decline in eastern gorillas, Curr. Biol., 29, 1, 165-170.e6 (2019)
[58] Wallberg, A.; Han, F.; Wellhagen, G.; Dahle, B.; Kawata, M.; Haddad, N.; Simões, Z. L.P.; Allsopp, M. H.; Kandemir, I.; De la Rúa, P.; Pirk, C. W.; Webster, M. T., A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera, Nature Genet., 46, 10, 1081-1088 (2014)
[59] Watterson, G. A., On the number of segregating sites in genetical models without recombination, Theor. Popul. Biol., 7, 2, 256-276 (1975) · Zbl 0294.92011
[60] Wiuf, C.; Hein, J., The ancestry of a sample of sequences subject to recombination, Genetics, 151, 3, 1217-1228 (1999)
[61] Wright, S., Evolution in mendelian populations, Genetics, 16, 2, 97-159 (1931)
[62] Zhang, W.; Westerman, E.; Nitzany, E.; Palmer, S.; Kronforst, M. R., Tracing the origin and evolution of supergene mimicry in butterflies, Nature Commun., 8, 1 (2017)
[63] Zhao, S.; Zheng, P.; Dong, S.; Zhan, X.; Wu, Q.; Guo, X.; Hu, Y.; He, W.; Zhang, S.; Fan, W.; Zhu, L.; Li, D.; Zhang, X.; Chen, Q.; Zhang, H.; Zhang, Z.; Jin, X.; Zhang, J.; Yang, H.; Wang, J.; Wang, J.; Wei, F., Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation, Nature Genet., 45, 1, 67-71 (2013)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.