Inbreeding depression in polyploid species: a meta-analysis
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu metaanalýza, časopisecké články, práce podpořená grantem
PubMed
36514955
PubMed Central
PMC9748776
DOI
10.1098/rsbl.2022.0477
Knihovny.cz E-zdroje
- Klíčová slova
- fitness, genome doubling, inbreeding depression, polyploid establishment, polyploidy,
- MeSH
- diploidie MeSH
- inbrední deprese * MeSH
- inbreeding MeSH
- Magnoliopsida * genetika MeSH
- polyploidie MeSH
- Publikační typ
- časopisecké články MeSH
- metaanalýza MeSH
- práce podpořená grantem MeSH
Whole-genome duplication is a common mutation in eukaryotes with far-reaching phenotypic effects, the resulting morphological and fitness consequences and how they affect the survival of polyploid lineages are intensively studied. Another important factor may also determine the probability of establishment and success of polyploid lineages: inbreeding depression. Inbreeding depression is expected to play an important role in the establishment of neopolyploid lineages, their capacity to colonize new environments, and in the simultaneous evolution of ploidy and other life-history traits such as self-fertilization. Both theoretically and empirically, there is no consensus on the consequences of polyploidy on inbreeding depression. In this meta-analysis, we investigated the effect of polyploidy on the evolution of inbreeding depression, by performing a meta-analysis within angiosperm species. The main results of our study are that the consequences of polyploidy on inbreeding depression are complex and depend on the time since polyploidization. We found that young polyploid lineages have a much lower amount of inbreeding depression than their diploid relatives and their established counterparts. Natural polyploid lineages are intermediate and have a higher amount of inbreeding depression than synthetic neopolyploids, and a smaller amount than diploids, suggesting that the negative effect of polyploidy on inbreeding depression decreases with time since polyploidization.
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Gregory TR, Mable BK. 2005. Polyploidy in animals. In The evolution of the genome, pp. 427-517. Amsterdam, The Netherlands: Elsevier.
Leebens-Mack JH, et al. 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574, 679-685 (10.1038/s41586-019-1693-2) PubMed DOI PMC
Van de Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411. (10.1038/nrg.2017.26) PubMed DOI
Levin DA. 1975. Minority cytotype exclusion in local plant populations. Taxon 24, 35-43. (10.2307/1218997) DOI
Comai L. 2005. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836-846. (10.1038/nrg1711) PubMed DOI
Otto SP. 2007. The evolutionary consequences of polyploidy. Cell 131, 452-462. (10.1016/j.cell.2007.10.022) PubMed DOI
Doyle JJ, Coate JE. 2019. Polyploidy, the nucleotype, and novelty: the impact of genome doubling on the biology of the cell. Int. J. Plant Sci. 180, 1-52. (10.1086/700636) DOI
Clo J, Kolář F. 2021. Short- and long-term consequences of genome doubling: a meta-analysis. Am. J. Bot. 108, 2315-2322. (10.1002/ajb2.1759) PubMed DOI
Gemble S, et al. 2022. Genetic instability from a single S phase after whole-genome duplication. Nature 604, 146-151. (10.1038/s41586-022-04578-4) PubMed DOI PMC
Rausch JH, Morgan MT. 2005. The effect of self-fertilization, inbreeding depression, and population size on autopolyploid establishmen. Evolution 59, 1867-1875. PubMed
Griswold CK. 2021. The effects of migration load, selfing, inbreeding depression, and the genetics of adaptation on autotetraploid versus diploid establishment in peripheral habitats. Evolution 75, 39-55. (10.1111/evo.14127) PubMed DOI
Charlesworth D, Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18, 237-268. (10.1146/annurev.es.18.110187.001321) DOI
Charlesworth D, Willis JH. 2009. The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783-796. (10.1038/nrg2664) PubMed DOI
Rosche C, Hensen I, Mraz P, Durka W, Hartmann M, Lachmuth S. 2017. Invasion success in polyploids: the role of inbreeding in the contrasting colonization abilities of diploid versus tetraploid populations of Centaurea stoebe s.l. J. Ecol. 105, 425-435. (10.1111/1365-2745.12670) DOI
Soltis PS, Soltis DE. 2000. The role of genetic and genomic attributes in the success of polyploids. Proc. Natl Acad. Sci. USA 97, 7051-7057. (10.1073/pnas.97.13.7051) PubMed DOI PMC
Layman NC, Busch JW. 2018. Bottlenecks and inbreeding depression in autotetraploids. Evolution 72, 2025-2037. (10.1111/evo.13587) PubMed DOI
Bever JD, Felber F. 1992. The theoretical population genetics of autopolyploidy. Oxford Surveys Evol. Biol. 8, 185.
Clo J. 2022. The evolution of the additive variance of a trait under stabilizing selection after autopolyploidization. J. Evol. Biol. 35, 891-897. (10.1111/jeb.14010) PubMed DOI PMC
Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39, 24-40. PubMed
Ronfort J. 1999. The mutation load under tetrasomic inheritance and its consequences for the evolution of the selfing rate in autotetraploid species. Genet. Res. 74, 31-42. (10.1017/S0016672399003845) DOI
Husband BC, Ozimec B, Martin SL, Pollock L. 2008. Mating consequences of polyploid evolution in flowering plants: current trends and insights from synthetic polyploids. Int. J. Plant Sci. 169, 195-206. (10.1086/523367) DOI
Siopa C, Dias MC, Castro M, Loureiro J, Castro S. 2020. Is selfing a reproductive assurance promoting polyploid establishment? Reduced fitness, leaky self-incompatibility and lower inbreeding depression in neotetraploids. Am. J. Bot. 107, 526-538. (10.1002/ajb2.1441) PubMed DOI
Busbice TH, Wilsie CP. 1966. Inbreeding depression and heterosis in autotetraploids with application to Medicago sativa L. Euphytica 15, 52-67. (10.1007/BF00024079) DOI
Dewey DR. 1966. Inbreeding depression in diploid, tetraploid, and hexaploid crested wheatgrass. Crop Sci. 6, 144-147. (10.2135/cropsci1966.0011183X000600020011x) DOI
Hedrick PW. 1987. Genetic load and the mating system in homosporous ferns. Evolution 41, 1282-1289. (10.1111/j.1558-5646.1987.tb02466.x) PubMed DOI
Huwaldt JA, Steinhorst S. 2015. Plot Digitizer, version 2.6. 8. See https://sourceforge.net/projects/plotdigitizer.
Le S, Griffin RA, Harwood CE, Vaillancourt RE, Harbard JL, Price A, Nghiem CQ, Koutoulis A, Nguyen KD. 2021. Breeding polyploid varieties of acacia: reproductive and early growth characteristics of the allotetraploid hybrid (Acacia mangium×A. auriculiformis) in comparison with diploid progenitors. Forests 12, 778. (10.3390/f12060778) DOI
Dewey DR. 1969. Inbreeding depression in diploid and induced-autotetraploid crested wheatgrass. Crop Sci. 9, 592-595. (10.2135/cropsci1969.0011183X000900050023x) DOI
Johnston MO, Schoen DJ. 1996. Correlated evolution of self-fertilization and inbreeding depression: an experimental study of nine populations of Amsinckia (Boraginaceae). Evolution 50, 1478-1491. (10.1111/j.1558-5646.1996.tb03921.x) PubMed DOI
Rosquist G. 2001. Reproductive biology in diploid Anthericum ramosum and tetraploid A. liliago (Anthericaceae). Oikos 92, 143-152. (10.1034/j.1600-0706.2001.920117.x) DOI
Inoue K, Masuda M, Maki M. 1998. Brief communication. Inbreeding depression and outcrossing rate in the endangered autotetraploid plant Aster kantoensis (Asteraceae). J. Hered. 89, 559-562. (10.1093/jhered/89.6.559) DOI
Hecker RJ. 1972. Inbreeding depression in diploid and autotetraploid sugarbeet, Beta vulgaris L. Euphytica 21, 106-111. (10.1007/BF00040554) DOI
Galloway LF, Etterson JR, Hamrick JL. 2003. Outcrossing rate and inbreeding depression in the herbaceous autotetraploid, Campanula americana. Heredity 90, 308-315. (10.1038/sj.hdy.6800242) PubMed DOI
Galloway LF, Etterson JR. 2007. Inbreeding depression in an autotetraploid herb: a three cohort field study. New Phytol. 173, 383-392. (10.1111/j.1469-8137.2006.01909.x) PubMed DOI
Husband BC. 2016. Effect of inbreeding on pollen tube growth in diploid and tetraploid Chamerion angustifolium: do polyploids mask mutational load in pollen? Am. J. Bot. 103, 532-540. (10.3732/ajb.1500243) PubMed DOI
Husband BC, Schemske DW. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50, 54-70. (10.1111/j.1558-5646.1996.tb04472.x) PubMed DOI
Ozimec BC. 2006. Inbreeding depression and mating system evolution in the autotetraploid Chamerion angustifolium. PhD Thesis, University of Guelph, Guelph, Ontario, Canada.
Barringer BC, Geber MA. 2008. Mating system and ploidy influence levels of inbreeding depression in Clarkia (Onagraceae). Evol.: Int. J. Org. Evol. 62, 1040-1051. (10.1111/j.1558-5646.2008.00361.x) PubMed DOI
Grindeland JM. 2008. Inbreeding depression and outbreeding depression in Digitalis purpurea: optimal outcrossing distance in a tetraploid. J. Evol. Biol. 21, 716-726. (10.1111/j.1420-9101.2008.01519.x) PubMed DOI
Kwok A. 2013. The role of polyploidy in the evolution of gender dimorphism: an experimental approach using Fragaria vesca. PhD Thesis, University of Guelph, Guelph, Ontario, Canada.
Wheelwright NT, Begin E, Ellwanger C, Taylor SH, Stone JL. 2016. Minimal loss of genetic diversity and no inbreeding depression in blueflag iris (Iris versicolor) on islands in the Bay of Fundy. Botany 94, 543-554. (10.1139/cjb-2016-0004) DOI
Vange V. 2002. Breeding system and inbreeding depression in the clonal plant species Knautia arvensis (Dipsacaceae): implications for survival in abandoned grassland. Biol. Conserv. 108, 59-67. (10.1016/S0006-3207(02)00090-3) DOI
Wilsie CP. 1958. Effect of inbreeding on fertility and vigor of alfalfa. Agron. J. 50, 182-185. (10.2134/agronj1958.00021962005000040004x) DOI
Posler GL, Wilsie CP, Atkins RE. 1972. Inbreeding Medicago sativa L. by selfing, sib-mating, and intergenerational crossing. Crop Sci. 12, 49-52. (10.2135/cropsci1972.0011183X001200010017x) DOI
Pujol B, Zhou SR, Sanchez Vilas J, Pannell JR. 2009. Reduced inbreeding depression after species range expansion. Proc. Natl Acad. Sci. USA 106, 15 379-15 383. (10.1073/pnas.0902257106) PubMed DOI PMC
Eppley SM, Pannell JR. 2009. Inbreeding depression in dioecious populations of the plant Mercurialis annua: comparisons between outcrossed progeny and the progeny of self-fertilized feminized males. Heredity 102, 600-608. (10.1038/hdy.2009.21) PubMed DOI
Crane MB, Lewis D. 1942. Genetical studies in pears. J. Genet. 43, 31-43. (10.1007/BF02982745) PubMed DOI
Nielsen LR, Siegismund HR, Hansen T. 2007. Inbreeding depression in the partially self-incompatible endemic plant species Scalesia affinis (Asteraceae) from Galápagos islands. Evol. Ecol. 21, 1-12. (10.1007/s10682-006-9128-6) DOI
Dudash MR, Fenster CB. 2001. The role of breeding system and inbreeding depression in the maintenance of an outcrossing mating strategy in Silene virginica (Caryophyllaceae). Am. J. Bot. 88, 1953-1959. (10.2307/3558422) PubMed DOI
Daehler CC. 1998. Variation in self-fertility and the reproductive advantage of self-fertility for an invading plant (Spartina alterniflora). Evol. Ecol. 12, 553-568. (10.1023/A:1006556709662) DOI
Armstrong JM, Robertson RW. 1956. Studies of colchicine-induced tetraploids of Trifolium Hybridum L.: I. Cross and self-fertility and cytological observations. Can. J. Agr. Sci. 36, 255-266.
Hokanson K, Hancock J. 2000. Early-acting inbreeding depression in three species of Vaccinium (Ericaceae). Sexual Plant Reprod. 13, 145-150. (10.1007/s004970000046) DOI
Kumar S, Stecher G, Suleski M, Hedges SB. 2017. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812-1819. (10.1093/molbev/msx116) PubMed DOI
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547. (10.1093/molbev/msy096) PubMed DOI PMC
Viechtbauer W. 2010. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1-48. (10.18637/jss.v036.i03) DOI
Hadfield JD. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1-22. (10.18637/jss.v033.i02) PubMed DOI
Winn AA, et al. 2011. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evol.: Int. J. Org. Evol. 65, 3339-3359. (10.1111/j.1558-5646.2011.01462.x) PubMed DOI
Otto SP, Whitton J. 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401-437. (10.1146/annurev.genet.34.1.401) PubMed DOI
Te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M, Pyšek P. 2012. The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109, 19-45. (10.1093/aob/mcr277) PubMed DOI PMC
Padilla-García N, et al. 2022. The importance of considering the evolutionary history of polyploids when assessing climatic niche evolution. J. Biogeogr. (10.1111/jbi.14496) DOI
Glennon KL, Ritchie ME, Segraves KA. 2014. Evidence for shared broad-scale climatic niches of diploid and polyploid plants. Ecol. Lett. 17, 574-582. (10.1111/ele.12259) PubMed DOI
Barringer BC. 2007. Polyploidy and self-fertilization in flowering plants. Am. J. Bot. 94, 1527-1533. (10.3732/ajb.94.9.1527) PubMed DOI
Novikova PYu, Kolesnikova UK, Scott AD. 2022. Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae. Plant Reprod. (10.1007/s00497-022-00451-6) PubMed DOI PMC
Clo J, Padilla-García N, Kolář F. 2022. Polyploidization as an opportunistic mutation: the role of unreduced gametes formation and genetic drift in polyploid establishment. J. Evol. Biol. 35, 1099-1109. (10.1111/jeb.14055) PubMed DOI
Porturas LD, Anneberg TJ, Curé AE, Wang S, Althoff DM, Segraves KA. 2019. A meta-analysis of whole genome duplication and the effects on flowering traits in plants. Am. J. Bot. 106, 469-476. (10.1002/ajb2.1258) PubMed DOI
Julião SA, et al. 2020. Induction of synthetic polyploids and assessment of genomic stability in Lippia alba. Front. Plant Sci. 11, 292. (10.3389/fpls.2020.00292) PubMed DOI PMC
Clo J, Kolář F. 2022. Data from: Inbreeding depression in polyploid species: a meta-analysis. Dryad Digital Repository. (10.5061/dryad.hx3ffbgj1) PubMed DOI PMC
Clo J, Kolář F. 2022. Inbreeding depression in polyploid species: a meta-analysis. Figshare. (10.6084/m9.figshare.c.6328854) PubMed DOI PMC
Inbreeding depression in polyploid species: a meta-analysis