Increased inbreeding but not homozygosity in small populations of Sabatia angularis (Gentianaceae)
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Abstract
Understanding how the mating system varies with population size in plant populations is critical for understanding their genetic and demographic fates. We examined how the mating system, characterized by outcrossing rate, biparental inbreeding rate, and inbreeding coefficient, and genetic diversity varied with population size in natural populations of the biennial Sabatia angularis. We found a significant, positive relationship between outcrossing and population size. Selfing was as high as 40% in one small population but was only 7% in the largest population. Despite this pattern, observed heterozygosity did not vary with population size, and we suggest that selection against inbred individuals maintains observed heterozygosity in small populations. Consistent with this hypothesis, we found a trend of lower inbreeding coefficients in the maternal than progeny generation in all of the populations, and half of the populations exhibited significant excesses of adult heterozygosity. Moreover, genetic diversity was not related to population size and was similar across all populations examined. Our results suggest that the consequences of increased selfing for population fitness in S. angularis, a species that experiences significant inbreeding depression, will depend on the relative magnitude and consistency of inbreeding depression and the demographic cost of selection for outcrossed progeny in small populations.
Keywords
Genetic diversity Inbreeding coefficient Heterozygosity Mating system Outcrossing rate Population sizeNotes
Acknowledgments
Funding for this study was awarded to R.B.S. through grants from Adkins Arboretum, Georgia Native Plant Society, North Carolina Native Plant Society, and the Department of Plant Biology at the University of Georgia. R.B.S. was supported in part by a National Science Foundation Graduate Research Fellowship. The authors thank M. Boyd, C. Deen, A. Tull, and B. Waitman for lab, field, and greenhouse assistance and Coweeta Hydrological Station and the Wykle and Spoon families for permission to work on their properties. We thank L. Comita for writing the R programs and C. Heckel for help creating the map figure. S. Hubbell, J. Leebens-Mack, R. Mauricio, D. Waller and an anonymous reviewer provided helpful comments on earlier versions of this manuscript.
Supplementary material
References
- Allard RW (1975) Mating system and microevolution. Genetics 79:115–126PubMedGoogle Scholar
- Barrett SCH, Kohn JR (1991) Genetic and evolutionary consequences of small population size in plant: implications for conservation. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 3–30Google Scholar
- Booy G, Hendriks RJJ, Smulders MJM, Van Groenendael JM, Vosman B (2000) Genetic diversity and the survival of populations. Plant Biol 2:379–395CrossRefGoogle Scholar
- Brown AHD, Allard RW (1970) Estimation of the mating system in open-pollinated maize populations using isozyme polymorphisms. Genetics 66:133–145PubMedGoogle Scholar
- Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268CrossRefGoogle Scholar
- Cheliak WM, Pitel JA (1984) Techniques for starch gel electrophoresis of enzymes from forest tree species. Information report P1-X-42. Petawawa National Forestry Institute, Canadian Forest Service, Chalk River, ONGoogle Scholar
- Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond B Bio 267:1149–1152CrossRefGoogle Scholar
- de Vere N, Jongejans E, Plowman A, Williams E (2009) Population size and habitat quality affect genetic diversity and fitness in the clonal herb Cirsium dissectum. Oecologia 159:59–68CrossRefPubMedGoogle Scholar
- Dole J, Ritland K (1993) Inbreeding depression in two Mimulus taxa measured by multigenerational changes in the inbreeding coefficient. Evolution 47:361–373CrossRefGoogle Scholar
- Dudash MR (1987) The reproductive biology of Sabatia angularis L. (Gentianaceae). PhD Thesis, University of Illinois at Chicago, ChicagoGoogle Scholar
- Dudash MR (1990) Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44:1129–1139CrossRefGoogle Scholar
- Dudash MR (1991) Plant size effects on female and male function in hermaphroditic Sabatia angularis (Gentianaceae). Ecology 72:1004–1012CrossRefGoogle Scholar
- Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
- Farris MA, Mitton JB (1984) Population density, outcrossing rate, and heterozygote superiority in ponderosa pine. Evolution 38:1151–1154CrossRefGoogle Scholar
- Field DL, Ayre DJ, Whelan RJ (2005) The effect of local plant density on pollinator behavior and the breeding system of Persoonia bargoensis (Proteaceae). Int J Plant Sci 166:969–977CrossRefGoogle Scholar
- Fischer M, Matthies D (1998a) Effects of population size on performance in the rare plant Gentianella germanica. J Ecol 86:195–204CrossRefGoogle Scholar
- Fischer M, Matthies D (1998b) RAPD variation in relation to population size and plant fitness in the rare Gentianella germanica (Gentianaceae). Am J Bot 85:811–819CrossRefGoogle Scholar
- Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, CambridgeGoogle Scholar
- Ghazoul J, Liston KA, Boyle TJB (1998) Disturbance-induced density-dependent seed set in Shorea siamensis (Dipterocarpaceae), a tropical forest tree. J Ecol 86:462–473CrossRefGoogle Scholar
- Gilpin ME, Soulé ME (1986) Minimum viable populations: the processes of species extinctions. In: Soulé M (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 13-34Google Scholar
- Goudet J (2005) Hierfstat, a package for R to compute and test hierarchical F-statistics. Molec Ecol Notes 5:184–186CrossRefGoogle Scholar
- Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Phil Trans R Soc B 351:1291–1298CrossRefGoogle Scholar
- Hamrick JL, Nason JD (1996) Consequences of dispersal in plants. In: Rhodes OE, Chesser RK, Smith MH (eds) Population dynamics in ecological space and time. University of Chicago Press, Chicago, pp 203–236Google Scholar
- Harder LD, Barrett SCH (1996) Pollen dispersal and mating patterns in animal-pollinated plants. In: Lloyd DG, Barrett SCH (eds) Floral biology: studies on floral evolution in animal-pollinated plants. Chapman & Hall, New York, pp 140–190Google Scholar
- Heinrich B (1979) Resource heterogeneity and patterns of movement in foraging bumblebees. Oecologia 40:235–245CrossRefGoogle Scholar
- Hensen I, Oberprieler C (2005) Effects of population size on genetic diversity and seed production in the rare Dictamnus albus (Rutaceae) in central Germany. Conserv Genet 6:63–73CrossRefGoogle Scholar
- Herlihy CR, Eckert CG (2004) Experimental dissection of inbreeding and its adaptive significance in a flowering plant, Aquilegia canadensis (Ranunculaceae). Evolution 58:2693–2703PubMedGoogle Scholar
- Heschel MS, Paige KN (1994) Inbreeding depression, environmental stress, and population size variation in scarlet gilia (Ipomopsis aggregata). Conserv Biol 9:126–133CrossRefGoogle Scholar
- Heywood JS (1993) Biparental inbreeding depression in the self-incompatible annual plant Gaillardia pulchella (Asteraceae). Am J Bot 80:545–550CrossRefGoogle Scholar
- Hodgins KA, Barrett SCH (2006) Mating patterns and demography in the tristylous daffodil Narcissus triandrus. Heredity 96:262–270CrossRefPubMedGoogle Scholar
- Jennersten O (1988) Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conserv Biol 2:359–366CrossRefGoogle Scholar
- Kalisz S, Vogler DM, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884–887CrossRefPubMedGoogle Scholar
- Kéry M, Matthies D, Spillman HH (2000) Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J Ecol 88:17–30CrossRefGoogle Scholar
- Knight TM, Steets JA, Vamosi JC et al (2005) Pollen limitation of plant reproduction: pattern and process. Annu Rev Ecol Syst 36:467–497CrossRefGoogle Scholar
- Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952CrossRefGoogle Scholar
- Levin DA (1990) The seed bank as a source of genetic novelty in plants. Am Nat 135:563–572CrossRefGoogle Scholar
- Levin DA, Kerster H (1969) Density-dependent gene dispersal in Liatris. Am Nat 103:61–74CrossRefGoogle Scholar
- Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95CrossRefGoogle Scholar
- McCue KA, Holtsford TP (1998) Seed bank influences on genetic diversity in the rare annual Clarkia springvillensis (Onagraceae). Am J Bot 85:30–36CrossRefGoogle Scholar
- Menges ES (1991) Seed germination percentage increases with population size in a fragmented prairie species. Conserv Biol 5:158–164CrossRefGoogle Scholar
- Mitton JB, Linhart YB, Sturgeon KB, Hamrick JL (1979) Allozyme polymorphisms detected in mature needle tissue of ponderosa pine. J Hered 70:86–89Google Scholar
- Murawski DA, Hamrick JL (1991) The effect of the density of flowering individuals on the mating system of nine tropical tree species. Heredity 67:167–174CrossRefGoogle Scholar
- Nason JD, Ellstrand NC (1995) Lifetime estimates of biparental inbreeding depression in the self-incompatible annual plant Raphanus sativus. Evolution 49:307–316CrossRefGoogle Scholar
- NatureServe (2009) NatureServe explorer: an online encyclopedia of life [web application], version 7.1. NatureServe, Arlington, VA. http://www.natureserve.org/explorer
- Oostermeijer JGB (2000) Population viability analysis of the rare Gentiana pneumonanthe: the importance of genetics, demography and reproductive biology. In: Young AG, Clarke GM (eds) Genetics, demography and viability of fragmented populations. Cambridge University Press, Cambridge, pp 294–313Google Scholar
- Oostermeijer JGB, van Eijck MW, van Leeuwen NC, den Nijs JCM (1995) Analysis of the relationship between allozyme heterozygosity and fitness in the rare Gentiana pneumonanthe. J Evol Biol 8:739–759CrossRefGoogle Scholar
- Oostermeijer JGB, Luijten SH, den Nijs HCM (2003) Integrating demographic and genetic approaches in plant conservation. Biol Conserv 113:389–398CrossRefGoogle Scholar
- Paschke M, Abs C, Schmid B (2002) Effects of population size and pollen diversity on reproductive success and offspring size in the narrow endemic Cochlearia bavarica (Brassicaceae). Am J Bot 89:1250–1259CrossRefGoogle Scholar
- Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molec Ecol Notes 6:288–295CrossRefGoogle Scholar
- Pluess AR, Stöcklin J (2004) Genetic diversity and fitness in Scabiosa columbaria in the Swiss Jura in relation to population size. Conserv Genet 5:145–156CrossRefGoogle Scholar
- Raijmann LEL, van Leeuwen NC, Kersten R, Oostermeijer JGB, den Nijs HCM, Menken SBJ (1994) Genetic variation and outcrossing rate in relation to population size in Gentiana pneumonanthe L. Conserv Biol 8:1014–1026CrossRefGoogle Scholar
- Richards CM (2000) Inbreeding depression and genetic rescue in a plant metapopulation. Am Nat 155:383–394CrossRefPubMedGoogle Scholar
- Ritland K (1990) A series of FORTRAN computer programs for estimating plant mating systems. J Hered 81:235–237Google Scholar
- Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228CrossRefPubMedGoogle Scholar
- Robledo-Arnuncio JJ, Alía R, Gil L (2004) Increased selfing and correlated paternity in a small population of a predominantly outcrossing conifer, Pinus sylvestris. Molec Ecol 13:2567–2577CrossRefGoogle Scholar
- Routley MB, Mavraganis K, Eckert C (1999) Effect of population size on the mating system in a self-compatible, autogamous plant, Aquilegia canadensis (Ranunculaceae). Heredity 82:518–528CrossRefPubMedGoogle Scholar
- Schaal BA, Levin DA (1976) The demographic genetics of Liatris cylindracea Michx. (Compositae). Am Nat 110:191–206CrossRefGoogle Scholar
- Schoen DJ, Clegg MT (1984) Estimation of mating system parameters when outcrossing events are correlated. Proc Natl Acad Sci USA 81:5258–5262CrossRefPubMedGoogle Scholar
- Sih A, Baltus M-S (1987) Patch size, pollinator behavior, and pollinator limitation in catnip. Ecology 68:1679–1690CrossRefGoogle Scholar
- Soltis DE, Haufler CH, Darrow DC, Gastony GJ (1983) Starch-gel electrophoresis of ferns: a compilation of grinding buffers, gel and electrode buffers, and staining schedules. Am Fern J 73:9–27CrossRefGoogle Scholar
- Spigler RB (2007) The reproductive consequences of reduced population size in the biennial Sabatia angularis (Gentianaceae). PhD Thesis, University of GeorgiaGoogle Scholar
- Spigler RB, Chang S-M (2008) Effects of plant abundance on reproductive success in the biennial Sabatia angularis (Gentianaceae): spatial scale matters. J Ecol 96:323–333CrossRefGoogle Scholar
- USDA (2009) The plants database. National Plant Data Center, Baton Rouge, LA. http://plants.usda.gov
- van Geert A, Van Rossum F, Triest L (2008) Genetic diversity in adult and seedling populations of Primula vulgaris in a fragmented agricultural landscape. Conserv Genet 9:845–853CrossRefGoogle Scholar
- van Treuren R, Bijlsma R, van Delden W, Ouborg NJ (1991) The significance of genetic erosion in the process of extinction. I. Genetic differentiation in Salvia pratensis and Scabiosa columbaria in relation to population size. Heredity 66:181–189CrossRefGoogle Scholar
- van Treuren R, Bijlsma R, Ouborg NJ, van Delden W (1993) The effects of population size and plant density on outcrossing rates in locally endangered Salvia pratensis. Evolution 47:1094–1104CrossRefGoogle Scholar
- Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–158PubMedGoogle Scholar
- Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedGoogle Scholar
- Young AG, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418CrossRefGoogle Scholar
- Zhao R, Xia H, Lu B-R (2009) Fine-scale genetic structure enhances biparental inbreeding by promoting mating events between more related individuals in wild soybean (Glycine soja; Fabaceae) populations. Am J Bot 96:1138–1147CrossRefGoogle Scholar