Abstract
The negative effects of inbreeding depression on fragmented small populations are likely to be expressed more strongly after restoration efforts if regeneration processes have been highly restricted in degraded habitats. We examined the potential influences of inbreeding depression on a population of Nymphoides peltata (Menyanthaceae) restored from the remnant soil seed bank. A hand-pollination experiment demonstrated self-compatibility of a single remaining homostyle genet and significant inbreeding depression in selfed progeny, especially in parameters related to seedling growth (\(\updelta=0.5\)–0.6 for biomass, and \(\updelta=0.3\)–0.4 for relative growth rate). Our genetic analysis indicated that the presumed number of parents contributing to the current soil seed bank was only 2–8 genets and that a single sib-family dominated at each of three sampling sites. The results also showed that the selfed progeny of the homostyle genet were overwhelmingly dominant at two sites (86.8 and 94.7%). As a result, the growth performance of the seed bank seedlings was significantly reduced, to a level as low as that of the selfed progeny. Active restoration efforts to minimize the negative effects of the genetic bottleneck and continuous monitoring based on genetic and demographic study are recommended.
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References
Aparicio A, Guisande R (1997). Replenishment of the endangered Echinospartum algibicum (Genisteae, Fabaceae) from the soil seed bank. Biol. Conserv. 81:267–273
Balloux F, Amos W, Coulson T (2004). Does heterozygosity estimate inbreeding in real populations? Mol. Ecol. 13:3021–3031
Barrett SC, Kohn JR (1991). Genetic and evolutionary consequences of small population size in plants: Implications for conservation. In: Falk DA, Holsinger KE (eds). Genetics and Conservation of Rare Plants. Oxford University Press, New York, pp. 3–30
Bataillon TM, David JL, Schoen DJ (1996). Neutral genetic markers and conservation genetics: Simulated germplasm collections. Genetics 144:409–417
Charlesworth D, Charlesworth B (1987). Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18:237–268
Cornuet JM, Luikart G (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
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 44:1129–1139
Eckert CG, Barrett SCH (1994). Post-pollination mechanisms and the maintenance of outcrossing in self-compatible, tristylous, Decodon verticillatus (Lythraceae). Heredity 72:396–411
Environment Agency of Japan (2000) Threatened wildlife of Japan—Red data book, 2nd edn. Vascular plants, vol. 8. Japan Wildlife Research Center, Tokyo.
Fischer M, Matthies D (1998). Experimental demography of the rare Gentianella germanica: Seed bank formation and microsite effects on seedling establishment. Ecography 21:269–278
Frankham R (1995). Conservation genetics. Annu. Rev. Genetics 29:305–327
Friar EA, Ladoux T, Roalson EH, Robichaux RH (2000). Microsatellite analysis of a population crash and bottleneck in the Mauna Kea silversword, Argyroxiphium sandwicense ssp. sandwicense (Asteraceae), and its implications for reintroduction. Mol. Ecol. 9:2027–2034
Glück H (1924). Biologische und morphologishe Untersuchungen über Wasser- und Sumpfgewächse. IV. Untergetauchte und Schwimmblattflora. Gustav Fischer, Jenap
Goodnight KF, Queller DC (1999). Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol. Ecol. 8:1231–1234
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (ver 2.9.3). Available from 〈http://www.2.unil.ch/popgen/softwares/fstat.htm〉.
Hill WG, Robertson A (1966). The effect of linkage on limits to artificial selection. Genet. Res. 8:269–294
Hoffman AA, Parsons PA (1997). Extreme Environmental Change and Evolution. Cambridge University Press, Cambridge
Hufford KM, Mazer SJ (2003). Plant ecotypes: Genetic differentiation in the age of ecological restoration. Trends Ecol. Evol. 18:147–155
Husband BC, Schemske DW (1996). Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70
Keller LF, Waller DM (2002). Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230–241
Kirkpatrick M, Jarne P (2000). The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155:154–167
Koch M, Huthmann M, Bernhardt KG (2003). Cardamine amara L. (Brassicaceae) in dynamic habitats: Genetic composition and diversity of seed bank and established populations. Basic Appl. Ecol. 4:339–348
Konovalov DA, Manning C, Henshaw MT (2004). KINGROUP: A program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol. Ecol. Notes 4:779–782
Lande R (1994). Risk of population extinction from fixation of new deleterious mutations. Evolution 48:1460–1469
Lande R (1995). Mutation and conservation. Conserv. Biol. 9:782–791
Lande R, Schemske DW, Schultz ST (1994). High inbreeding depression, selective interference among loci, and the threshold selfing rate for purging recessive lethal mutations. Evolution 48:965–978
Lande R, Shannon S (1996). The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50:434–437
Lenssen JP, Dolle GE, Blom CWPM (1998). The effect of flooding in the recruitment of reed marsh and tall forb plant species. Plant Ecol. 139:13–23
Levin DA (1990). The seed bank as a source of genetic novelty in plants. Am. Nat. 135:563–572
Luijten SH, Dierick A, Gerard J, Oostermeijer JGB, Raijmann LEL, den Nijs HCM (2000). Population size, genetic variation, and reproductive success in a rapidly declining, self-incompatible perennial (Arnica montana) in The Netherlands. Conserv. Biol. 14:1776–1787
Lynch M, Conery J, Burger R (1995). Mutation accumulation and extinction of small populations. Am. Nat. 146:489–518
Madsen T, Shine R, Olsson M, Wittzell H (1999). Restoration of an inbred adder population. Nature 402:34–35
Mahy G, Vekemans X, Jacquemart AL (1999). Patterns of allozymic variation within Calluna vulgaris populations at seed bank and adult stages. Heredity 82:432–440
Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7:639–655
Marui H, Washitani I (1993). Heterostyly and seed production of Nymphoides peltata in Lake Kasumigaura (In Japanese). Syuseibutsugaku Kenkyu 17:59–63
McCue KA, Holtsford TP (1998). Seed bank influences on genetic diversity in the rare annual Clarkia springvillensis (Onagraceae). Am. J. Bot. 85:30–36
Middleton B (1999). Wetland restoration: Flood pulsing and disturbance dynamics. John Wiley & Sons, New York
Miller PS, Hedrick PW (2001). Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster. J. Evol. Biol. 14:595–601
Murray MG, Thompson WF (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8:4321–4325
Nei M, Maruyama T, Chakraborty R (1975). The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Newman D, Pilson D (1997). Increased probability of extinction due to decreased genetic effective population size: Experimental populations of Clarkia pulchella. Evolution 51:354–362
Nishihiro J, Araki S, Fujiwara N, Washitani I (2004). Germination characteristics of lakeshore plants under an artificially stabilized water regime. Aquat. Bot. 79:333–343
Nishihiro J, Kawaguchi H, Iijima H, Fujiwara N, Washitani I (2001) Conservation ecology ofNymphoides peltata in Lake Kasumigaura. Ecol. Civil Eng. 4:39–48
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. 313–334
Oostermeijer JGB, Luijten SH, den Nijs JCM (2003). Integrating demographic and genetic approaches in plant conservation. Biol. Conserv. 113:389–398
Oostermeijer JGB, van Eijck MW, den Nijs JCM (1994). Offspring fitness in relation to population size and genetic variation in the rare perennial plant species Gentiana pneumonanthe (Gentianaceae). Oecologia 97:289–296
Oostermeijer JGB, van’t Veer R, den Nijs JCM (1994). Population structure of the rare, long-lived perennial Gentiana pneumonanthe in relation to vegetation and management in the Netherlands. J. Appl. Ecol. 31:428–438
Ornduff R (1966). The origin of dioecism from heterostyly in Nymphoides (Menyanthaceae). Evolution 20:309–314
Petit RJ, El Mousadik A, Pons O (1998). Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12:844–855
Piry S, Luikart G, Cornuet JM (1999). BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J. Heredity 90:502–503
Presciuttini S, Toni C, Tempestini E, Verdiani S, Casarino L, Spinetti I, De Stefano F, Domenici R, Bailey-Wilson JE (2002) Inferring relationships between pairs of individuals from locus heterozygosities. BMC Genetics, 3
Pywell RF, Pakeman RJ, Allchin EA, Bourn NAD, Warman EA, Warler KJ (2002). The potential for lowland heath regeneration following plantation removal. Biol. Conserv. 108:247–258
Raymond M, Rousset F (1995). Genepop (version-1.2): Population genetics software for exact tests and ecumenicism. J. Hered 86:248–249
Reed DH (2005). Relationship between population size and fitness. Conserv. Biol. 19:563–568
Roberts HA, Feast PM (1973). Emergence and longevity of seeds of annual weeds in cultivated and undisturbed soil. J. Appl. Ecol. 10:133–143
Rowland J, Maun MA (2001). Restoration ecology of an endangered plant species: Establishment of new populations of Cirsium pitcheri. Restor. Ecol. 9:60–70
Schmidt K, Jensen K (2000). Genetic structure and AFLP variation of remnant populations in the rare plant Pedicularis palustris (Scrophulariaceae) and its relation to population size and reproductive components. Am. J. Bot. 87:678–689
Schoen DJ, Brown AHD (1993). Conservation of allelic richness in wild crop relatives is aided by assessment of genetic markers. Proc. Natl. Acad. Sci. 90:10623–10627
Smits AJM, Van Avesaath PH, Van der Velde G (1990). Germination requirements and seed banks of some nymphaeid macrophytes: Nymphaea alba L., Nuphar lutea (L.) Sm. and Nymphoides peltata (Gmel.) O. Kuntze. Freshwtr. Biol. 24:315–326
Takagawa S, Nishihiro J, Washitani I (2005). Safe sites for establishment of Nymphoides peltata seedlings for recovering the population from the soil seed bank. Ecol. Res. 20:661–667
Tallmon DA, Luikart G, Waples RS (2004). The alluring simplicity and complex reality of genetic rescue. Trends Ecol. Evol. 19:489–496
Uesugi R, Goka K, Nishihiro J, Washitani I (2004). Allozyme polymorphism and conservation of the Lake Kasumigaura population of Nymphoides peltata. Aquat. Bot. 79:203–210
Uesugi R, Tani N, Goka K, Nishihiro J, Tsumura Y, Washitani I (2005). Isolation and characterization of highly polymorphic microsatellites in the aquatic plant, Nymphoides peltata (Menyanthaceae). Mol. Ecol. Notes 5:343–345
van der Velde G, Giesen TG, van der Heijden L (1979) Structure, biomass and seasonal changes in biomass of Nymphoides peltata (Gmel.) O. Kuntze (Menyanthaceae), a preliminary study. Aquat. Bot., 7, 279–300
Wang Y, Wang QF, Guo YH, Barrett SCH (2005). Reproductive consequences of interactions between clonal growth and sexual reproduction in Nymphoides peltata: A distylous aquatic plant. New Phytol. 165:329–335
Washitani I, Osawa R, Namai H, Niwa M (1994). Patterns of female fertility in heterostylous Primula sieboldii under severe pollinator limitation. J. Ecol. 82:571–579
Weir BS, Cockerham CC (1984). Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Weisner SEB, Ekstam B (1993). Influence of germination time on juvenile performance of Phragmites australis on temporarily exposed bottoms: Implications for the colonization of lake beds. Aquat. Bot. 45:107–118
Acknowledgments
We thank the Kasumigaura River Office of MLIT (Ministry of Land, Infrastructure and Transport, Government of Japan) and the Japan Water Agency for permitting the use of plant materials and their experiment station for our hand-pollination experiment. We also thank J. Nishihiro, F. Ishihama, M. Honjo, and two anonymous reviewers for their valuable comments on the manuscript. This research was partly supported by a Grant-in-Aid for Fellows of the Japan Society for the Promotion of Science (17-52322).
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Takagawa, S., Washitani, I., Uesugi, R. et al. Influence of inbreeding depression on a lake population of Nymphoides peltata after restoration from the soil seed bank. Conserv Genet 7, 705–716 (2006). https://doi.org/10.1007/s10592-005-9107-4
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DOI: https://doi.org/10.1007/s10592-005-9107-4