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Influence of inbreeding depression on a lake population of Nymphoides peltata after restoration from the soil seed bank

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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

    Article  Google Scholar 

  • Balloux F, Amos W, Coulson T (2004). Does heterozygosity estimate inbreeding in real populations? Mol. Ecol. 13:3021–3031

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Bataillon TM, David JL, Schoen DJ (1996). Neutral genetic markers and conservation genetics: Simulated germplasm collections. Genetics 144:409–417

    PubMed  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B (1987). Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18:237–268

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google 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 44:1129–1139

    Article  Google Scholar 

  • Eckert CG, Barrett SCH (1994). Post-pollination mechanisms and the maintenance of outcrossing in self-compatible, tristylous, Decodon verticillatus (Lythraceae). Heredity 72:396–411

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Frankham R (1995). Conservation genetics. Annu. Rev. Genetics 29:305–327

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Glück H (1924). Biologische und morphologishe Untersuchungen über Wasser- und Sumpfgewächse. IV. Untergetauchte und Schwimmblattflora. Gustav Fischer, Jenap

    Google Scholar 

  • Goodnight KF, Queller DC (1999). Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol. Ecol. 8:1231–1234

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hoffman AA, Parsons PA (1997). Extreme Environmental Change and Evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Hufford KM, Mazer SJ (2003). Plant ecotypes: Genetic differentiation in the age of ecological restoration. Trends Ecol. Evol. 18:147–155

    Article  Google Scholar 

  • Husband BC, Schemske DW (1996). Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70

    Article  Google Scholar 

  • Keller LF, Waller DM (2002). Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230–241

    Article  Google Scholar 

  • Kirkpatrick M, Jarne P (2000). The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155:154–167

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lande R (1994). Risk of population extinction from fixation of new deleterious mutations. Evolution 48:1460–1469

    Article  Google Scholar 

  • Lande R (1995). Mutation and conservation. Conserv. Biol. 9:782–791

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lande R, Shannon S (1996). The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50:434–437

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Levin DA (1990). The seed bank as a source of genetic novelty in plants. Am. Nat. 135:563–572

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lynch M, Conery J, Burger R (1995). Mutation accumulation and extinction of small populations. Am. Nat. 146:489–518

    Article  Google Scholar 

  • Madsen T, Shine R, Olsson M, Wittzell H (1999). Restoration of an inbred adder population. Nature 402:34–35

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7:639–655

    Article  PubMed  CAS  Google Scholar 

  • Marui H, Washitani I (1993). Heterostyly and seed production of Nymphoides peltata in Lake Kasumigaura (In Japanese). Syuseibutsugaku Kenkyu 17:59–63

    Google Scholar 

  • McCue KA, Holtsford TP (1998). Seed bank influences on genetic diversity in the rare annual Clarkia springvillensis (Onagraceae). Am. J. Bot. 85:30–36

    Article  Google Scholar 

  • Middleton B (1999). Wetland restoration: Flood pulsing and disturbance dynamics. John Wiley & Sons, New York

    Google Scholar 

  • Miller PS, Hedrick PW (2001). Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster. J. Evol. Biol. 14:595–601

    Article  Google Scholar 

  • Murray MG, Thompson WF (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8:4321–4325

    PubMed  CAS  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975). The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nishihiro J, Kawaguchi H, Iijima H, Fujiwara N, Washitani I (2001) Conservation ecology ofNymphoides peltata in Lake Kasumigaura. Ecol. Civil Eng. 4:39–48

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Oostermeijer JGB, Luijten SH, den Nijs JCM (2003). Integrating demographic and genetic approaches in plant conservation. Biol. Conserv. 113:389–398

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Ornduff R (1966). The origin of dioecism from heterostyly in Nymphoides (Menyanthaceae). Evolution 20:309–314

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998). Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12:844–855

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Raymond M, Rousset F (1995). Genepop (version-1.2): Population genetics software for exact tests and ecumenicism. J. Hered 86:248–249

    Google Scholar 

  • Reed DH (2005). Relationship between population size and fitness. Conserv. Biol. 19:563–568

    Article  Google Scholar 

  • Roberts HA, Feast PM (1973). Emergence and longevity of seeds of annual weeds in cultivated and undisturbed soil. J. Appl. Ecol. 10:133–143

    Article  Google Scholar 

  • Rowland J, Maun MA (2001). Restoration ecology of an endangered plant species: Establishment of new populations of Cirsium pitcheri. Restor. Ecol. 9:60–70

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tallmon DA, Luikart G, Waples RS (2004). The alluring simplicity and complex reality of genetic rescue. Trends Ecol. Evol. 19:489–496

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984). Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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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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Correspondence to Shinichi Takagawa.

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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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