Advertisement

Conservation Genetics

, Volume 18, Issue 6, pp 1317–1329 | Cite as

Keeping it in the family: strong fine-scale genetic structure and inbreeding in Lodoicea maldivica, the largest-seeded plant in the world

  • E. J. MorganEmail author
  • C. N. Kaiser-Bunbury
  • P. J. Edwards
  • F. Fleischer-Dogley
  • C. J. Kettle
Research Article

Abstract

The fine-scale spatial genetic structure (FSGS) of plant populations is strongly influenced by patterns of seed dispersal. An extreme case of limited dispersal is found in the charismatic yet endangered palm Lodoicea maldivica, which produces large fruits (up to 20 kg) dispersed only by gravity. To investigate patterns of seed dispersal and FSGS in natural populations we sampled 1252 individual adults and regenerating offspring across the species’ natural range in the Seychelles archipelago, and characterised their genotypes at 12 microsatellite loci. The average dispersal distance was 8.7 ± 0.7 m. Topography had a significant effect on seed dispersal, with plants on steep slopes exhibiting the longest distances. FSGS was intense, especially in younger cohorts. Contrary to what might be expected in a dioecious species, we found high levels of inbreeding, with most neighbouring pairs of male and female trees (≤10 m) being closely related. Nonetheless, levels of genetic diversity were relatively high and similar in the various sampling areas, although these differed in disturbance and habitat fragmentation. We discuss potential trade-offs associated with maternal resource provisioning of progeny, seed dispersal and inbreeding, and consider the implications of our findings for managing this globally significant flagship species.

Keywords

Coco de mer Dioecy Fine-scale spatial genetic structure Inbreeding Limited seed dispersal Seychelles Islands 

Notes

Acknowledgements

The authors thank the Seychelles Islands Foundation, Ravin de Fond Ferdinand Nature Reserve, Seychelles National Parks Authority, and GVI Seychelles for project support and permission to work in the Lodoicea forests. In particular Marc Jean-Baptiste, Wilna Accouche, Nancy Bunbury, Estephan Germain, Allen Cedras and Chris Mason-Parker for providing valuable advice and information, and facilitating field work. We also thank Gerry Rose and Fabio Lesperance who were invaluable field assistants, and Kirsti Määttänen for advice in the lab. Myriam Heuertz and three anonymous reviewers provided useful comments that allowed us to improve the manuscript. Permission to conduct research, and export of samples was approved by the Seychelles Bureau of Standards and the Ministry of Environment, Energy and Climate Change, respectively. Fragment analysis was conducted at the Genetic Diversity Centre (GDC), ETH Zürich. C.N.K.-B. received funding from the DFG (KA 3349/2-1).

Funding

This research was funded under grant number ETH-37 12-1 ETH, Zürich.

Supplementary material

10592_2017_982_MOESM1_ESM.pdf (214 kb)
Supplementary material 1 (PDF 214 KB)
10592_2017_982_MOESM2_ESM.pdf (211 kb)
Supplementary material 2 (PDF 211 KB)
10592_2017_982_MOESM3_ESM.pdf (238 kb)
Supplementary material 3 (PDF 238 KB)
10592_2017_982_MOESM4_ESM.pdf (150 kb)
Supplementary material 4 (PDF 150 KB)
10592_2017_982_MOESM5_ESM.pdf (190 kb)
Supplementary material 5 (PDF 190 KB)
10592_2017_982_MOESM6_ESM.pdf (194 kb)
Supplementary material 6 (PDF 194 KB)
10592_2017_982_MOESM7_ESM.pdf (194 kb)
Supplementary material 7 (PDF 194 KB)
10592_2017_982_MOESM8_ESM.pdf (190 kb)
Supplementary material 8 (PDF 189 KB)

References

  1. Araújo MRG, Melo Júnior AF, Menezes EV, Brandão MM, Cota LG, Oliveira DA, Royo VA, Vieira FA (2017) Fine-scale spatial genetic structure and gene flow in Acrocomia aculeata (Arecaceae): analysis in an overlapping generation. Biochem Syst Ecol 71:147–154CrossRefGoogle Scholar
  2. Baker HG, Cox PA (1984) Further thoughts on dioecism and islands. Ann Missouri Bot Gard 71:244–253CrossRefGoogle Scholar
  3. Baker BH, Miller JA (1963) Geology and geochronology of the Seychelles Islands and structure of the floor of the Arabian Sea. Nature 199:346–348CrossRefGoogle Scholar
  4. Banks SC, Peakall R (2012) Genetic spatial autocorrelation can readily detect sex-biased dispersal. Mol Ecol 21:2092–2105CrossRefPubMedGoogle Scholar
  5. Bawa K (1980) Evolution of dioecy in flowering plants. Ann Rev Ecol Syst 11:15–39CrossRefGoogle Scholar
  6. Blackmore S, Chin S-C, Chong Seng L et al (2012) Observations on the morphology, pollination and cultivation of coco de mer (Lodoicea maldivica (J F Gmel.) Pers., Palmae). J Bot 2012:1–13CrossRefGoogle Scholar
  7. Breed MF, Marklund MHK, Ottewell KM, Gardner MG, Harris JBC, Lowe AJ (2012) Pollen diversity matters: revealing the neglected effect of pollen diversity on fitness in fragmented landscapes. Mol Ecol 21:5955–5968CrossRefPubMedGoogle Scholar
  8. Browne L, Ottewell K, Karubian J (2015) Short-term genetic consequences of habitat loss and fragmentation for the neotropical palm Oenocarpus bataua. Heredity 115:389–395CrossRefPubMedPubMedCentralGoogle Scholar
  9. Choo J, Juenger TE, Simpson BB (2012) Consequences of frugivore-mediated seed dispersal for the spatial and genetic structures of a neotropical palm. Mol Ecol 21:1019–1031CrossRefPubMedGoogle Scholar
  10. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509CrossRefPubMedGoogle Scholar
  11. Darwin C (1877) The different forms of flowers on plants of the same species. John Murray, LondonCrossRefGoogle Scholar
  12. De Cauwer I, Dufay M, Cuguen J, Arnaud J-F (2010) Effects of fine-scale genetic structure on male mating success in gynodioecious Beta vulgaris ssp. maritima. Mol Ecol 19:1540–1558CrossRefGoogle Scholar
  13. Dick CW, Bermingham E, Lemes MR, Gribel R (2007) Extreme long-distance dispersal of the lowland tropical rainforest tree Ceiba pentandra L. (Malvaceae) in Africa and the Neotropics. Mol Ecol 16:3039–3049CrossRefPubMedGoogle Scholar
  14. Dick CW, Hardy OJ, Jones FA, Petit RJ (2008) Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Trop Plant Biol 1:20–33CrossRefGoogle Scholar
  15. Dransfield J, Uhl NW, Asmussen CB (2008) Genera Palmarum: the evolution and classification of palms, 2nd edn. Kew Publishing, KewGoogle Scholar
  16. Dubreuil M, Riba M, Gonzalez-Martinez SC, Vendramin GG, Sebastiani F, Mayol M (2010) Genetic effects of chronic habitat fragmentation revisited: strong genetic structure in a temperate tree, Taxus baccata (Taxaceae), with great dispersal capability. Am J Bot 97:303–310CrossRefPubMedGoogle Scholar
  17. Edwards PJ, Kollmann J, Fleischmann K (2002) Life history evolution in Lodoicea maldivica (Arecaceae). Nord J Bot 22:227–237CrossRefGoogle Scholar
  18. Edwards PJ, Fleischer-Dogley F, Kaiser-Bunbury CN (2015) The nutrient economy of Lodoicea maldivica, a monodominant palm producing the world’s largest seed. New Phytol 206:990–999CrossRefPubMedGoogle Scholar
  19. Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259CrossRefGoogle Scholar
  20. Fauvel AA (1909) Unpublished documents on the history of the Seychelles Islands anterior to 1810: together with a cartography enumerating 94 ancient maps and plans dating from 1501, and a bibliography of books and mss. concerning these islands. Government Printing Office, MaheGoogle Scholar
  21. Fauvel AA (1915) Le cocotier de mer des iles Seychelles (Lodoicea sechellarum). Annales du Musée colonial de Marseille 3:169–307Google Scholar
  22. Finger A, Kettle CJ, Kaiser-Bunbury CN, Valentin T, Mougal J, Ghazoul J (2012) Forest fragmentation genetics in a formerly widespread island endemic tree: Vateriopsis seychellarum (Dipterocarpaceae). Mol Ecol 21:2369–2382CrossRefPubMedGoogle Scholar
  23. Fischer BE, Fleischer-Dogley F (2008) Coco de mer: myth and eros of the sea coconut, 1st edn. AB Fischer, BerlinGoogle Scholar
  24. Fleischer-Dogley F, Kettle CJ, Edwards PJ, Ghazoul J, Määttänen K, Kaiser-Bunbury CN (2011) Morphological and genetic differentiation in populations of the dispersal-limited coco de mer (Lodoicea maldivica): implications for management and conservation. Diversity Distrib 17:235–243CrossRefGoogle Scholar
  25. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  26. Galen C, Shore JS, Deyoe H (1991) Ecotypic divergence in Alpine Polemonium viscosum: genetic structure, quantitative variation, and local adaptation. Evol Int J Org Evol 45:1218–1228Google Scholar
  27. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  28. Grivet D, Robledo-Arnuncio JJ, Smouse PE, Sork VL (2009) Relative contribution of contemporary pollen and seed dispersal to the effective parental size of seedling population of California valley oak (Quercus lobata, Née). Mol Ecol 18:3967–3979CrossRefPubMedGoogle Scholar
  29. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  30. Hardy OJ, Maggia L, Bandou E et al (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15:559–571CrossRefPubMedGoogle Scholar
  31. Hart TB, Hart JA, Murphy PG (1989) Monodominant and species-rich forests of the humid tropics: causes for their co-occurrence. Am Nat 133:613–633CrossRefGoogle Scholar
  32. Holland MM, Parson W (2011) GeneMarker(R) HID: a reliable software tool for the analysis of forensic STR data. J Forensic Sci 56:29–35CrossRefPubMedGoogle Scholar
  33. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  34. Ismail SA, Ghazoul J, Ravikanth G, Uma Shaanker R, Kushalappa CG, Kettle CJ (2012) Does long-distance pollen dispersal preclude inbreeding in tropical trees? Fragmentation genetics of Dysoxylum malabaricum in an agro-forest landscape. Mol Ecol 21:5484–5496CrossRefPubMedGoogle Scholar
  35. Ismail SA, Ghazoul J, Ravikanth G, Kushalappa CG, Uma Shaanker R, Kettle CJ (2014) Fragmentation genetics of Vateria indica: implications for management of forest genetic resources of an endemic dipterocarp. Conserv Genet 15:533–545CrossRefGoogle Scholar
  36. Ismail SA, Ghazoul J, Ravikanth G, Kushalappa CG, Uma Shaanker R, Kettle CJ (2017) Evaluating realized seed dispersal across fragmented tropical landscapes: a two-fold approach using parentage analysis and the neighbourhood model. New Phytol 214:1307–1316CrossRefPubMedGoogle Scholar
  37. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  38. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  39. Kettle CJ, Hollingsworth PM, Jaffré T, Moran B, Ennos RA (2007) Identifying the early genetic consequences of habitat degradation in a highly threatened tropical conifer, Araucaria nemorosa Laubenfels. Mol Ecol 16:3581–3591CrossRefPubMedGoogle Scholar
  40. Kramer AT, Ison JL, Ashley MV, Howe HF (2008) The paradox of forest fragmentation genetics. Conserv Biol 22:878–885CrossRefPubMedGoogle Scholar
  41. Lionnet G (1976) The double coconut of the Seychelles. West Aust Nut Tree Crops Assoc Yearb 2:6–20Google Scholar
  42. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425CrossRefGoogle Scholar
  43. Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273CrossRefPubMedGoogle Scholar
  44. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655CrossRefPubMedGoogle Scholar
  45. Morgan EJ, Määttänen K, Kaiser-Bunbury CN, Buser A, Fleischer-Dogley F, Kettle CJ (2016) Development of 12 polymorphic microsatellite loci for the endangered Seychelles palm Lodoicea maldivica (Arecaceae). Appl Plant Sci 4:1500119CrossRefGoogle Scholar
  46. Nazareno AG, dos Reis MS (2014) At risk of population decline? An ecological and genetic approach to the threatened palm species Butia eriospatha (Arecaceae) of Southern Brazil. J Hered 105:120–129CrossRefPubMedGoogle Scholar
  47. Oostermeijer JGB, Luijten SH, den Nijs JCM (2003) Integrating demographic and genetic approaches in plant conservation. Biol Conserv 113:389–398CrossRefGoogle Scholar
  48. Parisod C, Christin P-A (2008) Genome-wide association to fine-scale ecological heterogeneity within a continuous population of Biscutella laevigata (Brassicaceae). New Phytol 178:436–447CrossRefPubMedGoogle Scholar
  49. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  50. Peakall R, Ebert D, Scott LJ, Meagher PF, Offord CA (2003) Comparative genetic study confirms exceptionally low genetic variation in the ancient and endangered relictual conifer, Wollemia nobilis (Araucariaceae). Mol Ecol 12:2331–2343CrossRefPubMedGoogle Scholar
  51. Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701CrossRefPubMedGoogle Scholar
  52. Pither R, Shore JS, Kellman M (2003) Genetic diversity of the tropical tree Terminalia amazonia (Combretaceae) in naturally fragmented populations. Heredity 91:307–313CrossRefPubMedGoogle Scholar
  53. Procter J (1984) Vegetation of the granitic islands of the Seychelles. In: Stoddart DR (ed) Biogeography and ecology of the Seychelles Islands. Junk, Boston, pp 209–219Google Scholar
  54. Ramos SLF, Dequigiovanni G, Sebbenn AM, Lopes MTG, Kageyama PY, Vasconcelos de Macêdo JL, Kirst M, Veasey EA (2016) Spatial genetic structure, genetic diversity and pollen dispersal in a harvested population of Astrocaryum aculeatum in the Brazilian Amazon. BMC Genet 17:63CrossRefPubMedPubMedCentralGoogle Scholar
  55. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  56. Rosas F, Quesada M, Lobo JA, Sork VL (2011) Effects of habitat fragmentation on pollen flow and genetic diversity of the endangered tropical tree Swietenia humilis (Meliaceae). Biol Conserv 144:3082–3088CrossRefGoogle Scholar
  57. Savage AJP, Ashton PS (1983) The population structure of the double coconut and some other Seychelles palms. Biotropica 15:15–25CrossRefGoogle Scholar
  58. Seidler TG, Plotkin JB (2006) Seed dispersal and spatial pattern in tropical trees. PLoS Biol 4:e344CrossRefPubMedPubMedCentralGoogle Scholar
  59. Shapcott A, Rakotoarinivo M, Smith RJ, Lysakova G, Fay MF, Dransfield J (2007) Can we bring Madagascar’s critically endangered palms back from the brink? Genetics, ecology and conservation of the critically endangered palm Beccariophoenix madagascariensis. Bot J Linn Soc 154:589–608CrossRefGoogle Scholar
  60. Shapcott A, Quinn J, Rakotoarinivo M, Dransfield J (2012) Contrasting patterns of genetic diversity between two endangered palms with overlapping distributions, Voanioala gerardii (Arecoideae) and Lemurophoenix halleuxii (Arecoideae), from North-east Madagascar. Conserv Genet 13:1393–1408CrossRefGoogle Scholar
  61. Silvestrini M, McCauley DE, Zucchi MI, dos Santos FAM (2015) How do gap dynamics and colonization of a human disturbed area affect genetic diversity and structure of a pioneer tropical tree species? For Ecol Manag 344:38–52CrossRefGoogle Scholar
  62. Slatkin M (1985) Rare alleles as indicators of gene flow. Evol Int J Org Evol 39:53–65CrossRefGoogle Scholar
  63. Smouse PE, Peakall R, Gonzales E (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17:3389–3400CrossRefPubMedGoogle Scholar
  64. Tomlinson PB (2006) The uniqueness of palms. Bot J Linn Soc 151:5–14CrossRefGoogle Scholar
  65. Torimaru T, Tani N, Tsumura Y, Nishimura N, Tomaru N (2007) Effects of kin-structured seed dispersal on the genetic structure of the clonal dioecious shrub Ilex leucoclada. Evol Int J Org Evol 61:1289–1300CrossRefGoogle Scholar
  66. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  67. Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935CrossRefPubMedGoogle Scholar
  68. Vranckx G, Jacquemyn H, Muys B, Honnay O (2012) Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conserv Biol 26:228–237CrossRefPubMedGoogle Scholar
  69. Wahlund S (1928) Zusammensetzung von population und korrelationserscheinung vom standpunkt der vererbungslehre aus betrachtet. Hereditas 11:65–106CrossRefGoogle Scholar
  70. Wright S (1943) Isolation by distance. Genetics 28:114PubMedPubMedCentralGoogle Scholar
  71. Yampolsky C, Yampolsky H (1922) Distribution of sex forms in the phanerogamic flora (Bibliotheca genetica series). Gebrüder Borntraeger, LeipzigGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.ITES–Ecosystem ManagementETH ZürichZurichSwitzerland
  2. 2.Ecological Networks, Department of BiologyTU DarmstadtDarmstadtGermany
  3. 3.Singapore-ETH CentreSingaporeSingapore
  4. 4.Seychelles Islands FoundationVictoria, MahéSeychelles

Personalised recommendations