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Active sexual reproduction but no sign of genetic diversity in range-edge populations of Vanilla roscheri Rchb. f. (Orchidaceae) in South Africa

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Abstract

In South Africa, the wild leafless Vanilla roscheri Rchb. f. (Orchidaceae) is distributed only on the banks of the Lake Sibaya in KwaZulu-Natal Coastal Forest in the iSimangaliso Wetland Park. It is the southernmost vanilloid orchid on the African continent and a species of high conservation priority with little understanding of its reproductive biology and levels of genetic diversity. Mating systems and pollination ecology of the species were assessed by in situ experiments, in addition to genotyping plants at 16 microsatellite markers. Allogamous but self-compatible, V. roscheri depends on pollinators to achieve sexual reproduction. Its natural fruit set (26.3 %) is the highest reported for a non-spontaneously self-pollinating Vanilla species. It was associated with numerous flower visitors including two female allodapine bees (Allodapula variegata and Allodape rufogastra, Xylocopinae), captured with pollinia stored on the hind legs, and one female anthophorine bee. On the other hand, we report an absence of genetic diversity and homozygosity of the South-African populations of V. roscheri for all the genetic markers. Given the preferential outbreeding, the high natural fruit set and the pollinator/visitor richness of V. roscheri in Sibaya, a high level of genetic diversity was expected, but this was not the case. We detected a counterintuitive situation between the results of reproductive biology and genetics, making sense once the population situation on the margins of the species distribution is included. The null diversity expressed through the homozygous monomorphic markers is a consequence of the range-edge localization of the populations, which may have been subjected to severe bottlenecks (due to long distance colonization or fragmentation) along with inbreeding, in the past. The analysis highlights the complementarity of the approaches for which the implications in terms of conservation of the species in South Africa are discussed.

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Acknowledgments

The authors thank the anonymous reviewers for their valuable comments on the manuscript. This work was performed under a research agreement with iSimangaliso Wetland Park Authority as hosting organization and Ezemvelo KwaZulu Natal Wildlife. iSimangaliso is a World Heritage Site listed for its natural attributes, including specifically the sense of place, rich biodiversity and rare and threatened species, and has as one of its goals, in addition to conservation, the stimulation of the economic development of the adjacent regions and the empowerment of local communities. The authors wish to thank Ezemvelo KwaZulu Natal Wildlife for collecting permits and their help in field trip organization and particularly Z. Diamini and his team of rangers for their precious logistic help during the forest experimentations in the Lake Sibaya. We acknowledge Dr. C. Eardley (Plant Protection Research Institute, South Africa) for bee identifications, Pr. S. Johnson (University of KwaZulu Natal, Pietermartizburg, South Africa), Dr. C. Peter (Rhodes University, Grahamstown, South Africa) for helpful discussions on South African orchids and their pollination and also T. François, A. Franck, C. Ajaguin, J.-B. Dijoux, K. Jade (Cirad Réunion), A. Chabirand (ANSES Réunion) and D. Pastou (FDGEDON Réunion) for their technical assistance. This work was partly funded by F.R.R.O.I. (Fédération des Recherches Réunion—Océan Indien) CORE-DIVGEN project, and La Réunion Regional Council fundings to University of La Réunion (Pluri-annual Biodiversité et Santé project & Annual ValOrchidSOOI project). It was also funded by a PhD grant to R. Gigant from the European Social Fund attributed by the Regional Council of La Réunion.

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Authors and Affiliations

  1. Cirad, Unité Mixte de Recherche C53 Peuplements Végétaux et Bioagresseurs en Milieu Tropical Université de la Réunion (UMR C53 PVBMT), 7 Chemin de l’Irat, Ligne Paradis, 97410, Saint Pierre, île de la Réunion, France

    Rodolphe L. Gigant, Alexandre De Bruyn & Michel Grisoni

  2. Université de la Réunion, UMR C53 PVBMT, 15 Avenue René Cassin, BP7151, 97715, Saint Denis Messag Cedex 9, île de la Réunion, France

    Rodolphe L. Gigant, Alexandre De Bruyn, Laurence Humeau, Thierry Pailler & Pascale Besse

  3. Threatened Plant Conservation Unit, Biodiversity Research, E-KwaZulu Natal Wildlife, P.O. Box 13053, Cascades, 3202, KwaZulu-Natal, South Africa

    Brigitte Church

  4. Université de la Réunion, Laboratoire de Chimie des Substances Naturelles et des Sciences des Aliments, 15 Avenue René Cassin, BP7151, 97715, Saint Denis Messag Cedex 9, île de la Réunion, France

    Anne Gauvin-Bialecki

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  1. Rodolphe L. Gigant
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  4. Laurence Humeau
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  5. Anne Gauvin-Bialecki
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Correspondence to Pascale Besse.

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Appendix

Appendix

List of specimen voucher information of South African V. roscheri deposited at the University Herbarium of Réunion Island (France)

REU09989; REU09987; REU09983; REU09982; REU09981; REU09980; REU09979; REU09977; REU09975; REU09974.

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Gigant, R.L., De Bruyn, A., Church, B. et al. Active sexual reproduction but no sign of genetic diversity in range-edge populations of Vanilla roscheri Rchb. f. (Orchidaceae) in South Africa. Conserv Genet 15, 1403–1415 (2014). https://doi.org/10.1007/s10592-014-0626-8

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