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Dating the origin of the Orchidaceae from a fossil orchid with its pollinator

Abstract

Since the time of Darwin1, evolutionary biologists have been fascinated by the spectacular adaptations to insect pollination exhibited by orchids. However, despite being the most diverse plant family on Earth2, the Orchidaceae lack a definitive fossil record and thus many aspects of their evolutionary history remain obscure. Here we report an exquisitely preserved orchid pollinarium (of Meliorchis caribea gen. et sp. nov.) attached to the mesoscutellum of an extinct stingless bee, Proplebeia dominicana, recovered from Miocene amber in the Dominican Republic, that is 15–20 million years (Myr) old3. This discovery constitutes both the first unambiguous fossil of Orchidaceae4 and an unprecedented direct fossil observation of a plant–pollinator interaction5,6. By applying cladistic methods to a morphological character matrix, we resolve the phylogenetic position of M. caribea within the extant subtribe Goodyerinae (subfamily Orchidoideae). We use the ages of other fossil monocots and M. caribea to calibrate a molecular phylogenetic tree of the Orchidaceae. Our results indicate that the most recent common ancestor of extant orchids lived in the Late Cretaceous (76–84 Myr ago), and also suggest that the dramatic radiation of orchids began shortly after the mass extinctions at the K/T boundary. These results further support the hypothesis of an ancient origin for Orchidaceae.

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Figure 1: Holotype of Meliorchis caribea gen. et sp. nov.
Figure 2: Morphology and pollinarium placement of modern Goodyerinae and hypothetical reconstruction of floral morphology of Meliorchis caribea.
Figure 3: Cladogram showing the estimated position of Meliorchis among modern clades in the orchid subfamily Orchidoideae.
Figure 4: Fossil-calibrated molecular clock chronogram of the family Orchidaceae, based on 3 kilobases of plastid DNA ( matK and rbcL).

References

  1. 1

    Darwin, C. On the Various Contrivances by which British and Foreign Orchids are Fertilised by Insects, and on the Good Effects of Intercrossing (J. Murray, London, 1862)

    Google Scholar 

  2. 2

    Dressler, R. L. The Orchids: Natural History and Classification (Harvard Univ. Press, Cambridge, Massachusetts, 1981)

    Google Scholar 

  3. 3

    Iturralde-Vinent, M. E. & MacPhee, R. D. E. Age and paleogeography of Dominican amber. Science 273, 1850–1852 (1996)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Schmid, R. & Schmid, M. J. in Orchid Biology: Reviews and Perspectives Vol. 1 (ed. Arditti J.) 17–45 (Cornell Univ. Press, London, 1977)

    Google Scholar 

  5. 5

    Grimaldi, D. & Engel, M. S. Evolution of the Insects (Cambridge Univ. Press, New York, 2005)

    Google Scholar 

  6. 6

    Peñalver, E., Engel, M. S. & Grimaldi, D. Fig wasps in Dominican amber (Hymenoptera: Agaonidae). Am. Mus. Novit. 3541, 1–16 (2006)

    Article  Google Scholar 

  7. 7

    Camargo, J. M. F., Grimaldi, D. & Pedro, S. R. M. The extinct fauna of stingless bees (Hymenoptera: Apidae: Meliponini) in Dominican amber: Two new species and redescription of the male of Proplebeia dominicana (Wille and Chandler). Am. Mus. Novit. 3293, 1–24 (2000)

    Article  Google Scholar 

  8. 8

    Freudenstein, J. V. & Rasmussen, F. N. Sectile pollinia and relationships in Orchidaceae. Plant Syst. Evol. 205, 125–146 (1997)

    Article  Google Scholar 

  9. 9

    Singer, R. B. & Sazima, M. Flower morphology and pollination mechanism in three sympatric Goodyerinae orchids from southeastern Brazil. Ann. Bot. (Lond.) 88, 989–997 (2001)

    Article  Google Scholar 

  10. 10

    Poinar, G. O. & Danforth, B. N. A fossil bee from Early Cretaceous Burmese amber. Science 314, 614 (2006)

    CAS  Article  Google Scholar 

  11. 11

    Ren, D. Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science 280, 85–88 (1998)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Grimaldi, D. The co-radiations of pollinating insects and angiosperms in the Cretaceous. Ann. Mo. Bot. Gard. 86, 373–406 (1999)

    Article  Google Scholar 

  13. 13

    Crepet, W. L., Friis, E. M., Nixon, K. C., Lack, A. J. & Jarzembowski, E. A. Fossil evidence for the evolution of biotic pollination. Phil.Trans. R. Soc. London.B 333, 187–195 (1991)

    ADS  Article  Google Scholar 

  14. 14

    Crepet, W. L. Some aspects of the pollination biology of Middle Eocene angiosperms. Rev. Palaeobot. Palynol. 27, 213–238 (1979)

    Article  Google Scholar 

  15. 15

    Gandolfo, M. A., Nixon, K. C. & Crepet, W. L. Cretaceous flowers of Nymphaeaceae and implications for complex insect entrapment pollination mechanisms in early Angiosperms. Proc. Natl Acad. Sci. USA 101, 8056–8060 (2004)

    ADS  CAS  Article  Google Scholar 

  16. 16

    Heard, T. A. The role of stingless bees in crop pollination. Annu. Rev. Entomol. 44, 183–206 (1999)

    CAS  Article  Google Scholar 

  17. 17

    Roubik, D. W. Deceptive orchids with Meliponini as pollinators. Plant Syst. Evol. 222, 271–279 (2000)

    Article  Google Scholar 

  18. 18

    Freudenstein, J. V. & Rasmussen, F. N. What does morphology tell us about orchid relationships?—A cladistic analysis. Am. J. Bot. 86, 225–248 (1999)

    CAS  Article  Google Scholar 

  19. 19

    Herendeen, P. S. & Crane, P. S. in Monocotyledons: Systematics and Evolution (eds Rudall, P. J., Cribb, P. J., Cutler, D. F. & Humphries, C. J.) 1–21 (Royal Botanic Gardens, Kew, 1995)

    Google Scholar 

  20. 20

    Crepet, W. L. Insect pollination: a paleontological perspective. Bioscience 29, 102–107 (1979)

    Article  Google Scholar 

  21. 21

    Labandeira, C. C. Paleobiology: how old is the flower and the fly? Science 280 57–59 10.1126/science.280.5360.57 (1998)

    CAS  Article  Google Scholar 

  22. 22

    Chase, M. W. in Genera Orchidacearum Vol. 2 (eds Pridgeon, A. M., Cribb, P. J., Chase, M. W. & Rasmussen, F. N.) 1–5 (Oxford Univ. Press, New York, 2001)

    Google Scholar 

  23. 23

    Wikström, N., Savolainen, V. & Chase, M. W. Evolution of the angiosperms: calibrating the family tree. Proc. R. Soc. Lond. B 268, 2211–2220 (2001)

    Article  Google Scholar 

  24. 24

    Bremer, K. Early Cretaceous lineages of monocot flowering plants. Proc. Natl Acad. Sci. USA 97, 4707–4711 (2000)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Janssen, T. & Bremer, K. The age of major monocot groups inferred from 800+ rbcL sequences. Bot. J. Linn. Soc. 146, 385–398 (2004)

    Article  Google Scholar 

  26. 26

    van der Berg, C. et al. An overview of the phylogenetic relationships within Epidendroideae inferred from multiple DNA regions and recircumscription of Epidendreae and Arethuseae (Orchidaeceae). Am. J. Bot. 92, 613–624 (2005)

    Article  Google Scholar 

  27. 27

    Cameron, K. M. et al. A phylogenetic anlaysis of the Orchidaceae: evidence from rbcl nucleotide sequences. Am. J. Bot. 86, 208–224 (1999)

    Article  Google Scholar 

  28. 28

    Freudenstein, J. V. et al. An expanded plastid DNA phylogeny of Orchidaceae and analysis of jackknife branch support strategy. Am. J. Bot. 91, 149–157 (2004)

    CAS  Article  Google Scholar 

  29. 29

    Sanderson, M. J. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302 (2003)

    CAS  Article  Google Scholar 

  30. 30

    Friis, E. M., Pedersen, K. R. & Crane, P. R. Araceae from the Early Cretaceous of Portugal: Evidence on the emergence of monocotyledons. Proc. Natl Acad. Sci. USA 101, 16565–16570 (2004)

    ADS  CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank Y. Goldman for facilitating access to the amber inclusion discussed here, G. Romero for his assistance in the examination of herbarium specimens, and G. Alpert and D. Smith for assistance in the production of the fossil microphotographs. We thank B. Archibald, C. Bell, M. Chase, A. Knoll, R. van der Ham, D. Hewitt, C. Jaramillo, M. Patten, E. Pringle, J. Pringle and T. Quental for useful comments. This research was sponsored by grants from the Barbour Fund (Museum of Comparative Zoology) and the National Science Foundation (DDIG) to S.R.R. and N.E.P., and a grant from the Fulbright Junior Scholar programme to B.G.

Author Contributions S.R.R., B.G. and N.E.P. procured and curated the specimen. S.R.R., B.G. and R.B.S. reviewed herbaria specimens, analysed ancestral floral morphology, and coded and analysed morphological characters. S.R.R. and C.R.M. designed dating approaches and considered their interpretation. S.R.R. wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Santiago R. Ramírez.

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Supplementary information

Supplementary Information

This file contains Supplementary Figure 1 with Legend, detailing the fossil-calibrated molecular clock analyses presented in Figure 4; Supplementary Methods 1-6, showing the morphological character codes and the matrix used to explore the phylogenetic placement of M. caribea, the methodology used in the phylogenetic analyses and divergence time estimation, and additional comments on the palaeontology of fossil calibrations; Supplementary Tables 1-3, indicating herbarium specimens examined, age estimates obtained with different methods, and GenBank accession numbers; and Supplementary Notes, indicating additional cited references. (PDF 534 kb)

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Ramírez, S., Gravendeel, B., Singer, R. et al. Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448, 1042–1045 (2007). https://doi.org/10.1038/nature06039

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