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Post-pollination barriers enable coexistence of pollinator-sharing ornithophilous Erica species

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Abstract

Some evolutionary radiations produce a number of closely-related species that continue to coexist. In such plant systems, when pre-pollination barriers are weak, relatively strong post-pollination reproductive barriers are required to maintain species boundaries. Even when post-pollination barriers are in place, however, reproductive interference and pollinator dependence may strengthen selection for pre-pollination barriers. We assessed whether coexistence of species from the unusually speciose Erica genus in the fynbos biome, South Africa, is enabled through pre-pollination or post-pollination barriers. We also tested for reproductive interference and pollinator dependence. We investigated this in natural populations of three bird-pollinated Erica species (Erica plukenetii, E. curviflora and E. coccinea), which form part of a large guild of congeneric species that co-flower and share a single pollinator species (Orange-breasted Sunbird Anthobaphes violacea). At least two of the three pre-pollination barriers assessed (distribution ranges, flowering phenology and flower morphology) were weak in each species pair. Hand-pollination experiments revealed that seed set from heterospecific pollination (average 8%) was significantly lower than seed set from outcross pollination (average 50%), supporting the hypothesis that species boundaries are maintained through post-pollination barriers. Reproductive interference, assessed in one population by applying outcross pollen three hours after applying heterospecific pollen, significantly reduced seed set compared to outcross pollen alone. This may drive selection for traits that enhance pre-pollination barriers, particularly given that two of the three species were self-sterile, and therefore pollinator dependent. This study suggests that post-pollination reproductive barriers could facilitate the coexistence of congeneric species, in a recent radiation with weak pre-pollination reproductive barriers.

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Acknowledgements

We thank Stuart Hall, Kylie Pires, Geraldine Jacobs, Caroli Diener, Genevieve Theron, Mvana Sibiya and Gina Arena for assistance with the pollination experiments, Sally Reece for allowing us to work at Lourensford Estate, and two anonymous referees for their comments which greatly improved the manuscript. This study was conducted under South African National Parks (CRC/2016-2017/020--2016/V1) and CapeNature permits (AAA043-00008-0056). AC was funded by the Department of Science and Innovation/National Research Foundation Centre of Excellent at the FitzPatrick Institute of African Ornithology, the South African National Biodiversity Institute, the Botanical Education Trust and the Claude Leon Foundation. CNS was partly funded by a BBSRC David Phillips Fellowship (BB/J014109/1).

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Authors and Affiliations

  1. FitzPatrick Institute of African Ornithology, DSI-NRF Centre of Excellence, University of Cape Town, Private Bag X3, Rondebosch, 7701, South Africa

    Anina Coetzee, Claire N. Spottiswoode & Colleen L. Seymour

  2. Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

    Claire N. Spottiswoode

  3. South African National Biodiversity Institute, Kirstenbosch Research Centre, Claremont, 7753, South Africa

    Colleen L. Seymour

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  1. Anina Coetzee
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  2. Claire N. Spottiswoode
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All authors designed the study, AC collected and analysed data, AC led the writing, to which all authors contributed critically.

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Correspondence to Anina Coetzee.

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Coetzee, A., Spottiswoode, C.N. & Seymour, C.L. Post-pollination barriers enable coexistence of pollinator-sharing ornithophilous Erica species. J Plant Res 133, 873–881 (2020). https://doi.org/10.1007/s10265-020-01226-8

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