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Reproductive barriers and genetic differentiation between continental and island populations of Epidendrum fulgens (Orchidaceae)

Abstract

Studies on insular organisms provide an important framework for investigating patterns of genetic differentiation and reproductive isolation. By focusing on populations of the same species, we have the opportunity to study the mechanisms operating during the earliest stages of speciation, as reproductive barriers can be examined among divergent lineages in a geographic context. We investigated the genetic differentiation and the evolution of early stages of intrinsic postmating reproductive isolation between continental and insular populations of Epidendrum fulgens, a neotropical orchid distributed in southeastern Brazil. Genetic diversity and structure were estimated for both nuclear and plastid markers by using genetic differentiation measures and model-based assignment test. Furthermore, two components of reproductive isolation were examined by analyzing fruit set and seed viability in interpopulation crosses. Strong plastid genetic structure (FST = 0.679) was found between insular and remaining populations, indicating that E. fulgens reduced gene flow via seed dispersal, although significant nuclear genetic structure was lower (DST = 0.179), likely due to the smaller effective population size of the plastid genome. Significant differences in seed viability between self- and cross-pollinated plants were found, indicating the occurrence of inbreeding depression in all populations. Seed viability was significantly lower in crosses between insular and remaining populations, suggesting a late postzygotic reproductive barrier due to low migration associated with genetic drift (i.e., bottleneck) and its consequences. Our results confirm the importance of islands as drivers for populational differentiation and suggest a central role for outbreeding depression during the early stages of lineage diversification.

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Fig. 1
Fig. 2

Modified from Pinheiro et al. (2011)

Fig. 3

Data availability

The datasets generated during and/or analyzed during the current study will be deposited on Dryad upon acceptance.

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Acknowledgements

We thank Lucia Rossi and Thais de Beauclair Guimarães for the assistance in sampling plants at Alcatrazes Island. The authors thank Espaço da Escrita – Pró-Reitoria de Pesquisa—UNICAMP—for the language services provided.

Funding

This research was supported by grants from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP-2009/15052–0, 2020/02150–3) to FP, fellowships from CNPq –PIBIC to GSV and FAEPEX (FUNCAMP) to TC. FP and CPS received fellowships in scientific productivity from CNPq (300927/2016–9; 300819/2016–1, respectively).

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FP and CPS participated in the study design and drafted the manuscript. GSV conducted the crossing experiments. CJNC analyzed the data from reproductive experiments. TCC genotyped the samples. All authors helped to draft the manuscript, read and approved the final version.

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Correspondence to Fábio Pinheiro.

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Online Resource 1. Results of assignment test performed with the software Maverick.

Online Resource 2. Fruit set of hand pollination experiments.

Online Resource 3. Description of nine plastid microsatellite haplotypes of Epidendrum fulgens.

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Pinheiro, F., Veiga, G.S., Chaves, C.J.N. et al. Reproductive barriers and genetic differentiation between continental and island populations of Epidendrum fulgens (Orchidaceae). Plant Syst Evol 307, 36 (2021). https://doi.org/10.1007/s00606-021-01759-y

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Keywords

  • Genetic drift
  • Gene flow
  • Inbreeding depression
  • Outbreeding depression
  • Reproductive isolation
  • Speciation