Testing reticulate versus coalescent origins of Erica lusitanica using a species phylogeny of the northern heathers (Ericeae, Ericaceae)☆
Graphical abstract
Introduction
Erica L. is among the largest genera of flowering plants (Frodin, 2004) with 830–840 species (Oliver and Oliver, 2003, Oliver and Forshaw, 2012). Most of the immense richness of Erica is endemic to the Cape Floristic Region (CFR) of South Africa, but species of Erica and closely related Calluna Salisb. and Daboecia D.Don (Ericaceae; Ericeae, commonly referred to as ‘heaths’ or ‘heathers’) are archetypal elements of open landscapes of Europe and surrounding areas, in both the Temperate and Mediterranean biomes. These northern heathers (Nelson, 2012) have been the subject of various empirical studies addressing evolutionary and ecological questions including the environmental factors dictating species distributions (Gil-López et al., 2014, Ojeda et al., 1998), and patterns of dispersal and genetic diversity (investigated for individual species by e.g. Beatty and Provan, 2012, Désamoré et al., 2010, Désamoré et al., 2012). The tree heather, Erica arborea, in particular, has been investigated to infer dispersal patterns between Europe and Tropical East Africa (TEA) (Désamoré et al., 2010) and within TEA (Gizaw et al., 2013).
The geographically widespread E. arborea is very similar in gross morphology to another species found exclusively in Europe: E. lusitanica. They share a tall habit and white corollas, and have been grouped in different formal and informal classifications (e.g. Bentham, 1839; ‘Tree heathers’, Nelson, 2012). However, the interpretation of morphological variation in Erica is far from straightforward: there is evidence for extensive homoplasy of morphological characters (Oliver, 2000, Pirie et al., 2011). Floral characters may evolve rapidly, probably as adaptations to changing (pollinator) environments (Pirie et al., 2011, Rebelo et al., 1985, Van der Niet et al., 2014), and vegetative characters such as adaptations to recurrent fires (Ojeda et al., 2005) may have undergone similar shifts. As a result, the classic generic classification (Bentham, 1839, Hansen, 1950), based on such characters, has long been considered artificial (Hansen, 1950, Oliver, 2000). In E. lusitanica, micromorphological characters such as indumentum and seed coat sculpture appear more similar to some other northern species than they are to E. arborea (Fagúndez et al., 2010, Fagúndez and Izco, 2010, Nelson, 2012).
The obvious means to assess this kind of morphological complexity is the molecular phylogeny. However, E. lusitanica has not previously been included in phylogenetic analyses, nor have several other European species, and current knowledge of the relationship of species of Erica L. in general is limited. Evidence available to date suggests that the heathers (tribe Ericeae; Ericaceae, including Erica, Calluna and Daboecia) comprise a basal grade of ‘northern’, largely European, species (McGuire and Kron, 2005, Pirie et al., 2011) subtending a single, much larger, ‘southern’ clade (‘African/Malagasy Erica’; Pirie et al., 2011). Data that we collected in the course of ongoing work on the phylogeny of Ericeae confirmed this general pattern. The results that we report here showed much improved resolution between lineages of the northern grade, revealing strong conflict between phylogenetic trees based on plastid data and independent nuclear ITS with regard to the position of E. lusitanica.
This gene tree conflict raises an alternative hypothesis to explain homoplasy of morphological characters in E. lusitanica: instead of indicating parallel evolution of traits, it could be the result of hybridisation between morphologically dissimilar species (de Villiers et al., 2013). However, gene tree conflict can instead represent incomplete lineage sorting, being the result of coalescent stochasticity given a linear (rather than reticulate) species tree (Nichols, 2001).
As is the case in many empirical examples of gene tree conflict (Blanco-Pastor et al., 2012, de Villiers et al., 2013, Maureira-Butler et al., 2008, Pirie et al., 2009), both coalescent and reticulate scenarios are in principle plausible for E. lusitanica: The possibility of ancient hybridisation events cannot be ruled out since hybridisation between extant Erica species is documented: wild hybrids between European species include Erica × stuartii (MacFarl.) Mast. (E. tetralix L. × E. mackayana Bab.); Erica × veitchii Bean (E. arborea L. × E. lusitanica Rudolphi.); Erica × watsonii Benth. (E. ciliaris L. × E. tetralix); Erica × williamsii Druce. (E. vagans L. × E. tetralix); and Erica × nelsonii Fagúndez (E. tetralix × E. cinerea L.) (Fagúndez, 2006, Fagúndez, 2012, Nelson, 2012, Rose, 2007), and various further crosses have been achieved in cultivation (Nelson, 2012). Moreover, there are no obvious karyological barriers to homoploid hybridisation: polyploidy has not been reported in Erica and chromosome counts are constant at n = 12 for all studied species with the exception of the European species E. spiculifolia that is n = 18 (Nelson and Oliver, 2005). Coalescent stochasticity on the other hand can generally be assumed to result in greater or lesser differences between inferred gene trees depending in particular on effective population sizes through time (Nichols, 2001).
In this paper, we attempt to discern whether gene tree conflict in the northern Ericeae with regards to E. lusitanica is the result of reticulate evolution or coalescent processes. We present two independent gene trees from DNA sequences (1) of multiple plastid markers and (2) of nuclear ribosomal ITS; from samples representing multiple accessions of all northern species of Erica, Calluna vulgaris (L.) Hull and Daboecia cantabrica (Huds.) K.Koch and exemplar sampling of the large African/Madagascan Erica clade. We use coalescent simulations and ancestral state reconstructions of selected morphological characters, and use data concatenation and coalescence based approaches in order to infer and test reticulate and linear species trees under each assumption separately. Finally, we use these trees to reassess the hypotheses concerning colonisation of Tropical East Africa by the putatively closely related tree heather, Erica arborea.
Section snippets
Taxon sampling
We sampled multiple populations from across the geographic distributions of all 21 non-hybrid species and two subspecies of Erica recognised by Nelson (2012) within the northern area (including for the first time E. umbellata and E. maderensis, as well as E. platycodon and E. azorica not previously included in phylogenetic analyses of the genus), plus multiple accessions of Calluna vulgaris and Daboecia cantabrica (123 accessions in total). In addition, we sampled one naturally occurring
Phylogenetic inference
Trees inferred from individual chloroplast markers did not show supported topological conflict (data not shown), therefore the data were combined under the assumption of a single bifurcating chloroplast tree. For ITS, the total alignment length was 974, of which 31 positions were variable but parsimony uninformative and 271 parsimony informative (33 and 183 respectively, for Erica alone); CI = 0.85, RI = 0.89. For the concatenated plastid regions, the total alignment length was 10,222 positions,
A robust and representative phylogenetic hypothesis for northern Ericeae
The phylogenetic results presented here represent the first analysis including all northern species of Erica and a considerable improvement in resolution compared to previous work (McGuire and Kron, 2005, Pirie et al., 2011). Our results indicate the monophyly of most currently accepted species. A notable exception is the E. scoparia clade, or wind-pollinated ‘besom heaths’ (Nelson, 2012), formed by the south-western Mediterranean E. scoparia and its relatives of the Macaronesian islands (E.
Acknowledgments
The authors gratefully thank Mr. Kurt Kramer, Ms. Bettina Banse, the plant breeders and producers of the Azerca group, Mr. Michael Knaack and his team from Belvedere Garten in Vienna, the gardener’s team of the Botanical Garden in Bonn, and the Gartenbauzentrum team in Straelen for spending their valuable time and making available plant material for this study. Further material was kindly provided by Charles Nelson, various members of The Heather Society, and Fernando Ojeda. For financial
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This paper has been recommended for acceptance by Quan Wang Xiao.