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Araucaria Species Edinburgh Research Explorer Evolutionary dynamics of emblematic Araucaria species (Araucariaceae) in New Caledonia Citation for published version: Gaudeul, M, Gardner, MF, Thomas, P, Ennos, RA & Hollingsworth, PM 2014, 'Evolutionary dynamics of emblematic Araucaria species (Araucariaceae) in New Caledonia: Nuclear and chloroplast markers suggest recent diversification, introgression, and a tight link between genetics and geography within species', BMC Evolutionary Biology, vol. 14, no. 1, 171. https://doi.org/10.1186/s12862-014-0171-6 Digital Object Identifier (DOI): 10.1186/s12862-014-0171-6 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: BMC Evolutionary Biology Publisher Rights Statement: © 2014 Gaudeul et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 06. Oct. 2021 Gaudeul et al. BMC Evolutionary Biology 2014, 14:171 http://www.biomedcentral.com/1471-2148/14/171 RESEARCH ARTICLE Open Access Evolutionary dynamics of emblematic Araucaria species (Araucariaceae) in New Caledonia: nuclear and chloroplast markers suggest recent diversification, introgression, and a tight link between genetics and geography within species Myriam Gaudeul1*, Martin F Gardner2, Philip Thomas2, Richard A Ennos3 and Pete M Hollingsworth2 Abstract Background: New Caledonia harbours a highly diverse and endemic flora, and 13 (out of the 19 worldwide) species of Araucaria are endemic to this territory. Their phylogenetic relationships remain largely unresolved. Using nuclear microsatellites and chloroplast DNA sequencing, we focused on five closely related Araucaria species to investigate among-species relationships and the distribution of within-species genetic diversity across New Caledonia. Results: The species could be clearly distinguished here, except A. montana and A. laubenfelsii that were not differentiated and, at most, form a genetic cline. Given their apparent morphological and ecological similarity, we suggested that these two species may be considered as a single evolutionary unit. We observed cases of nuclear admixture and incongruence between nuclear and chloroplast data, probably explained by introgression and shared ancestral polymorphism. Ancient hybridization was evidenced between A. biramulata and A. laubenfelsii in Mt Do, and is strongly suspected between A. biramulata and A. rulei in Mt Tonta. In both cases, extensive asymmetrical backcrossing eliminated the influence of one parent in the nuclear DNA composition. Shared ancestral polymorphism was also observed for cpDNA, suggesting that species diverged recently, have large effective sizes and/or that cpDNA experienced slow rates of molecular evolution. Within-species genetic structure was pronounced, probably because of low gene flow and significant inbreeding, and appeared clearly influenced by geography. This may be due to survival in distinct refugia during Quaternary climatic oscillations. Conclusions: The study species probably diverged recently and/or are characterized by a slow rate of cpDNA sequence evolution, and introgression is strongly suspected. Within-species genetic structure is tightly linked with geography. We underline the conservation implications of our results, and highlight several perspectives. Keywords: Admixture, Closely related species, Conifers, Diversification, Hotspot, Hybridization, Introgression, Phylogeography, Population genetics, Systematics * Correspondence: [email protected] 1UMR CNRS-MNHN-UPMC-EPHE 7205 ‘Institut de Systématique, Evolution, Biodiversité’, Muséum National d’Histoire Naturelle, 16 rue Buffon, CP 39, F-75005 Paris, France Full list of author information is available at the end of the article © 2014 Gaudeul et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Gaudeul et al. BMC Evolutionary Biology 2014, 14:171 Page 2 of 21 http://www.biomedcentral.com/1471-2148/14/171 Background genetics also provide information on the recent history Over the last decades, both theoretical and empirical and could be useful to detect the possible impacts of the investigations have underlined the continuum of evo- Quaternary climatic oscillations experienced by the New lutionary processes acting on populations and species Caledonian flora: in the southeast of the island, palyno- (e.g. [1-5]). Therefore, an increasing number of studies logical records suggested that vegetation alternated be- adopt an integrative approach and combine concepts, mo- tween rainforest and maquis from 120,000 to 50,000 yr lecular techniques and statistical tools from both areas to ago, and a compelling Araucaria decline was detected shed light on the evolutionary dynamics of closely related around 45,000 yr ago [31]. However, the location of poten- species. In such groups, species may undergo a process of tial refugia remains highly uncertain (but see [30,32]). divergence (with population differentiation as the first step) Populations that originate from the same refugia are ex- and reproductive isolation and, in different places or at dif- pected to form a genetically more or less homogeneous ferent times, may exchange genes through hybridization group compared to populations that colonized from dis- and introgression if reproductive isolation is not complete. tinct refugia [33]. Nevertheless, given the complex top- The speciation process lies at the heart of this interface be- ology of the island, with many physical barriers, genetic tween population genetics and phylogenetics, with many drift could have a strong influence on the genetic struc- questions that remain unanswered in most cases e.g. when ture relative to current gene flow, and cause significant and why did populations initially diverge? What were their differentiation among populations. relative geographic distributions (sympatry vs. allopatry)? Here, we studied species of the conifer genus Araucaria How did reproductive isolation emerge? Such questions Juss. (Araucariaceae) and were both interested in among- are crucial challenges faced by biologists to understand the species relationships and the distribution of within-species evolution of species, and to better preserve the mecha- genetic diversity across New Caledonia. The genus Arau- nisms generating diversity in the face of today’s major en- caria comprises a total of 19 species worldwide, 13 of vironmental threats. which are endemic to the archipelago. They usually occur New Caledonia is a biodiversity hotspot [6] with more as large populations, in a variety of ecological habitats than 3000 native angiosperm and 43 conifer species in (most often humid forest or maquis; [34]). Importantly, all an area of ca. 19000 km2. It is characterized by high en- species are confined to ultramafic soils –characterized by demism (77% for angiosperms and 100% for conifers; [7]). low fertility (low N, P, K), high concentrations of heavy Although it is of continental Gondwanan origin and geo- metals (e.g., Co, Cr, Ni) and low water-holding capacity graphically isolated (1500 km east of Australia), recent [35]– except A. montana Brongn. & Gris, which occurs studies have shown that the modern New Caledonian bio- on both ultramafic and non-ultramafic soils and A. colum- diversity largely originates from dispersal events and in naris Hook. and A. schmidii de Laub., which only occur on situ species radiations [8,9]. This is congruent with the calcareous and acidic soils, respectively. Araucaria trees long submersion of the island (ca. 65–37 Ma; [10,11]), and are long-lived, monoecious trees whose breeding system is radiations were probably favoured by environmental largely unknown. Pollen dispersal is wind-mediated and gradients –notably in terms of soil substrate, altitude and probably larger than seed dispersal, which mainly occurs climate– which have created a variety of habitats within a by gravity. However, secondary seed dispersal by animals small geographic area. Also, in contrast to what was long and strong winds is likely since
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