See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/318245071 Genetic Patterns of Myrceugenia correifolia, a Rare Species of Fog-Dependent Forests of Mediterranean Chile: Is I.... Article in Frontiers in Plant Science · July 2017 DOI: 10.3389/fpls.2017.01097 CITATIONS READS 0 75 6 authors, including: Fernanda Perez Felipe Hinojosa Pontifical Catholic University of Chile University of Chile 23 PUBLICATIONS 435 CITATIONS 52 PUBLICATIONS 1,226 CITATIONS SEE PROFILE SEE PROFILE Paz Montenegro Michel Cossio Veas University of Chile Pontifical Catholic University of Chile 2 PUBLICATIONS 0 CITATIONS 3 PUBLICATIONS 1 CITATION SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Unravelling global rules of species assembly: an experimental approach based on annual plant communities in semi-arid systems worldwide (AGORA). View project Paleo-geographic patterns v/s climate change in South America and the Antarctic Peninsula during the latest Cretaceous: a possible explanation for the origin of the Austral biota? View project All content following this page was uploaded by Felipe Hinojosa on 12 July 2017. The user has requested enhancement of the downloaded file. fpls-08-01097 July 4, 2017 Time: 19:18 # 1 ORIGINAL RESEARCH published: 06 July 2017 doi: 10.3389/fpls.2017.01097 Genetic Patterns of Myrceugenia correifolia, a Rare Species of Fog-Dependent Forests of Mediterranean Chile: Is It a Climatic Relict? Fernanda Pérez1,2*, Luis F. Hinojosa2,3, Gioconda Peralta1, Paz Montenegro3, Carla Irarrázabal1 and Michel Cossio1 1 Departamento de Ecología, Pontificia Universidad Católica de Chile, Santiago, Chile, 2 Institute of Ecology and Biodiversity, Santiago, Chile, 3 Departamento de Ciencias Ecológicas, Universidad de Chile, Santiago, Chile Rare species frequently occur in areas with microclimatic conditions that are atypical for their regions, but that were more common in the past, and that probably have operated as climatic refugia for a long time. Myrceugenia correifolia is a rare arboreal species that grows in deep canyons and hilltops of the Coast Range of north-central Chile between 30◦ and 35◦S. In the northern edge of its distribution M. correifolia Edited by: grows in small patches of fog-dependent forest surrounding by xeric vegetation. These Federico Luebert, forest formations are thought to be remnants of an ancient and continuous rainforest University of Bonn, Germany that according to some authors became fragmented during aridization of the Neogene Reviewed by: Cristian Torres, (Neogene relict) and to others during warm-dry cycles of the Pleistocene (glacial relicts). University of the Bío Bío, Chile Here we asked whether the northernmost populations of M. correifolia are Neogene José Murillo, relicts, glacial relicts, or the result of a recent northward colonization. To answer this National University of Colombia at Bogotá, Colombia question we examined genetic diversity and population divergence of M. correifolia using *Correspondence: microsatellite markers, tested various competing population history scenarios with an Fernanda Pérez approximate Bayesian computation (ABC) method, and complemented these data with [email protected] ecological niche modeling (ENM). We detected three genetic clusters with a distinctive Specialty section: latitudinal pattern (north, center, and south) and high levels of differentiation (FST D 0.36). This article was submitted to Demographic inference supported an admixture event 31 kya between two populations Evolutionary and Population Genetics, a section of the journal that diverged from an ancient population 139 kya. The admixture time coincides with Frontiers in Plant Science the beginning of a period of wet conditions in north-central Chile that extended from Received: 10 February 2017 33 to 19 kya and was preceded by dry and cold conditions. These results suggest Accepted: 06 June 2017 Published: 06 July 2017 that increased precipitation during glacial periods triggered northward expansion of the Citation: range of M. correifolia, with subsequent admixture between populations that remained Pérez F, Hinojosa LF, Peralta G, separated during interglacial periods. Accordingly, ENM models showed that suitable Montenegro P, Irarrázabal C and habitats for M. correifolia in north-central Chile were larger and less fragmented during Cossio M (2017) Genetic Patterns of Myrceugenia correifolia, a Rare the Last Glacial Maximum than at present, suggesting that northernmost populations of Species of Fog-Dependent Forests this species are glacial relicts. of Mediterranean Chile: Is It a Climatic Relict? Front. Plant Sci. 8:1097. Keywords: climatic relict, fog-dependent forest, Mediterranean climate, microsatellites, Pleistocene climatic doi: 10.3389/fpls.2017.01097 fluctuations, rare species Frontiers in Plant Science| www.frontiersin.org 1 July 2017| Volume 8| Article 1097 fpls-08-01097 July 4, 2017 Time: 19:18 # 2 Pérez et al. Genetic Patterns in Myrceugenia correifolia INTRODUCTION In the fog-dependent forest of north-central Chile arboreal species that are restricted to the Mediterranean region coexist Species with limited geographic distributions are considered with tree species that reach temperate latitudes. Phylogeographic more vulnerable to climatic changes and land use conversion studies have been conducted in two of them: Aextoxicon than widespread species, and therefore are of central concern punctatum, distributed from 30◦ to 43◦S(Núñez-Ávila and in conservation biology (Malcolm et al., 2006; Honnay and Armesto, 2006) and Drimys winteri, distributed between 30◦S Jacquemy, 2007). Rare species frequently occur in areas with and 55◦S(Jara-Arancio et al., 2012). Both species show a microclimatic conditions that are atypical for their regions but strong genetic divergence between populations located north of were more widespread in the past (Ohlemüller et al., 2008; 32◦S and other populations. Although in both studies RAPD Harrison and Noss, 2017). These species (or their marginal markers were used and no time estimation was therefore populations) are thought to be climatic relicts, that is, remnants made, strong divergence has been attributed to the onset of of past populations that have become fragmented by climate- aridity during Neogene (Núñez-Ávila and Armesto, 2006). No driven changes (Hampe and Jump, 2011; Woolbright et al., phylogeographic studies have been conducted in species of fog- 2014). In arid and semiarid regions, for example, many rare dependent forest with narrow distributions, and it is not known species that currently grow in isolated patches with local humid if their northernmost populations may also be considered to be conditions probably had wider distribution in the past (Herrera, climatic relicts. 1992; Thompson, 1999). Fragmentation and contraction of Myrceugenia is a genus of evergreen trees and shrubs endemic their distribution ranges might be triggered by the increased to southern South America with two disjunct dispersal centers, warming and reduced rainfall that occurred during Neogene one located in central Chile and the other in south-eastern Brazil (Neogene relicts), or maybe latter, during warm/dry cycles of the (Landrum, 1981). The species that reaches the most northern Pleistocene (glacial relicts) (Cox and Moore, 2010; Hampe and latitude in Chile is M. correifolia. Together with other four species Jump, 2011; Villagrán et al., 2004). it comprises a clade sister to the remainder of the genus. The The Mediterranean region of central Chile, one of the world’s crown node of this clade was dated to 24–17 Mya, suggesting plant diversity hotspots, has high levels of richness and endemism that the group evolved before the Neogene aridization (Murillo, (Villagrán, 1994; Armesto et al., 2007). Many tree species are 2011; Murillo et al., 2012). M. correifolia grows in remnants restricted to the Coast Range, where a chain of remnant forest of forest in the summits and deep valleys of the Coast Range formations extends as far north as 30◦S. At this latitude forest between 30◦390S and 35◦050S and, given its narrow distribution, patches are isolated on hilltops surrounded by xeric scrublands has been listed as rare (Benoit, 1989) and Endangered (EN, and fog interception by plants is the primary source of water Hechenleitner et al., 2005). Even so, this species forms relatively (Squeo et al., 2005). Winter rains caused by westerly storm large populations in the northern edge of its distribution, and fronts supply increasing humidity southward. The northernmost together with A. punctatum dominates the relict fog-dependent forest formations, including those of the Fray Jorge–Talinay forest formations of Fray Jorge–Talinay and Santa Inés. However, National Park, have high floristic similarity with temperate forests M. correifolia is more tolerant to drought and occurs on drier soils of southern Chile located 1,000 km to the south that have (Salgado-Negret et al., 2013). puzzled biogeographers for a century (Philippi, 1884; Looser, Here we examined genetic diversity and population 1935; Muñoz and Pisano, 1947; Schmithüsen, 1956; Croizat, divergence of the rare Mediterranean species M. correifolia using 1962; Troncoso et al., 1980; Villagrán et al., 2004). Some authors microsatellite markers. In addition, we used the approximate have proposed that these forests are relicts of the Neogene Bayesian computation (ABC) approach to test different (Schmithüsen, 1956; Núñez-Ávila