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Pliocene–Pleistocene Ecological Niche Evolution Shapes the Phylogeography of a Mediterranean Plant Group

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Pliocene–Pleistocene Ecological Niche Evolution Shapes the Phylogeography of a Mediterranean Plant Group Received: 28 September 2017 | Revised: 2 March 2018 | Accepted: 3 March 2018 DOI: 10.1111/mec.14567 ORIGINAL ARTICLE Pliocene–Pleistocene ecological niche evolution shapes the phylogeography of a Mediterranean plant group C. Benıtez-Benıtez1 | M. Escudero2 | F. Rodrıguez-Sanchez 3 | S. Martın- Bravo1,† | P. Jimenez-Mej ıas4,† 1Area de Botanica, Departamento de Biologıa Molecular e Ingenierıa Bioquımica, Abstract Universidad Pablo de Olavide, Seville, Spain Estimating species ability to adapt to environmental changes is crucial to understand 2Department of Plant Biology and Ecology, their past and future response to climate change. The Mediterranean Basin has University of Seville, Seville, Spain 3Departamento de Ecologıa Integrativa, experienced remarkable climatic changes since the Miocene, which have greatly Estacion Biologica de Donana,~ Consejo influenced the evolution of the Mediterranean flora. Here, we examine the evolu- Superior de Investigaciones Cientıficas, Seville, Spain tionary history and biogeographic patterns of two sedge sister species (Carex, 4Department of Botany, Smithsonian Cyperaceae) restricted to the western Mediterranean Basin, but with Pliocene fossil Institution, Washington, DC, USA record in central Europe. In particular, we estimated the evolution of climatic niches Correspondence through time and its influence in lineage differentiation. We carried out a dated ı ı C. Ben tez-Ben tez, Area de Botanica, phylogenetic–phylogeographic study based on seven DNA regions (nDNA and Departamento de Biologıa Molecular e Ingenierıa Bioquımica, Universidad Pablo de ptDNA) and fingerprinting data (AFLPs), and modelled ecological niches and species Olavide, Seville, Spain. distributions for the Pliocene, Pleistocene and present. Phylogenetic and divergence Email: [email protected] time analyses revealed that both species form a monophyletic lineage originated in Funding information the late Pliocene–early Pleistocene. We detected clear genetic differentiation Spanish Ministry of Economy and Competitiveness, Grant/Award Number: between both species with distinct genetic clusters in disjunct areas, indicating the CGL2016-77401-P predominant role of geographic barriers limiting gene flow. We found a remarkable shift in the climatic requirements between Pliocene and extant populations, although the niche seems to have been relatively conserved since the Pleistocene split of both species. This study highlights how an integrative approach combining different data sources and analyses, including fossils, allows solid and robust infer- ences about the evolutionary history of a plant group since the Pliocene. KEYWORDS allopatric speciation, Carex sect. Phacocystis, genetic structure, niche conservatism, niche differentiation, species distribution modelling 1 | INTRODUCTION speciation patterns, it is crucial to understand how ecological require- ments evolve through time. An increasing number of studies on the The interplay of ecological and evolutionary processes shapes the dis- evolution of species climatic niches show that, although negligible tribution of species and the dynamics of speciation, dispersal, adapta- niche change may happen since the split of sister lineages (phyloge- tion and extinction, which results from geological and climatic changes netic niche conservatism, PNC; Ackerly, 2003; Harvey & Pagel, 1991; (Lavergne, Mouquet, Thuiller, & Ronce, 2010; Webb, Ackerly, McPeek, Wiens & Graham, 2005), there are also examples of ecological innova- & Donoghue, 2002). Therefore, to explain biogeographic and tion (niche shift) since the species’ divergence (Ackerly, 2003). One of the most recognized signatures of niche conservatism is †Both authors contributed equally to the senior authorship. the similarity of ecological preferences among closely related species 1696 | © 2018 John Wiley & Sons Ltd wileyonlinelibrary.com/journal/mec Molecular Ecology. 2018;27:1696–1713. BENITEZ-BENITEZ ET AL. | 1697 (Losos, 2008; Wiens & Graham, 2005), hypothesis previously identi- (Fiz-Palacios & Valcarcel, 2013; Rodrıguez-Sanchez, Perez-Barrales, fied by Darwin (1859) as a consequence of their relatively recent Ojeda, Vargas, & Arroyo, 2008). The progressive global cooling and common ancestry. In addition to shared ancestry, Grafen (1989) pro- local aridification already initiated during the late Miocene (Milne posed that niche similarity is also due to shared environmental con- & Abbott, 2002; Suc et al., 1995; Thompson, 2005) culminated straints and biogeographic history (Crisp & Cook, 2012; Losos, 2008; with the onset of the Mediterranean climatic regime during the Wiens & Graham, 2005). The niche conservatism idea has played an late Pliocene (3.4–2.8 Ma). This climatic progression modified the important role particularly in relation to climate change impacts composition and structure of the Mediterranean forests, which lost (Thuiller, 2003), as climatic tolerance limits the ranges of species elements from the pre-existing subtropical lauroid flora and began (Wiens & Graham, 2005), even at very large geographical and evolu- to resemble contemporary vegetation (Thompson, 2005). Remnants tionary scales (Crisp et al., 2009; Mairal, Sanmartın, & Pellissier, of such subtropical vegetation persisted in the form of relict ele- 2017). Holt (1996) related the absence of evolutionary change with ments mostly at the eastern or western parts of the basin (Fernan- the difficulty for adaptive traits to evolve and stabilize in novel eco- dez-Mazuecos et al., 2016; Medail & Diadema, 2009; Mıguez, logical conditions. However, niches are rarely considered completely Gehrke, Maguilla, Jimenez-Mej ıas, & Martın-Bravo, 2017), as well conserved due to processes of local adaptation (Thompson, 2005; as in Mediterranean islands and Macaronesia (Medail & Diadema, Wiens & Graham, 2005). In particular, the presence of barriers that 2009; Medail & Quezel, 1997). The later Quaternary climatic oscil- limit expansion (e.g., mountain ranges; Taberlet, Fumagalli, Wust- lations (starting c. 2.5 Ma), characterized by the alternation of Saucy, & Cosson, 1998) may play a key role for niche evolution in colder (glacial) and warmer (interglacial) periods, strongly affected allopatric speciation (Wiens, 2004a), as the adaptation to ecological the distribution and genetic structure of species due to the recur- conditions could be associated with the constraints imposed in dif- rent range shifts (e.g., Gentili et al., 2015; Mansion et al., 2008). In ferent microhabitat preferences (Thompson, 2005). Moreover, recent this case, the Mediterranean Basin and Macaronesia served as gla- studies have demonstrated that niche differences could not always cial refugial areas (Gentili et al., 2015; Mairal et al., 2017; Medail be related to phylogenetic distances, as in some cases sister species & Diadema, 2009; Vargas, 2007), where the long-term persistence have not conserved the ancestral niche (Munkem€ uller,€ Boucher, of isolated sets of populations from ancestral species frequently Thuiller, & Lavergne, 2015; Revell, Harmon, & Collar, 2008). resulted in the formation of new allopatric lineages (Wiens, The assumption of niche conservatism has recently been further 2004b). The role of niche evolution in the biogeographic and challenged based on examples of rapid niche shifts during species diversification patterns of the Mediterranean Basin is crucial but diversification (Evans, Smith, Flynn, & Donoghue, 2009). Only niche still poorly understood. shift allows species to colonize and adapt to new habitats ecologi- Our study group is a complex of two closely related sister cally dissimilar from those on their ancestral areas (Spalink et al., species, Carex reuteriana Boiss. and Carex panormitana Guss. 2016), or persist in the same area after an environmental change. (Cyperaceae), allopatrically distributed in the western Mediterra- There is also evidence of niche shifts derived from biological inva- nean Basin (Figure 1), where they inhabit creeks and river shores sions (Broennimann et al., 2007; Stiels, Gaißer, Schidelko, Engler, & at low and medium altitudes (20–1,900 m; Luceno~ & Jimenez- Rodder,€ 2015). Large-scale shifts in plant species across biomes have Mejıas, 2008). C. reuteriana is endemic to the Iberian Peninsula also been revealed (e.g., Jara-Arancio et al., 2014; Koecke, Muellner- and northwestern Africa (Luceno~ & Jimenez-Mej ıas, 2008), and Riehl, Pennington, Schorr, & Schnitzler, 2013). The divergence of C. panormitana has a restricted distribution in Sardinia and in a ecologically relevant traits may have initially evolved sympatrically in few isolated populations in Sicily and Tunisia (Jimenez-Mej ıas, the past; however, range shifts resulting in small range overlap can Martın-Bravo, Amini-Rad, & Luceno,~ 2013; Pignatti, 1982; Urbani, promote high trait divergence (Anacker & Strauss, 2014) associated Gianguzzi, & Ilardi, 1995). A close phylogenetic relationship with the evolutionary specialization of species to a particular climatic between both disjunct taxa has been recently found (Global Carex regime (Thompson, 2005). Group, 2016). Currently, two subspecies are accepted for The Mediterranean Basin is considered one of the Earth’s hot C. reuteriana (Jimenez-Mej ıas, Escudero, Guerra-Cardenas, Lye, & spots of plant biodiversity regarding species richness and ende- Luceno,~ 2011): (i) C. reuteriana ssp. reuteriana, which shows a pat- mism (Medail & Quezel, 1997; Myers, Mittermeier, Mittermeier, da chy and disjunct distribution in the central and western
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