Org Divers Evol (2017) 17:29–41 DOI 10.1007/s13127-016-0312-4 ORIGINAL ARTICLE Diversification of Caiophora (Loasaceae subfam. Loasoideae) during the uplift of the Central Andes Marina Micaela Strelin1 & José Ignacio Arroyo2,3 & Stella Fliesswasser5 & Markus Ackermann4,5 Received: 25 May 2016 /Accepted: 16 November 2016 /Published online: 29 November 2016 # Gesellschaft für Biologische Systematik 2016 Abstract Andean orogeny and the ecological changes that solve phylogenetic relationships among 19 Caiophora species followed promoted diversification in plant and animal line- (including different accessions). We also included 10 species ages since the Early Miocene. The angiosperm genus of the allied genera Blumenbachia and Loasa. Aosa rostrata Caiophora (Loasaceae, subfam. Loasoideae) comprises and Xylopodia klaprothioides were used as outgroups. around 50 species that are endemic to South America. These Phylogenetic reconstruction strongly supports the monophyly are distributed from southern Ecuador to Central Chile and of Caiophora, and although several clades within this genus Argentina. Bee pollination and distribution at low- are poorly supported, our study yielded a better infra-generic intermediate elevations probably represent the ancestral con- resolution than previous studies. The origin of Caiophora is dition in the lineage that includes Caiophora and its allied dated to the Early-Middle Miocene and can be related to the genera. The majority of Caiophora species grow at high ele- uplift of the Cordilleras Frontal and Principal and to Pacific vations in the Andes, where some depend on vertebrate polli- marine transgressions. According to our estimations, nation. Previous studies did not resolve phylogenetic relation- Caiophora began to diversify during the Middle-Late ships within Caiophora, which precluded the dating of the Miocene and this unfolding proceeded eastwards during the origin and divergence of this group. We used markers of one Pliocene and the Pleistocene, in parallel to the uplift of differ- nuclear (ITS) and one plastid region (trnSGCU-trnGUUC)to ent Andean mountain ranges. Keywords Diversification . Caiophora . Loasaceae, subfam. Electronic supplementary material The online version of this article Loasoideae . Diversification . Central Andes . Orogeny (doi:10.1007/s13127-016-0312-4) contains supplementary material, which is available to authorized users. * Marina Micaela Strelin Introduction [email protected] The diversification of a lineage can be promoted by intrinsic factors, e.g. the acquisition of an evolutionary novelty 1 Laboratorio Ecotono, INIBIOMA (Universidad Nacional del Comahue-CONICET), Pasaje Gutierrez 1125, 8400 Bariloche, Rio (Minelli and Fusco 2012), or by extrinsic factors. The latter Negro, Argentina can be either abiotic, e.g. orogeny and climate change (Bryson 2 Departamento de Ecología, Facultad de Ciencias Biológicas, et al. 2012;Solàetal.2013; Meng and Zhang 2013), or biotic, Pontificia Universidad Católica de Chile, Santiago, Chile e.g. changes in the selective regimes (Nylin et al. 2014), and 3 Instituto de Ecología & Biodiversidad (IEB-Chile), Casilla 653, emergence of new ecological niches (Muschick et al. 2012). Santiago, Chile Among the most striking examples of lineage diversification 4 Nees Institut für Biodiversität der Pflanzen, Rheinische are those related to Andean orogeny (Gamble et al. 2008; Friedrich-Wilhelms-Universität, Meckenheimer Allee 170, Antonelli et al. 2009;Chavesetal.2011;Drummondetal. 53115 Bonn, Germany 2012a). 5 Institut für Integrierte Naturwissenschaften – Biologie, Universität The Andean uplift started about 40 Ma during the Middle Koblenz-Landau, Universitätsstr. 1, 56070 Koblenz, Germany Eocene, but the most pronounced uplift events took place in 30 Strelin M.M. et al. the Late Oligocene-Middle Miocene (∼25 to 17 Ma), in the high-Andean environments. The recent origin of a two- Late Miocene-Early Pliocene (∼9 to 5 Ma) and in the Early species clade in Schizanthus (Solanaceae) from a presum- Pliocene-Pleistocene (∼5–less than 5 Ma) (Lamb et al. 1997). ably bee-pollinated ancestor is related to plant specializa- These events are linked to considerable diversification in an- tion on hummingbird pollination in high-Andean environ- giosperm lineages, e.g. Smith and Baum (2006), Särkinen ments (Perez et al. 2006). et al. (2012), Drummond et al. (2012a), Baranzelli et al. Loasaceae subfamily Loasoideae is a monophyletic lineage (2014) and Moré et al. (2015). In addition to acting as a dis- largely restricted to Central and South America. It comprises persion corridor for plant lineages, the rising Andes resulted in 13 genera and more than 220 species, being the most species- the formation of vicariant barriers fostering allopatric specia- rich group within Loasaceae. Nasa Weigend, the largest genus tion in lineages growing on the eastern and the western within the subfamily, has its centre of diversity in the Andean slopes or inhabiting different inner Andean valleys Amotape-Huancabamba Zone (northern Peru) (Mutke et al. (Luebert and Weigend 2014). Glaciations, which resulted 2014). The second largest genus, Caiophora C. Presl from the interplay between the Andean uplift and periods of (Fig. 1), shows its highest diversity in the area from northern intense cooling (Mercer and Sutter 1982; Clapperton 1983; Peru to northern Argentina. The ca. 50 species in this genus Zech et al. 2009; Rubioldo et al. 2001; Martini et al. 2012), are distributed from Ecuador to Central Chile and Argentina, constituted additional vicariant barriers between the middle between 2000 and 5000 m a.s.l. This genus is associated to Miocene and the Pliocene and during the Pleistocene (e.g. different Andean mountain ranges, and only a single species, Cosacov et al. 2010; Sérsic et al. 2011). Glaciations also fos- Caiophora arechavaletae Urb. & Gilg., is found in southern tered northward dispersal and displacement of different plant Brazilian and Uruguayan grasslands (Zuloaga et al. 2008). lineages (Palazzesi et al. 2012). Some Caiophora species, e.g. Caiophora cirsiifolia C. Presl, The rising of the Andes fostered plant lineage diversi- present phenotypic variants, which were defined on the basis fication not only through the generation of vicariant bar- of flower characteristics, e.g. corolla shape and nectar compo- riers, but also through the generation of high-elevation sition, as well as inflorescence and vegetative traits areas, which were vacant for colonization, e.g. high- (Ackermann and Weigend 2006). Andean species of Lupinus (Hughes and Eastwood Bee pollination is presumably the ancestral condition in 2006). Besides the origin of these high-elevation areas, Caiophora and its allied genera (Strelin et al. 2016a). In addi- unprecedented ecological conditions in these new envi- tion to bee-pollinated species, Caiophora also includes spe- ronmentsmayhavealsocontributedtoplantlineagedi- cies that rely on hummingbird pollination (Ackermann and versification (Antonelli and Sanmartín 2011; Särkinen Weigend 2006; Weigend et al. 2004)aswellasasingle et al. 2012; Luebert and Weigend 2014). For instance, rodent-pollinated species, Caiophora coronata (pollinated while altitude is believed to act as an environmental filter by the small rodent G. griseoflavus)(CocucciandSérsic on the diversity of bee communities (Hoiss et al. 2012) 1998). Despite the absence of pollinator records for and insect pollination tends to be negatively affected by Caiophora pentlandii (PaxtonexGraham)G.Donex altitude in the Andes (Arroyo et al. 1985), hummingbirds Loudon, this species is also believed to be pollinated by small diversified in a context of Andean uplift since the middle rodents, based on its floral and inflorescence morphology Miocene (∼15 Ma) (McGuire et al. 2014). Furthermore, (Ackermann and Weigend 2006). Previous work showed that some of these hummingbird lineages, e.g. Ensifera flower shape in Caiophora and allied taxa evolved in response ensifera and Patagona gigas, adapted their flight dynam- to bee, hummingbird and rodent pollination (Strelin et al. ics and their body size to high-elevation conditions in the 2016a). Andes (Altshuler et al. 2004). The Andean uplift also Although the monophyly of Caiophora was demonstrated fostered diversification in other vertebrate lineages, e.g. in previous phylogenetic analyses (Hufford et al. 2003, 2005; small rodents of the Sigmodontinae subfamily (Martinez Weigend et al. 2004), these studies included a restricted sam- et al. 2012 ). In fact, there is evidence that some rodent pling of this genus (10 out of the ∼50 Caiophora species in lineages in this subfamily, e.g. Graomys griseoflavus Hufford et al. 2005). Phylogenetic relationships between spe- (Cavides-Vidal et al. 1987)andPhyllotis xanthopygus cies of Caiophora are poorly resolved, presumably because (Nespolo et al. 1999), evolved adaptations to resist the previous phylogenetic inferences were based only on partial extreme environmental conditions characteristic of high- plastid DNA evidence. This impedes dating the origin of Andean environments. Since transitions from insect to Caiophora and the diversification events within the genus, hummingbird pollination are likely to take place in envi- which is crucial to better understand the effects that orogenic, ronments where insects are poorly represented (Cruden climatic and ecological factors may have had on the evolution 1972), adaptation to hummingbird pollination, and even- of this genus. tually to pollination by other vertebrates,