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Journal of Biogeography (J. Biogeogr.) (2016) 43, 1717–1727 ORIGINAL Incipient radiation versus multiple ARTICLE origins of the Galapagos Croton scouleri (Euphorbiaceae) Beatriz Rumeu1,2*, Pablo Vargas1 and Ricarda Riina1 1Real Jardın Botanico (CSIC-RJB), Madrid, ABSTRACT Spain, 2Centre for Functional Ecology, Aim Island radiations imply the emergence of numerous species in a short Department of Life Sciences, University of period of time. Downscaling at the infraspecific level, considerable differentia- Coimbra, Coimbra, Portugal tion among populations can be a sign of ‘incipient radiation’. However, this process remains largely unexplored. We focus on one of the most outstanding cases of infraspecific morphological variation in the Galapagos flora. Our hypothesis is that the phenotypic variation of Croton scouleri is a sign of incipi- ent radiation, in which a single colonization has generated new lineages with considerable morphological differentiation. Location The Galapagos Islands and Neotropics. Methods One hundred and forty-four nuclear ribosomal DNA (ITS) and plastid trnL-F sequences of Croton sect. Adenophylli were used to test the hypothesis of a single ancestry (monophyly) of C. scouleri using a phylogenetic approach. Sequence data were analysed using Bayesian inference (BI) and max- imum likelihood (ML). A complementary phylogeographical analysis of C. scouleri and phylogenetically related species was also performed using 123 plastid sequences (trnL-F, petL-psbE, trnH-psbA) in search for common ances- try of Galapagos lineages. Results The phylogenetic approach revealed that the closest relatives of C. scouleri were C. alnifolius, C. pavonis and C. rivinifolius. However, we failed to support monophyly of C. scouleri populations. Despite finding numerous haplotypes (14 polymorphic sequences/9 substitution-based sequences), their distribution across Croton species prevented us from inferring common ances- try for C. scouleri. The phylogeographical reconstruction revealed multiple lin- eages related to the origin of C. scouleri. Main conclusions Lack of monophyly likely indicates that an incipient radia- tion from a single ancestor does not account for the striking infraspecific phe- notypic variation in C. scouleri. This morphological diversity could be explained by recurrent biogeographical connections between Galapagos and the mainland, involving multiple colonizations to the islands from the continent rather than back colonizations from the islands to the mainland. Morphologi- cal, reproductive, geographical and ecological evidence better support the sce- nario of recurrent colonizations from the continent in different periods of time. *Correspondence: Beatriz Rumeu, Centre for Functional Ecology, Department of Life Keywords Sciences, Calcßada Martim de Freitas, University Euphorbiaceae, ITS, leaf morphotypes, oceanic islands, petL-psbE, phylogeny, of Coimbra, 3000-456 Coimbra, Portugal. trnH-psbA trnL-F E-mail: [email protected] phylogeography, plastid DNA, , ª 2016 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1717 doi:10.1111/jbi.12753 B. Rumeu et al. geographical correlation (Wiggins & Porter, 1971). These INTRODUCTION characteristics make C. scouleri a good candidate to test the Oceanic islands harbour a great deal of evolutionary radia- hypothesis of incipient radiation on oceanic islands. tions. Characteristics such as isolation, niche availability, The endemic status of C. scouleri in the Galapagos involves topographic complexity or habitat heterogeneity of many the assumption that all its morphological variation results archipelagos favour diversification and adaptive evolution from a single ancestor that evolved within the archipelago. (Paulay, 1994). Therefore, some of the most striking plant However, this assumption has not been tested by any molec- and animal radiations documented to date have been found ular phylogenetic study, and thus the origin of the species on islands. Among the most significant examples are the remains unclear. Our working hypothesis is that the enor- Hawaiian honeycreepers (Freed et al., 1987) and lobeliads mous phenotypic variation in C. scouleri reflects an incipient (Givnish et al., 2009), the Macaronesian Echium L. (Garcıa- radiation from a single ancestor. The considerable isolation Maroto et al., 2009) and Aeonium Webb & Berthel. (Jor- of the Galapagos archipelago (c. 1000-km west of South gensen & Olesen, 2001), and the Galapagos Scalesia Arn. America) and the absence of diaspore specialization in Cro- (Blaschke & Sanders, 2009) and finches (Grant & Grant, ton for long-distance dispersal also points towards the 2008). hypothesis of a single colonization event (see Vargas et al., The process of evolutionary radiation involves the emer- 2012). Studies on phylogenetic relationships have helped gence of numerous lineages and species from a common identify single versus multiple origins of plants on oceanic ancestor in a short period of time (Schluter, 2000). However, islands based on monophyletic versus polyphyletic groups at the infraspecific level, considerable morphological differen- (see Silvertown, 2004). In this study, we test the monophyly tiation can be a sign of ‘incipient radiation’, where popula- of the Galapagos lineages of C. scouleri to establish single ori- tions with derived characters represent ‘infant’ lineages over gin from the continent. To this end, a large sample of Croton the course of radiation (Coyne & Orr, 2004; Balao et al., species from section Adenophylli from the Neotropics was 2010). Incipient or not, the first step for the proposal of any used to perform phylogenetic analyses. In addition, a com- radiation is to establish that the current diversification is a plementary phylogeographical approach was explored by consequence of a single origin (Schluter, 2000). In other reconstructing ancestral haplotypes and lineage relationships words, rapid differentiation associated with radiation needs within the Galapagos Islands. Genealogical relationships help to be preceded by colonization of a single lineage. Knowledge interpret incipient differentiation of insular and continental of the number of colonizations helps determine whether the morphotypes. range of morphological and ecological differentiation among species arose from single or multiple lineages. The same is MATERIALS AND METHODS true at a lower taxonomic level. Incipient radiations have been seldom documented and there is a lack of molecular Study species studies aimed at gaining a deeper insight into significant divergence of populations on islands. Croton scouleri has not been included in any molecular Croton scouleri Hook. f. (Euphorbiaceae) is the only spe- phylogeny; however, it was classified in the Neotropical cies on the Galapagos Islands belonging to the genus Croton Croton sect. Adenophylli on basis of morphological charac- L., one of the largest monophyletic genera within angios- ters (van Ee et al., 2011). The distribution of C. scouleri in perms (over 1200 spp., van Ee et al., 2011). This species is the volcanic archipelago of Galapagos encompasses 12 of endemic to the archipelago (Wiggins & Porter, 1971) and the 13 main islands (> 10 km2), being only absent from thus is interpreted as the result of a single colonization from the island of Baltra (Fig. 1). It is an abundant arborescent the Americas (Svenson, 1946b). Most Croton fruits are explo- shrub with a wide habitat range, occurring both in the sive capsules with no adaptations for long-distance dispersal. arid lowlands and moist uplands. Within sect. Adenophylli Nevertheless, C. scouleri is an abundant arborescent shrub (223 species), the narrow-leaved shape is not common and widely distributed across the Galapagos archipelago (Fig. 1). it is only found in a few species (e.g. C. sagraeanus Morphological variation within this species offers one of the Mull.Arg.€ from Cuba, C. linearis Jacq. from Bahamas, Flor- most outstanding cases of the Galapagos flora as revealed by ida, Cuba and Jamaica), including the C. scouleri on the its nine taxonomic varieties, of which four had been origi- Galapagos Islands [C. scouleri f. macraei (Hook. f.) G. L. nally described at the species level (see Wiggins & Porter, Webster, see Appendix S1b]. Croton scouleri was considered 1971). Indeed, variation in plant habit and especially leaf to be exclusively dioecious (Wiggins & Porter, 1971), shape of C. scouleri, led Hamann (1979) to speculate about despite the observation that most of the species of the an ‘early’ speciation within the archipelago. For instance, C. genus Croton are monoecious (van Ee et al., 2011). How- scouleri displays strong extremes in leaf shape, such as broad- ever, monoecy has also been recorded in few individuals leaved forms (see Appendix S1a in Supporting Information) of C. scouleri on the islands of Genovesa, Isabela and and narrow-leaved forms (see Appendix S1b). A wide span Espanola,~ with a frequency of 8–15% of monoecious indi- of intermediate or elliptic-leaved forms between these two viduals in the populations studied (Mauchamp, 1997) (see morphotypes are also frequent (Fig. 2), but show little also Fig. 2d). 1718 Journal of Biogeography 43, 1717–1727 ª 2016 John Wiley & Sons Ltd Origin of the Galapagos Croton scouleri VENEZUELA ECUADOR COLOMBIA GALÁPAGOS BRASIL PINTA PERU (2) BOLIVIA MARCHENA (2) GENOVESA (1) 0° SANTIAGO FERNANDINA (1) BALTRA PINZÓN (1) SANTA CRUZ (8) SANTA FÉ 1° S (1) SAN CRISTÓBAL ISABELA (4) 025 50 100 km FLOREANA (3) ESPAÑOLA (2) 92° W 91° W 90° W 89° W Figure 1 Map of the