J Plant Res (2015) 128:73–90 DOI 10.1007/s10265-014-0666-7 REGULAR PAPER Progressive migration and anagenesis in Drimys confertifolia of the Juan Ferna´ndez Archipelago, Chile Patricio Lo´pez-Sepu´lveda • Koji Takayama • Josef Greimler • Daniel J. Crawford • Patricio Pen˜ailillo • Marcelo Baeza • Eduardo Ruiz • Gudrun Kohl • Karin Tremetsberger • Alejandro Gatica • Luis Letelier • Patricio Novoa • Johannes Novak • Tod F. Stuessy Received: 19 December 2013 / Accepted: 12 June 2014 / Published online: 8 October 2014 Ó The Author(s) 2014. This article is published with open access at Springerlink.com Abstract A common mode of speciation in oceanic populations of D. confertifolia and the continental species islands is by anagenesis, wherein an immigrant arrives and D. winteri and D. andina, and to test probable migration through time transforms by mutation, recombination, and routes between the major islands. Population genetic drift into a morphologically and genetically distinct spe- analyses were conducted using AFLPs and nuclear cies, with the new species accumulating a high level of microsatellites of 421 individuals from 42 populations genetic diversity. We investigate speciation in Drimys from the Juan Ferna´ndez islands and the continent. Drimys confertifolia, endemic to the two major islands of the Juan confertifolia shows a wide genetic variation within popu- Ferna´ndez Archipelago, Chile, to determine genetic con- lations on both islands, and values of genetic diversity sequences of anagenesis, to examine relationships among within populations are similar to those found within pop- ulations of the continental progenitor. The genetic results are compatible with the hypothesis of high levels of genetic Electronic supplementary material The online version of this variation accumulating within anagenetically derived spe- article (doi:10.1007/s10265-014-0666-7) contains supplementary material, which is available to authorized users. cies in oceanic islands, and with the concept of little or no P. Lo´pez-Sepu´lveda Á M. Baeza Á E. Ruiz A. Gatica Departamento de Bota´nica, Universidad de Concepcio´n, Laboratorio de Ecofisiologı´a Vegetal, Departamento de Biologı´a, Casilla 160-C, Concepcio´n, Chile Facultad de Ciencias, Universidad de La Serena, Casilla 599, La Serena, Chile K. Takayama The University Museum, The University of Tokyo, L. Letelier Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan Centro de Investigaciones en Ecosistemas, Universidad Nacional Auto´noma de Me´xico, C.P. 58190 Morelia, Michoaca´n, Mexico J. Greimler Á G. Kohl Department of Systematic and Evolutionary Botany, P. Novoa Biodiversity Center, University of Vienna, Rennweg 14, Jardı´n Bota´nico de Vin˜a del Mar, Corporacio´n Nacional Forestal, 1030 Vienna, Austria Camino El Olivar 305, Vin˜a del Mar, Chile D. J. Crawford J. Novak Department of Ecology and Evolutionary Biology and the Institute for Applied Botany and Pharmacognosy, University of Biodiversity Institute, University of Kansas, Lawrence, Veterinary Medicine, Veterina¨rplatz 1, 1210 Vienna, Austria KS 60045, USA T. F. Stuessy (&) P. Pen˜ailillo Herbarium, Department of Evolution, Ecology, and Organismal Instituto de Biologı´a Vegetal y Biotecnologı´a, Universidad de Biology, The Ohio State University, 1315 Kinnear Road, Talca, 2 Norte 685, Talca, Chile Columbus, OH 43212, USA e-mail: [email protected] K. Tremetsberger Department of Integrative Biology and Biodiversity Research, Institute of Botany, University of Natural Resources and Life Sciences, Gregor Mendel Straße 33, 1180 Vienna, Austria 123 74 J Plant Res (2015) 128:73–90 geographical partitioning of this variation over the land- and mutation. The final result is a new species that differs scape. Analysis of the probability of migration within the genetically and morphologically from its ancestor, with archipelago confirms colonization from the older island, levels of genetic variation approximating those of the Robinson Crusoe, to the younger island Alejandro Selkirk. progenitor species (Stuessy et al. 2006). Examples of this type of speciation are less frequent, but it has been docu- Keywords AFLPs Á Anagenesis Á Genetic variation Á mented in Dystaenia (Apiaceae; Pfosser et al. 2006) and Microsatellites Á Oceanic islands Á Migration Acer (Sapindaceae; Takayama et al. 2012a, b) of Ullung Island, Korea, and in Weigela (Caprifoliaceae; Yamada and Maki 2012) of the Izu Islands, Japan. The genetic conse- Introduction quences of anagenetic speciation show relatively high levels of genetic differentiation within and among popu- Patterns and processes of speciation in oceanic islands have lations of the island endemic relative to continental source long captured the attention of evolutionary biologists populations. Obviously, many factors impact levels of (Drake et al. 2002; Rosindell and Phillimore 2011; genetic variation within island populations, such as Schaefer et al. 2011; Stuessy and Ono 1998). Important breeding systems, island age, human impact, etc. (Stuessy attributes of oceanic islands, such as geographical isola- et al. 2013), but mode of speciation is particularly tion, clearly delimited area, and restricted fauna and flora, significant. have led to islands being regarded as natural laboratories Also important for understanding patterns and processes for the study of evolution. They offer countless opportu- of evolution in oceanic islands is inferring routes of nities for investigating evolutionary processes in detail, migration among islands within archipelagos. The classical especially for studying genetic, ecological, biogeographic, hypothesis regarding archipelagos has assumed a single reproductive, and morphological divergence (Moore et al. colonization event from a continental area first to the oldest 2002; Mort et al. 2002). island and subsequent colonization of the younger islands Numerous hypotheses and discussions regarding pro- (Juan et al. 2000; Gillespie and Roderick 2002), the so- cesses of speciation in oceanic islands have occurred called ‘‘progression rule’’ (Funk and Wagner 1995). (Carlquist 1974; Grant et al. 1996; Stuessy et al. 2006). The Although this concept relies on parsimony, which is not most commonly described speciation mechanism in islands unreasonable, other possibilities have been demonstrated, is through cladogenesis. In this process, after a single such as reverse colonization (Ballemain and Ricklefs 2008; introduction, numerous lineages diverge rapidly from the Carine et al. 2004), colonization followed by extinction, or founding population as they adapt to different habitats with migration from younger to older islands (Emerson 2002; appropriate adaptations (Schluter 2000). The genetic con- Juan et al. 2000). Obviously important also are availability sequence of this process is low level of genetic variation of transportation vectors (Gillespie and Roderick 2002) and within and among populations of each species (Baldwin adaptation and dispersal of propagules (Cowie and Holland et al. 1998; Crawford and Stuessy 1997; Emerson 2002; 2006). Johnson et al. 2000; Stuessy et al. 2006). Examples of this An appropriate group of islands in which to study ana- mechanism of divergence and speciation in oceanic islands genetic speciation and migration is the Juan Ferna´ndez are numerous, such as Aeonium (Crassulaceae) and Echium Archipelago, located in the Pacific Ocean 667 km W of (Boraginaceae) in the Canary Islands (Bo¨hle et al. 1996; continental Chile (33°S/78–80°W, Fig. 1). The archipelago Jorgensen and Olesen 2001), Dendroseris and Robinsonia consists of two main islands, Robinson Crusoe (=Masati- (Asteraceae) in the Juan Ferna´ndez Archipelago (Crawford erra) and Alejandro Selkirk (=Masafuera), separated by et al. 1998), Bidens (Asteraceae), Schiedea (Caryophylla- 181 kms. At present the islands are approximately of equal ceae), Cyanea, Lobelia and Trematolobelia (Lobeliaceae) size (50 km2, Stuessy 1995), but they differ in geological in the Hawaiian Islands (Givnish et al. 2009; Knope et al. age, c. 4 million years old for Robinson Crusoe Island and 2012; Price and Wagner 2004), and Scalesia (Asteraceae) 1–2 million years old for Alejandro Selkirk Island (Stuessy in the Gala´pagos Islands (Eliasson 1974; Schilling et al. et al. 1984). The native vascular flora of the archipelago 1994). includes 75 families, 213 genera, and 361 species, with a The other major type of speciation in oceanic islands is 12 % endemism at the generic level, and 60 % at the anagenesis, also called simple geographic or phyletic spe- specific level (Marticorena et al. 1998). ciation (Simpson 1953). In this case, after colonizers A suitable genus to study the genetic consequences of establish a population on a new island, the processes of anagenetic speciation and migration in the Juan Ferna´ndez drift, recombination, and mutation modify the composition Archipelago is Drimys (Winteraceae). The genus contains of the original pioneer population and over time genetic seven species distributed in Central and South America variation accumulates by the processes of recombination, (Ehrendorfer et al. 1979; Marquı´nez et al. 2009; Rodrı´guez 123 J Plant Res (2015) 128:73–90 75 Fig. 1 Geographical position of populations sampled of Drimys winteri and D. andina in continental Chile (a) and Drimys confertifolia in Robinson Crusoe (b) and Alejandro Selkirk (c) Islands and Quezada 2001; Smith 1943), two of which, D. andina the most probable migration route(s) of the endemic spe- and D. winteri (with two varieties, var. winteri and var. cies