Genetic Consequences of Anagenetic Speciation in Endemic Angiosperms of Ullung Island, Korea

J. Jpn. Bot. 91 Suppl.: 83–98 (2016) Genetic Consequences of Anagenetic Speciation in Endemic Angiosperms of Ullung Island, Korea a, b c,d Koji TAKAYAMA *, Byung-Yun SUN and Tod Falor STUESSY aMuseum of Natural and Environmental History, Shizuoka, 5762, Oya, Suruga-ku, Shizuoka, 422-8017 JAPAN; bDepartment of Life Science, Chonbuk National University, Jeonju, 54896 KOREA; cHerbarium and Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, 1315, Kinnear Road, Columbus, OH 43212, U.S.A.; dDepartment of Botany and Biodiversity Research, University of Vienna, 14, Rennweg, A-1030, Vienna, AUSTRIA *Corresponding author: [email protected] (Accepted on March 3, 2016) Two major modes of speciation exist in the evolution of endemic plants of oceanic islands: cladogenesis and anagenesis. The former is where an immigrant population becomes established and then disperses into different ecological zones on the same, or neighboring, island. Over time and in isolation, these different lineages diverge and adapt to their new environments, such that eventually they are regarded as distinct species. These cladogenetic radiations have been chronicled in considerable detail in Hawaii, Galápagos, and the Canary Islands. Anagenesis is a process of transformation of species. After establishment, an immigrant population grows in size but does not split into divergent lines due to a lack of ecological opportunity. Gene flow is maintained among subpopulations, and genetic variation accumulates due to mutation and recombination. The highest known level of anagenesis in the endemic flora of any oceanic island occurs in Ullung Island, Korea. This small island lies 137 km east of the Korean Peninsula. It is of volcanic origin, with no known connections to the mainland. Here, ca. 33 endemic species occur that represent transformational evolution from original immigrants during the past not more than 1.8 million years. A number of studies in this island have been done on isozymic genetic variation in natural populations and more recently also using AFLP and SSR molecular markers. The results from isozymes show a pattern of very limited genetic variation within these endemic species. More comprehensive AFLP and SSR markers, however, reveal much higher levels of variation in some species, even to the extent of approximating that seen in progenitor populations on the continent. The studies in Ullung Island show that anagenetic species can be expected to harbor high levels of genetic variation similar to that of the progenitor population. The individuals in subpopulations on the island appear to be held together genetically by gene flow such that no geographic partitioning of the genetic variation occurs over the landscape. Key words: AFLP, evolution, isozymes, population genetics, SSR, Ullung-do. It has long been recognized that oceanic plant evolution (Carlquist 1974, Whittaker archipelagos provide opportunities for and Ferrández-Palacios 2009, Bramwell and understanding patterns and processes of Caujapé-Castells 2011). Islands are especially —83— 84 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue encompassing some 110 woody endemic species (Wagner et al. 1999), all apparently from a single founding event (Givnish et al. 2009). In the Canary Islands, genera such as Echium (Boraginaceae; Böhle et al. 1996), Dendrosonchus (Asteraceae; Kim et al. 1996a, b), and Aeonium (Crassulaceae; Mort et al. 2002, Jorgensen and Olesen 2001) have been intensively studied. In the Galápagos Islands, the largest genus Scalesia (Asteraceae) has also been examined (Eliasson 1974, Schilling et al. 1994, Nielsen 2004). Endemic plants of smaller oceanic Fig. 1. Location of Ullung Island. archipelagos, however, have also been investigated for processes of speciation. attractive as study sites of the origin of plant Important in this regard are the Juan Fernández diversity because they are surrounded by water Archipelago and the Bonin (Ogasawara) Islands. and hence isolated from other land masses, In the former, speciation has been studied in often hundreds or thousands of kilometers the largest genera (all Asteraceae), Dendroseris distant. It is compelling to ask questions as to (Sanders et al. 1987, Sang et al. 1994), how the colonizers arrived to the islands, from Robinsonia (Sanders et al. 1987, Crawford et where they came, and how they proliferated and al. 1993a, Sang et al. 1995, Takayama et al. diversified after arrival. 2015a), and Erigeron (Valdebenito et al. 1992, Among the evolutionary processes of interest López-Sepúlveda et al. 2015). Likewise, in the in plants of islands is speciation. Studies have Bonin Islands, speciation has been examined shown numerous different modes of speciation in Crepidiastrum (Ito and Ono 1990), Ilex in continental regions, such as allopatric (Setogouchi and Watanabe 2000), and others. speciation, peripatric speciation, allopolyploidy, In nearly all of the above examples, the autopolyploidy, catastrophic speciation, and principal type of speciation examined has progenitor-derivative speciation, among others been allopatric, whereby individuals from the (Grant 1981, Crawford 2010). In oceanic islands, founding lineage disperse into different habitats the options appear to be fewer, especially due and adapt to new environments. Usually the to a near absence of mechanisms involving morphology of each lineage transforms to such chromosome change during speciation (Carr an extent that a new species is recognized. This 1998, Stuessy and Crawford 1998, Weiss et al. process, therefore, is one of splitting of the 2002). original immigrant population and hence has As might be expected, many investigators been referred to as cladogenesis (Rensch 1947, have focused on speciation in large endemic 1960, Grant 1985). It is also an evolutionary groups of the Hawaiian Islands, the Galápagos radiation based on rapid adaptation to new Islands, and the Canary Islands. Hawaii has environments, and hence, it is commonly also particularly received much attention due to known as adaptive radiation (Schluter 2000, its high level of endemism at the specific Givnish 2015). level (89%, Wagner et al. 1999). Perhaps But despite these examples of groups in most spectacular has been the evolution of oceanic islands originating by adaptive radiation, the lobelioid complex (Campanulaceae), this does not explain the origin of all endemic December 2016 Takayama et al.: Endemic angiosperms of Ullung Island 85 Table 1. Features of island systems, number of endemic species, and levels of anagenetic vs. cladogenetic speciation. Modified from Stuessy et al. (2006) Number Size Distance from Age Elevation Number of Anagenetic Cladogenetic Island system of islands (km2) mainland (km) (Myo) (m) endemic species speciation (%) speciation (%) Hawaii 8 16885 3660 5 4250 828 7 93 Canary 7 7601 100 21 3710 429 16 84 Tristan da Cuhna 4 208 2580 18 2060 27 33 67 Juan Fernández 3 100 600 4 1319 97 36 64 Cape Verde 12 4033 570 10 2829 68 37 63 Galápagos 16 7847 930 5 1707 133 43 57 Madeira 3 792 630 14 1862 96 48 52 Ogasawara 12 99 800 Tertiary 916 118 53 47 St Helena 1 123 1850 15 826 36 53 47 Ullung 1 73 130 2 984 37 88 12 species. Some immigrants never split and of the results of studies on speciation in Ullung diverge adaptively. Instead, after arrival they Island, especially at the genetic level. This is an increase in population size, accumulate genetic important island, because it represents a case of diversity through mutation and recombination, speciation so very different from the dramatic and slowly transform morphologically into adaptive radiations in other archipelagos. The what is recognized as a new species distinct purposes of this paper, therefore, are to: (1) from continental progenitors. Such a process is survey the genetic patterns within and among gradual and has been called anagenesis (Stuessy populations of endemic plant species on et al. 2006). Ullung island; (2) summarize these patterns To date, the oceanic island that has shown for an evaluation of the genetic consequences the highest level of anagenesis is Ullung Island, of anagenesis that have taken place; and (3) Korea (Fig. 1). Located 137 km E of the Korean compare these anagenetic trends with those seen Peninsula, it is a single oceanic island of 73 km2 in other oceanic archipelagos. reaching 984 m tall, and dated radiometrically as 1.8 myo (Kim 1985). It is also quite uniform Population genetics of endemic plant species ecologically (Kim 1988). The level of anagenesis on Ullung Island among the 36 endemic species of the island is A number of investigations on genetic at least 88% (Stuessy et al. 2006). Noteworthy diversity in endemic species of Ullung Island is that nearly all of the endemic species are the have been done previously using isozymes only endemics in their respective genera. The (Table 2). Park et al. (2010) investigated only exceptions are in Acer (Aceraceae), Carex genetic variation using eight enzymes within (Cyperaceae), and Viola (Violaceae), with two Scrophularia takesimensis, which is an species each. It is known, however, that in the endangered endemic species. High genetic case of Acer, the two species have each evolved diversity between populations was found. 79 anagenetically from different continental individuals were examined in four populations, progenitors (Pfosser et al. 2002a). Anagenetic which are the only known populations. All four speciation in Ullung Island, therefore, is the populations gave 11.1% polymorphic loci, an dominant form of speciation in the endemic average of 1.18 alleles per locus, mean observed vascular flora, and it is the highest level of heterozygosity in each of the populations (0.021, anagenesis known in any oceanic island (Table 1). 0.000, 0.006, 0.032; overall mean, 0.015), and What is needed at this time is a summary mean expected heterozygosity (0.020, 0.063, 86 The Journal of Japanese Botany Vol. 91 Centennial Memorial Issue Table 2. Genetic diversity based on isozymes in endemic species of Ullung Island (bold) plus continental relatives Number of Number of Species populations individuals PR HE HO A AE Reference sampled analyzed Campanula takesimana 6 300 7.14 0.021 0.014 1.07 1.03 Chung et al.

Load more