AAM Approximate Bayesian Computation Analysis of EST
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Aoki et al. 1 1 Approximate Bayesian computation analysis of EST-associated 2 microsatellites indicates that the broadleaved evergreen tree 3 Castanopsis sieboldii survived the Last Glacial Maximum in 4 multiple refugia in Japan 5 6 K Aoki1, I Tamaki2, K Nakao3, S Ueno4, T Kamijo5, H Setoguchi6, N 7 Murakami7, M Kato6, and Y Tsumura4,5 8 9 1United Graduate School of Child Development, Osaka University, 10 Suita, Osaka 565-0871, Japan, 2Gifu Academy of Forest Science 11 and Culture, Mino, Gifu 501-3714, Japan, 3Kansai Research Center, 12 Forestry and Forest Products Research Institute, Forest Research 13 and Management Organization, Kyoto, Kyoto 612-0855, Japan, 14 4Department of Forest Molecular Genetics and Biotechnology, 15 Forestry and Forest Products Research Institute, Forest Research 16 and Management Organization, Tsukuba, Ibaraki 305-8687, Japan, 17 5Faculty of Life and Environmental Sciences, University of Tsukuba, 18 Tsukuba, Ibaraki 305-8572, Japan, 6Graduate School of Human and 19 Environmental Studies, Kyoto University, Kyoto, Kyoto 606-8501, 20 Japan, 7Makino Herbarium, Tokyo Metropolitan University, Hachioji, 21 Tokyo 192-0397, Japan. 22 K. Aoki et al. 2 23 Correspondence: Saneyoshi Ueno, Department of Forest Molecular 24 Genetics and Biotechnology, Forestry and Forest Products Research 25 Institute, Forest Research and Management Organization, Tsukuba, 26 Ibaraki 305-8687, Japan; Tel. +81 29 829 8261; Fax. +81 29 874 27 3720; E-mail: [email protected] 28 29 Running title: ABC-based demographic history of Castanopsis 30 K. Aoki et al. 3 31 Abstract 32 Climatic changes have played major roles in plants’ evolutionary 33 history. Glacial oscillations have been particularly important, but 34 some of their effects on plants’ populations are poorly understood, 35 including the numbers and locations of refugia in Asian warm 36 temperate zones. In the present study, we investigated the 37 demographic history of the broadleaved evergreen tree species 38 Castanopsis sieboldii (Fagaceae) during the last glacial period in 39 Japan. We used approximate Bayesian computation (ABC) for model 40 comparison and parameter estimation for the demographic modelling 41 using 27 EST-associated microsatellites. We also performed the 42 species distribution modelling (SDM). The results strongly support a 43 demographic scenario that the Ryukyu Islands and the western parts 44 in the main islands (Kyushu and western Shikoku) were derived from 45 separate refugia and the eastern parts in the main islands and the 46 Japan Sea groups were diverged from the western parts prior to the 47 coldest stage of the Last Glacial Maximum (LGM). Our data indicate 48 that multiple refugia survived at least one in the Ryukyu Islands, and 49 the other three regions of the western and eastern parts and around 50 the Japan Sea of the main islands of Japan during the LGM. The 51 SDM analysis also suggests the potential habitats under LGM 52 climate conditions were mainly located along the Pacific Ocean side K. Aoki et al. 4 53 of coastal region. Our ABC-based study helps efforts resolve the 54 demographic history of a dominant species in warm temperate 55 broadleaved forests during and after the last glacial period, which 56 provides a basic model for future phylogeographical studies using 57 this approach. 58 59 Keywords: approximate Bayesian computation (ABC), demography, 60 phylogeography, glacial refugia, Castanopsis, species distribution 61 modelling (SDM) 62 63 K. Aoki et al. 5 64 INTRODUCTION 65 Glacial cycles during the Quaternary period have played important 66 roles in shaping the diversity patterns of contemporary populations 67 (Hewitt, 2000; Hewitt, 2004), even in the warm temperate zone 68 where the land was not covered with ice sheets (Tsukada, 1974; 69 Minato and Ijiri, 1976). Severe climatic oscillations drove repeated 70 north–south and highland–lowland migrations of communities and 71 ecosystems, thereby strongly affecting the genetic structure and the 72 distribution of organisms they hosted (reviewed in Taberlet et al., 73 1998; Hewitt, 1999; Hewitt, 2004). Thus, current geographic patterns 74 of genetic diversity within species reflect their responses to 75 expansions and contractions of their habitats associated with the 76 glacial cycles, particularly the numbers, sizes, and locations of 77 refugia; the timing and severity of bottlenecks; and the rates of 78 recolonization. 79 Molecular phylogeographic studies of the genetic structure of extant 80 populations have provided detailed insights into apparent glacial and 81 postglacial distributions of numerous species (Avise, 2000). Key 82 issues for phylogeographic analyses include the numbers and 83 locations of refugia, which are still uncertain, despite intensive recent 84 investigations, especially in Europe (Provan and Bennett, 2008b; K. Aoki et al. 6 85 Svenning et al., 2008; Stewart et al., 2010) and North America (Soltis 86 et al., 2006; Shafer et al., 2010). In Europe, Svenning et al. (2008) 87 found indications suggesting that temperate trees were probably 88 largely confined to the traditionally recognized southern refugia in 89 and around Mediterranean lowlands, but several boreal tree species 90 may have been widespread not only in these southern areas but also 91 in several areas of northern Europe during the Last Glacial Maximum 92 (LGM). Existence of previously unknown, or cryptic, northern refugia 93 have also been proposed (Birks and Willis, 2008; Provan and 94 Bennett, 2008a; Rull, 2009; Stewart et al., 2010; Parducci et al., 95 2012; Tzedakis et al., 2013; de Lafontaine et al., 2014) , based on 96 the phylogeographic patterns of several species together with 97 evidence from pollen and plant macrofossils. The eastern edge of 98 East Asia, including East China, Japan, and the Korean Peninsula, 99 harbors diverse of the temperate flora, and the effects of the 100 locations of refugia throughout Quaternary glacial cycles on the 101 current genetic structure are important (Qiu et al., 2011). For East 102 Asian temperate plants, the population fragmentation occurred 103 caused by fluctuations in sea level throughout the Quaternary, and 104 these taxa restricted to distinct refugia (Qiu et al., 2011). Recent 105 phylogeographic studies of the warm temperate trees in this region 106 also detected the multiple localized refugia (Huang et al., 2002; K. Aoki et al. 7 107 Cheng et al., 2005; Cheng et al., 2006; Wu et al., 2006; Lee et al., 108 2013; Lee et al., 2014; Xu et al., 2015), though most of them were 109 based on a single locus (chloroplast DNA). Tests of refugia models 110 using multi locus genetic data based on estimated impacts of 111 demographic events and the associated genetic processes to 112 patterns of species’ genetic variation can help to understand more 113 detailed history during and after the glacial periods. 114 Advances in population genetics have led to the development of 115 statistical approaches based on coalescent models for estimating 116 population genetic parameters, reconstructing demographic histories, 117 and testing related hypotheses using Bayesian or likelihood-based 118 frameworks (Knowles and Maddison, 2002). In these approaches, a 119 hypothesis is considered more probable than postulated alternatives 120 if all the available data are more likely under the applied model and 121 underlying assumptions (Hickerson et al., 2010). In addition, a more 122 versatile tool for phylogeographic analysis, termed the approximate 123 Bayesian computation (ABC), has been recently introduced. This 124 “likelihood-free” method relatively easily enables the formulation of 125 model-based inferences in a Bayesian setting for evaluating the 126 demographic or evolutionary scenarios (Pritchard et al., 1999). 127 Because it relies on only summary statistics (Beaumont et al., 2002) 128 rather than evaluations of the overall probability of the data, we can K. Aoki et al. 8 129 make models flexibly to conform to the situations and compare them 130 without much computational effort. ABC has been successfully used 131 very recently to estimate the demographic parameters relating to 132 various complex demographic scenarios and to assess the effects of 133 the past climatic oscillations (Gao et al., 2012; Budde et al., 2013; Li 134 et al., 2013; Liu et al., 2014a; Liu et al., 2014b; Louis et al., 2014; 135 Wang et al., 2016; Yoichi et al., 2016; Chen et al., 2017; Ren et al., 136 2017). 137 Following biogeographic scenarios have been proposed to 138 describe the glacial and postglacial history of Japan’s warm 139 temperate ecosystems based on fossilized pollen data and 140 reconstructions of past climate. The pollen record indicates that 141 refugial populations of broadleaved evergreen forests existed in the 142 warmer southern end of Kyushu in the main islands as well as in the 143 Ryukyu Islands and migrated northward from these southern refugia 144 after the LGM (Tsukada, 1974; Matsuoka and Miyoshi, 1998). 145 However, based on historical climate data and tolerance of cool 146 temperature of the component species of these forests, some 147 ecologists have proposed that these forests might also have survived 148 in multiple refugia along the Pacific coasts of the main islands as well 149 as on the southern end of Kyushu during the glacial periods (Maeda, 150 1980; Kamei and Research group for the biogeography from Würm K. Aoki et al. 9 151 Glacial, 1981; Nakanishi, 1996; Hattori, 2002). However, it has been 152 difficult to resolve the detailed demographic history of the plant 153 species currently inhabiting the broadleaved evergreen forests, 154 especially Castanopsis-type forest, because of the limited fossilized 155 pollen records and of the relatively slow molecular evolution of 156 chloroplast DNA in plants (Wolfe et al., 1987; Chase et al., 1993; 157 Aoki et al., 2005) and the extremely low levels of intraspecific 158 variation in the chloroplast DNA of Japanese broadleaved evergreen 159 species (Aoki et al., 2003; Aoki et al., 2004a; Aoki et al., 2016).