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Phylogeographic Structure and Genetic Variation in Formica Ants

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Phylogeographic Structure and Genetic Variation in Formica Ants Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 912 Phylogeographic Structure and Genetic Variation in Formica Ants BY ANNA GOROPASHNAYA ACTA UNIVERSITATIS UPSALIENSIS UPPSALA 2003 Dissertation to be publicly examined in Lindahl-salen, EBC, Uppsala University, on Saturday, December, 20, 2003 at 10:00, for the degree of Doctor of Philosophy. The examination will be conducted in English. Abstract Goropashnaya, A. 2003. Phylogeographic Structure and Genetic Variation in Formica Ants. Acta Universitatis Upsaliensis. Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 912. 36 pp. Uppsala. ISBN 91-554-5818-1. The aim of this thesis is to study phylogeny, species-wide phylogeography and genetic diversity in Formica ants across Eurasia in connection with the history of biotic responses to Quaternary environmental changes. The mitochondrial DNA phylogeny of Palaearctic Formica species supported the subgeneric grouping based on morphological similarity. The exception was that F. uralensis formed a separate phylogenetic group. The mitochondrial DNA phylogeny of the F. rufa group showed the division into three major phylogenetic groups: one with the species F. polyctena and F. rufa, one with F. aquilonia, F. lugubris and F. paralugubris, and the third one with F. pratensis. West-east phylogeographic divisions were found in F. pratensis suggesting post-glacial colonization of western Europe and a wide area from Sweden to the Baikal Lake from separate forest refugia. In contrast, no phylogeographic divisions were detected in either F. lugubris or F. exsecta. Contraction of the distribution range to a single refugial area during the late Pleistocene and the following population expansion could offer a general explanation for the lack of phylogeographic structure across most of Eurasia in these species. Sympatrically distributed and ecologically similar species F. uralensis and F. candida showed clear difference in the phylogeographic structure that reflected difference in their vicariant history. Whereas no phylogeographic divisions were detected in F. uralensis across Europe, F. candida showed a well-supported phylogeographic division between the western, the central and the southern group. In socially polymorphic F. cinerea , the overall level of intrapopulation microsatellite diversity was relatively high and differentiation among populations was low, indicating recent historical connections. The lack of correspondence between genetic affinities and geographic locations of studied populations did not provide any evidence for differentiating between alternative hypotheses concerning the directions and sources of postglacial colonization of Fennoscandia. Keywords: Formica ants, phylogeography, phylogeny, Pleistocene refugia, population expansion, social organization Anna Goropashnaya, Department of Evolutionary Biology, Uppsala University, Norbyv. 18 D, SE-752 36 Uppsala, Sweden. © Anna Goropashnaya 2003 ISSN 1104-232X ISBN 91-554-5818-1 URN:NBN:se:uu:diva-3803 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-3803) A. " # $ Formica &' % ( b ) & ( A. " % * V. $ Formica rufa &' % (+ ,-! &accepted( A. " % * V. $ # $ . Formica pratensis F. lugubris &' % ( & ( " A. " % * V. $ . Formica excecta &' % ( ,-! & ( " A. " # / &0112( # Formica cinerea 21+ 031450323. CONTENTS Introduction 5 Pleistocene ice ages and their consequences 5 Formica ants 6 Genetic markers 7 Objectives 9 Results and Discussion 10 Phylogenetic relationships of Palaearctic Formica species 10 Limited phylogeographic structure across Eurasia in the ants Formica pratensis, F. lugubris and F. exsecta 16 Mitochondrial DNA variation in Formica uralensis and F. candida 23 Genetic characteristics of northern European populations of Formica cinerea 26 Conclusions 29 Acknowledgments 31 References 32 4 INTRODUCTION Pleistocene ice ages and their consequences During the Pleistocene, the climate underwent dramatic fluctuations due to the orbital eccentricity of the earth around the sun (cf. Bennett 1997). These climate oscillations were expressed in ice ages that lasted from 10 to 100 kyr, and relatively short warm interglacials. During the glacials, massive ice sheets partly covered the land, and vast continental areas represented Arctic desert and tundra (Andersen & Borns 1997). As a consequence, all forest biota could not survive in the changed environment but moved to more suitable habitats further to the south or to the sheltered and moist valleys in mountain areas (Stewart & Lister 2001). The last glaciation that started about 115 kyr before present (BP) was characterized by colder and warmer periods with the last glacial maximum 22-18 kyr BP (Andersen & Borns 1997). According to paleoecological data, the most of non-glaciated northern Eurasia during that stage was covered by treeless vegetation (West 2000). Therefore, forest species were confined to small areas with favorable conditions, i.e. refugia, where they could survive the glacials and then re- colonize previously unsuitable habitats during interglacials. Recent paleoecological and genetic studies suggest that refugia for boreal and temperate species occurred not only in Iberia, Italy and the Balkans as previously suggested (Hewitt 1996) but also in Central and Northern Europe, the southern Urals and Siberia, and on the coasts of the Azov and Black Seas (Lagercrantz & Ryman 1990; Bilton et al. 1998; Tarasov et al. 2000; Schmitt & Seitz 2001; Jaarola & Searle 2002; Brunhoff et al. 2003; Haase et al. 2003;). Past isolation in separate glacial refugia and following post-glacial colonization are reflected in genes and gene pools of extant species (Hewitt 1996). Separation in different glacial refugia generated intraspecific divergence, and the isolated gene pools were protected from mixing by hybrid zones during interglacials. Throughout several glacial periods refugial separation became reflected in the phylogeographic structure, i. e. significant association between the genealogical relationship and geographic distribution of alleles. Since forest remained only in restricted areas during the last glaciation, the refugial populations of many forest species were small. Therefore, genetic drift was a strong factor in those populations and could lead to loss of genetic variation within each refugium and genetic differentiation between different refugia in a short time. With the advent of favorable conditions, forest fauna and flora spread over the continent resulting in an admixture of different refugial populations and/or forming suture zones. Unlike 5 phylogeography based on relatively slow evolving insect mtDNA (2% per Myr; DeSalle et al. 1987), a population level analysis that takes into account not only the haplotype genealogy but also differentiation in haplotype frequencies, can reveal refugial separation over shallow time span of the last glaciation. The genetic signal of the past refugial separation is expected to be stronger in species with limited dispersal abilities. Demographic history of populations is also reflected in genes and gene pools (Rogers 1995; Kuhner et al. 1998). While the refugial and colonization history has been studied by using genetic markers in a number of boreal forest species in North America (cf. Arbogast &Kenagy 2001; Lessa et al. 2003), Eurasian species have received much less attention. Forest taxa studied to date across the Palaearctic are mostly avian species. More phylogeographic studies are needed to elucidate the post-glacial history of Eurasian forest biota. Although the routes of the re-colonization may have been unique for different species, evidence of shared refugia has emerged from molecular data on various taxa (Taberlet et al. 1998; Hewitt 1999). Formica ants Formica ants represent a large group of soil insects that occur mainly in the Holarctic. There are about 150 species of this genus a bigger part of which is distributed in the Nearctic and a smaller part in the Palaearctic. Many species are widespread and abundant, and they play an important role in ecosystems being active predators, tending aphids and improving soil composition. Most taxonomists have distinguished four subgenera in the European Formica species (e.g. Dlussky 1967): Raptiformica, Coptoformica, Serviformica, and Formica s. str. The subgeneric subdivision of the Formica ants based on morphology has been questioned and remained unclear, and an earlier study based on allozymes of 13 species did not help to solve the question. Taxonomy of the F. rufa group ants that belong to Formica s. str. has also been unstable mainly because of their morphological similarity and ability to hybridize and to form mixed colonies (cf. Czechowski 1996). Since ants of this group are strictly associated with forest, estimating the divergence time among the species can reveal the possible speciation effect of the Pleistocene environmental changes. Formica species demonstrate a great diversity of complex behavior and social organization. The subgenus Raptiformica includes slave-making species, and the subgenera Formica s. str. and Coptoformica use temporary parasitism as a mode of founding new colonies, while the species of 6 the subgenus Serviformica are used as slaves. The organization of colonies ranges from simple monogynous (single-
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