Genetic diversity of Collembola in Europe

Large parts of northern and central Europe were covered by ice sheets and permafrost due to climate changes in Europe during the last ice age (2.7 million to 11.7 kya). Plant and animal species had to adapt to lower temperatures, retreated to warmer areas in the south or went extinct. Once, after the Last Glacial Maximum (LGM, 26.5 kya to 19 kya) higher temperatures induced ice free habitats and these new habitats could be recolonized from different refugia. Collembola are one of the most abundant soil living decomposer animals and play a major role in aboveground - belowground interactions. Surprisingly, little is known about genetic and phylogeographic patterns, dispersal routes and anthropogenic influences of sexual and parthenogenetic reproducing European Collembola species, neglecting one important part of the global biodiversity, the belowground system. This thesis focuses on genetic patterns of four Collembola species with different reproductive modes and overlapping ecology across Europe. Collembola existed millions of years in stable habitats, as Eocene fossils show only little variation to extant taxa. In contrast, Cenozoic and Quaternary climatic changes reduced diversity and changed genetic structure of above living animals and plants. In Chapter 2 I investigated the phylogeographic patterns of three common species of Collembola (Ceratophysella denticulata, Folsomia quadrioculata and Isotomiella minor) at a pan-European scale to identify glacial refuges and post-glacial colonization patterns with three genetic markers to cover different time scales. Results suggested density dependent processes for the establishment of new populations, as genetic diversity was high between but low within populations. This founder-takes-it-all principle is common in animal and plant species and suggests that only few early colonizing individuals founded the populations which grew and expanded rapidly. Arrival and invasion of other alleles into these populations was prevented by competition. Surprisingly and in contrast to the post-glacial recolonization patterns of aboveground organisms, the last ice age little affected the genetic composition of the studied Collembola species, indicating that soil provided habitat and resources for survival. The results show that divergence of populations took place during the Miocene (20-5 mya), when climatic conditions were favorable (warm and humid) for little sclerotized arthropods, susceptible to desiccation. Thus, the Miocene facilitated large scale expansion of European Collembola species. The results suggest that evolutionary processes of soil-living species are slowed-down, compared to above the ground living species, resulting in stable populations for millions of years. In chapter 3 I investigated differences in phylogeographic patterns due to different reproductive modes. As no partner is needed for reproduction, parthenogenesis provides a colonization advantage. To investigate the significance of reproductive modes for colonization, I compared the genetic structure of one sexual (Folsomia quadrioculata) and one parthenogenetic (Isotomiella minor) Collembola species with similar ecology across Europe, using one mitochondrial and two nuclear markers. Molecular variance was similar in both species and genetic differences were high between populations, indicating old diversifications. Northern and central Europe populations of I. minor were genetically homogenous suggesting that few lineages of this parthenogenetic species colonized these regions after LGM. Compared to I. minor the genetic structure of F. quadrioculata was more complex with more synonymous substitutions in protein coding genes. The results suggest that in addition to founder-effects and old diversifications, different forces affected sexual and parthenogenetic species, resulting in different phylogeographic patterns. In addition, mitonuclear compatibility among mating partners likely contributed to the more complex genetic structure in F. quadrioculata, whereas gene-environment interactions were of greater importance in I. minor. Overall, results indicate that the widespread view of central and northern European species being shaped by postglacial colonization patterns does not hold for both parthenogenetic and sexual soil-living species. In chapter 4 I investigated colonization patterns including cryptic diversity and the anthropogenic influence of the ubiquitous Collembola species Parisotoma notabilis in Europe. P. notabilis is the most widespread and abundant Collembola species in Europe colonizing many anthropogenic and disturbed habitats. Three molecular markers were used to investigate how anthropogenic factors and climate affected the present-day genetic structure of P. notabilis in Europe. The results showed that P. notabilis forms one morphologically coherent species comprising of several discrete genetic lineages. Molecular divergence estimates suggest that these lineages diverged in the Miocene during wet and warm climate, and a biome change in central and Eastern Europe from forest to grassland. The results further suggest that human activities favored the dispersal of P. notabilis as genetic lineages reflect human trading and migration routes such as the Channel and Mediterranean areas. These lineages are rather young and genetically uniform as compared to other soil-living arthropods. Overall, the results suggest that phylogeographic patterns of soil-living European Collembola follow the ‘southern-richness and northern-purity’ scenario, but in contrast to this scenario, the pattern is not due to climate driven extinction of populations in central Europe during the Quaternary and recolonization thereafter. Rather, the pattern originated during the Miocene (20-5 mya) as indicated by divergence times of most clades. This indicates that the soil forms a stable habitat buffering climatic variability. Moreover, the results suggest that the dispersal of Collembola in Europe was affected by human activities. Overall, colonization in the Miocene and human activities in the Holocene resulted in a more complex genetic structure in soil-living species as compared to those living above the ground