Evolutionary Genomics

Background and Significance

The genetic background of adaptation has intrigued biologists for a long time, but because of a lack of sufficient tools, it has been very difficult to identify the genes that govern adaptive variation in natural populations. This problem is closely related to finding the genetic basis of complex diseases, where many genes and the environment play a role. Finding the genes would allow the study of whether these are regulatory or structural mutations, what the sizes of the allelic effects are and what the mutation rates are at these loci. These are fundamental questions on the evolution of quantitative variation, with far-reaching implications, but so far these are poorly known. The answers to these questions also have an impact on how adaptive traits are best dealt with in plant (and animal) breeding. The new genetic tools finally make translational genomics, the use of genomics information in breeding, a realistic goal. An important part of our projects deal with the genetics of speciation, still a poorly known field, despite significant advances in the last ten years.

Recent Progress

Our plant adaptation work involves two organisms. One is Scots pine, the most important tree species in Finland. We finalized analyses of the strength of natural selection based on comparison of multiple conifer species. We have also prepared for two large-scale association studies on the timing of growth with our collaborators, the Finnish Forest Research Organization and the Department of Mathematics and Statistics at the University of Helsinki. This has involved large-scale phenotyping of trees derived from a southern Finnish population as regards adaptive traits (timing of growth cessation, frost hardiness) and the development of SNPs, and development of statistical methods (by our collaborators at the University of Helsinki). In the context of the discovery of SNPs, we have also obtained an exceptionally extensive data set for examining the effects of selection on candidate genes.

The work on Arabidopsis lyrata is aimed at discovering the effects of individual loci on flowering time variation in natural populations. For examining differences between populations, large QTL mapping populations have revealed the architecture of variation in crosses between different populations. On the other hand, variation within an individual population, studied in the greenhouse in controlled conditions and in the wild, in the native site of a Norwegian population, has been found to be partly due to one large effect gene (FRI, Kuittinen et al. 2008). At the sequence level, we have searched for evidence of natural selection during adaptation to the north and have found traces of strong selection at one light-measuring locus.

In social insects, we have also used sequence data to infer positive selection in the immune defence system. Many behavioural traits connected to defence against pathogens indicate the importance of pathogens in the evolution of social insects. However, very little is known about how pathogen pressure has affected the molecular evolution of genes involved in their innate immune systems. Our results on the sequence evolution of several immune genes in ants and honeybees show high rates of protein evolution in both kinds of insect. The rates have been measured as the ratio of amino acid changes to silent nucleotide changes (d N/d S), the ratio being clearly higher in ants and honeybees than in Drosophila immune genes or in non-immunity genes of bees. This conforms to our expectations based on high pathogen pressure in social insects. The codon-based likelihood method revealed clear evidence of positive selection in two immune genes in ants, one coding for an antimicrobial peptide, defensin. There is now an indication that selection pressure on the amino acid composition of immune system-related gene products has been an important part in the fight against pathogens by social insects. However, we cannot distinguish in all cases whether a high d N/d S ratio results from positive selection within a restricted part of the studied genes or from relaxation of purifying selection associated with effective measures of behaviourally based colony-level defences.

Our recent work has shown that highly diverged populations of Arabidopsis lyrata have developed incipient reproductive isolation. The genetic basis of the variation is being examined. So far we have found two kinds of hybrid sterility in the F2 generation – a complete lack of pollen production, and reduced pollen viability. The genetic bases of the two traits have different mechanisms. One involves cytonuclear interactions, the other mostly nuclear genes. In another project we have estimated genetic differences between two hybridizing ant lineages. The males (which in ants are haploid) of the two types differ as regards a large proportion of marker genes, but all the females seem to be of hybrid origin, though not F1 hybrids between the types represented by the males. The genetic differences between the sexes within a type are larger than between the two types of females. It is not clear what kind of genetic incompatibilities underlie the system, but it is possible that hybridization between two parental species has led to systematic departures from normal Mendelian segregation in a manner which also depends on the sex of the offspring.

Future Goals

One important goal in our work is to identify the loci governing variation in timing of growth, timing of flowering and intersubspecific sterility. The new sequencing technologies promise major advances in our work. The next year should see important improvements in genetic resources. For Scots pine, transcriptome sequencing with high throughput methods promises advances in SNP development, in the context of the EVOLTREE Network of Excellence. For A. lyrata, the genome sequence has just been completed by the Joint Genome Institute (USA). This will make our search for both adaptation and speciation genes easier. In ants, we are participating in international efforts to sequence a complete genome. The goal is to carry out comparative genomic studies, particularly for characterising the evolution of the gene families involved in immune defence and odour reception. The genomic sequence will also provide better resources for studying the genetic differences associated with speciation and hybrid incompatibilities in ants.

Another major goal is to develop within our group and the department the bioinformatics capacity for these new kinds of data analyses.

Publications 2008

Other Publications from the Biocenter Project:

Kuittinen H, Niittyvuopio A, Rinne P, Savolainen O. Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism. Mol Biol Evol 25:319-329, 2008.

Lascoux M, Pyhäjärvi T, Källman T, Savolainen O. Past demography in forest trees: what can we learn from nuclear DNA sequences that we do not already know? Plant Ecology and Diversity 1:209-215, 2008.

Leppälä J, Bechsgaard JS, Schierup MH, Savolainen O. Transmission ratio distortion in Arabidopsis lyrata: effects of population divergence and the S-locus. Heredity 100:71-78, 2008.

Muller M-H, Leppälä J, Savolainen O. Genome-wide effects of postglacial colonization in Arabidopsis lyrata . Heredity 100:47-58, 2008.

Palmé A, Wright M, Savolainen O. Patterns of divergence among conifer ESTs and polymorphism in Pinus sylvestris identify putative selective sweeps. Mol Biol Evol 25:2567-2577, 2008.

Pyhäjärvi T, Salmela MJ, Savolainen O. Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genomes 4:247-254, 2008.

Seppä P, Fernandez-Escudero I, Gyllenstrand N, Pamilo P. Colony fission affects kinship in a social insect. Behav Ecol Sociobiol 62:589-597, 2008.

Viljakainen L, Reuter M, Pamilo P. Wolbachia transmission dynamics in Formica wood ants. BMC Evol Biol 8:55-62, 2008.

Doctoral Theses 2008

Tanja Pyhäjärvi: Roles of demography and natural selection in molecular evolution of trees, focus on Pinus sylvestris. Acta Universitatis Ouluensis A 506, 2008.

Lumi Viljakainen: Evolutionary genetics of immunity and infection in social insects. Acta Universitatis Ouluensis A 514, 2008.

Research Group Members

Project Leaders:
Pekka Pamilo, Ph.D., Professor ( University of Helsinki)
Outi Savolainen, Ph.D., Professor ( University of Oulu)

Senior and Post-doctoral Investigators:
Helmi Kuittinen , Ph.D. ( University of Oulu)
Tanja Pyhäjärvi, Ph.D. ( University of Oulu)

Ph.D. Students:
Esa Aalto, M.Sc. (ERA-net Plant Genomics)
Christian Bernasconi, M.Sc. ( University of Lausanne)
Kukka Haapaniemi, M.Sc. ( Academy of Finland)
Timo Knürr, M.Sc. (statistics) ( Graduate School for Population Genetics)
Sonja Kujala, M.Sc. (Biocenter Oulu)
Päivi Leinonen, M.Sc. ( Graduate School for Population Genetics)
Johanna Leppälä, M.Sc. (Biocenter Oulu)
Anne Niittyvuopio (Faculty of Natural Sciences doctoral grant)
Jonna Saapunki, M.Sc. ( Graduate School for Population Genetics)
Anu Vihavainen, M.Sc. ( Academy of Finland)
Lumi Viljakainen, M.Sc. (Biocenter Oulu)

Laboratory Technicians:
Soile Finne ( University of Oulu)
Riitta Jokela ( Academy of Finland)

Foreign Scientists, 1

Pekka Pamilo, Ph.D. and Outi Savolainen, Ph.D.