Phylogeny and phylogeography of European Parids

Laura Kvist

Department of Biology

Abstract

Mitochondrial DNA sequences were used to study the phylogeny, population structure and colonisation history of Parus species.

The phylogenetic relationships of seven European and three American species were examined by sequencing a part of the cytochrome b gene. Phylogenetically the closest species were the great tit (Parus major) and the blue tit (P. caeruleus). Subgenus Poecile was divided into two clades, one consisting of the Siberian tit (P. cinctus), the Carolina chickadee (P. carolinensis) and the Black-capped chickadee (P. atricapillus) and the other consisting of the marsh tit (P. palustris) and the willow tit (P. montanus). The coal tit (P. ater) and the crested tit (P. cristatus) did not group with any of the species studied.

The population structure and the colonisation history of the willow tit, the great tit and the blue tit were examined by using control region sequences. The results suggest that the historical effective population size in the willow tit has been large and not contracted by the last ice age. Current gene flow must also be extensive as no population structuring was detected.

No population structuring was evident either in the great tit and the populations showed distinctive signs of a recent population expansion. The patterns of genetic variation probably reflect a population bottleneck during the ice age, and a recolonisation of the European continent thereafter, presumably from a refugium situated in the Balkans.

Two maternal lineages were found in the blue tit. The southern lineage was restricted to the Iberian peninsula whereas the northern lineage was detected from all the populations. The colonisation history has been similar to the one suggested for the great tit. The southern lineage, however, may have survived the ice age in a different refugium in the Iberian peninsula and was not as successful as the northern lineage in colonising available regions when the ice retreated. Both, the blue tit and the great tit have continued to expand their distribution northwards during this century and gene flow plays an important role in homogenising the populations.

Table of Contents

Acknowledgments

List of original publications

1. Introduction: Evolution and mitochondrial DNA in birds

1.1. Evolutionary forces and processes

1.2. Molecular markers and neutrality

1.2.1. Molecular clock
1.2.2. Genetic structure of populations, phylogeography and gene flow
1.2.3. Effective population size
1.2.4. Population growth or decline
1.2.5. Phylogeny

1.3. Mitochondrial DNA

1.3.1. Avian mitochondrial DNA
1.3.2. Cytochrome b
1.3.3. Control region of mtDNA

2. Outlines of the present study

3. Materials and methods

3.1. The bird species and populations studied

3.2. Molecular methods

3.3. DNA Sequence analysis

3.3.1. Genetic distances and phylogenetic methods
3.3.2. Population diversity indices and population divergence

4.1. Structure of the control region of the tits
4.2. Taxonomy and diversity at the species level
4.3. Diversity indices and coalescence times within populations
4.4. Population structure and gene flow

5. Discussion

5.1. Sequence variation in the cytochrome b and in the control region and their suitability to phylogenetic and population genetic studies
5.2. Phylogeography and spatial population structure
5.3. Effective population size
5.4. Post-glacial history
5.5. Present or past gene flow

6. Concluding remarks and some future aspects

List of Tables
1. Nucleotide diversity (%π ) and haplotype diversity (1 − Σf_i²) of the great, blue and willow tit populations studied.
2. Kimura"s two parameter distances of four Parus species. Above the diagonal are the mitochondrial control region distances. Below the diagonal are the cytochrome b gene distances based on a portion of the gene. The great tit and blue tit sequences are from Taberlet et al. (1992).

List of Figures
1. Mitochondrial genomes of birds (a, b) and mammals and Xenopus (c). tRNA genes are identified by their 1-letter amino acid codes. Outer circle represents the heavy (H) strand and the inner circle the light (L) strand. Polarity of transcription and the transcribed strand is shown with the arrowheads. When no arrowhead is marked the gene is transcribed from the H-strand with clockwise polarity. The regions used in this study are marked with dark grey. The genomes are redrawn from Desjardins and Morais (1990) and Mindell et al. (1998).
2. Structure of the cytochrome b protein. The gene region used in this study corresponds the shaded parts of the protein.
1-3. Control region alignment of one individual from each of four Parus species and the structural elements in the region. Identical nucleotide sites are shown by stars.
4. Distribution areas of the willow, the great and the blue tit and their sampling sites.
5. Comparison of the phylogenetic trees built from the control region and cytochrome b gene sequences. The numbers along branches denote percentages supporting the branching in 1000 bootstrap replicates.
6. Pairwise comparison of the nucleotide substitutions in the control region of four Parus species.
7. Nucleotide compositions of the control region and the cytochrome b gene of the Parids. The mean frequency of nucleotides has been calculated from one individual per each of blue tit, great tit, willow tit and Siberian tit.
8. Possible post-glacial colonisation routes of the blue and the great tit.

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