Molecular evolution in Drosophila melanogaster

The genetic basis underlying adaptive evolution is still largely
unknown. Adaptive evolution is facilitated by natural selection
that acts on the genetic variation present in a population.
Favoring some genetic variants over others, natural selection
eventually produces adaptations that allow populations to survive
in changing or new environments. Populations colonizing new
habitats that differ from their original habitat are often
confronted with a multitude of novel ecological constraints to
which they need to adapt. A well-annotated genome and a diverse
genetic toolkit make the fruit fly Drosophila melanogaster an ideal
model system for studying the genetics underlying adaptation. As a
cosmopolitan species, D. melanogaster has adapted to a wide range
of thermal environments. Despite having a tropical origin in
southern-central Africa, it has successfully settled in temperate
environments around the world. Thermal adaptations that have helped
to deal with the greater range and variability in temperature as
well as low-temperature extremes have been required to prosper in
temperate environments. Chromatin-based gene regulation is known to
be disrupted by varying temperatures. Variation in the temperature,
at which flies live, result in varying expression levels of
Polycomb group (PcG) regulated genes with higher expression at
lower temperatures. Chapter 1 and 2 of this thesis aim to answer
the question whether this thermosensitivity of PcG regulation has
been detrimental for colonizing temperate environments and thus
needed to be buffered by natural selection. Thermosensitivity of
PcG regulation was observed in different natural populations of D.
melanogaster. A lower degree of thermosensitive expression was
consistently found for populations from temperate climates when
compared to those from the tropics. In Chapter 1, evidence is
presented for positive selection acting on the polyhomeotic (ph)
gene region to reduce thermosensitivity of PcG regulation in
temperate populations from Europe. The targets of selection appear
to be single nucleotide polymorphisms (SNPs) in a relatively small
cis-regulatory region between the two PcG target genes polyhomeotic
proximal (ph-p) and CG3835 that are highly differentiated between
European and African populations. Using reporter gene assays, it
was demonstrated that these SNPs influence gene expression and that
the European alleles confer reduced thermosensitivity of expression
in contrast to the African alleles. In Chapter 2, thermosensitivity
of another PcG target gene, vestigial (vg), was investigated in six
natural populations including four temperate populations from
high-altitude Africa and central to high-latitude Europe, and two
tropical populations from the ancestral species range. All four
temperate populations exhibited a lower degree of thermosensitive
expression than the two tropical populations. The underlying
mechanisms of increased buffering, however, seem to differ between
these temperate populations. Thermal adaptation to temperate
environments also includes dealing with low-temperature extremes.
Severe cold stress is a main limiting factor imposed on D.
melanogaster by temperate climates. Increased cold tolerance in
temperate populations is thought to have evolved by natural
selection. Cold tolerance is a quantitative trait that appears to
be highly polygenic and has been mapped to different quantitative
trait loci (QTL) in the genome. In Chapter 3, such a QTL region was
fine-mapped to localize causal genes for increased cold tolerance
in temperate flies. As a result, brinker (brk) was identified as a
new candidate gene putatively involved in cold stress adaptation.