by Andrew Farrer
I was surprised to learn that the domestication of the Rock Pigeon (Columbia livia) has resulted in over 350 breeds. In a stunning example of macro-evolution within a species this domestication has led to some striking phenotype differences. Researchers have now started to explore the genomic diversity, genetic structure and phylogenetic relationships present in these birds. Studying the (relatively) simplistic genetic differences between breeds gives researchers a base to explore the more complex and less distinct differences between other avian species.
In a study by Shapiro et al. 38 domestic birds from 36 breeds and 2 feral individuals were sequenced, the results supporting the assumption that these birds would make good models. The Rock Pigeon isn’t on any endangered lists; its effective population size is roughly 521,000 which, apart from a recent bottle neck, has been stable for 1.5 million generations. More importantly, though, with a low expected Linkage Disequilibrium between gene pairs, association mapping techniques are possible (Association mapping exploits the fact that new alleles for new traits will still be close to ancestral genetic sequences. As such you can use SNP chips to explore specific regions of the genome in many individuals and link these differences with differences in phenotype).
Breed relationships were drawn up based on this initial examination and simulations showed that all the breeds had originated from a single ancestral population (rooted using sister species; Columbia rupestris). From this base, further analyses were conducted to associate specific genes and alleles with some of the phenotypic differences. (In case you were wondering, the two feral individuals included in this study appear to be descended from homing pigeons. Whether their ancestors escaped or got lost isn’t clear).
Change in plumage colouration is the primary result of bird domestication. This is followed by plumage and structural (skeletal and soft tissue) change and finally changes in behaviour. The head crest is an example of plumage alteration. This feature results from a reversed angle of feather projection on the neck. Growing upwards the feathers form a ring around the head, giving the bird a crown, or crest, of feathers. The degree varies between breeds. Some have no crest at all (the apparent ancestral state) whilst some have quite extreme crests (the Jacobin (pictured) hopefully doesn’t require a wide field of vision!). Importantly the presence of the crest follows a Mendelian recessive pattern, suggesting a single gene is responsible.
Re-sequencing confirmed that a single locus controlled the presence/absence of the crest. It was the pigeon homolog of the Ephrin receptor B2 gene, part of the tissue patterning and morphogenesis pathway in chickens and presumed to be similar in pigeons. Comparison between 8 crested birds showed that the same mutation caused the presence of the crest in differing breeds. The non-synonymous substitution of a Thymine (T) for a Cytosine (C) generates the recessive allele, the substitution of one base in the entire genome, causes the presence of the crest. As noted the trait is recessive so an individual requires both copies of the gene to be the T allele to have a crest. The presence of the C allele in one or both genes results in no crest.
The same mutation in all crest bearing breeds suggests a single occurrence in a common ancestor or repeated selection from a standing occurrence in the original, wild Rock Pigeon population. With crested breeds not necessarily being more closely related to each other than to non-crested breeds the standing occurrence hypothesis seems viable. Although, it seems to me that in such an artificially selected group it would be easy, whilst the allele was not fixed in the population to breed it in or out of sister lineages or to breed in other alleles in different genes that cause two closer related breeds to appear differentiated. For instance if you took a stock of birds and split them into three populations, you could breed the crest into two whilst not the third. However, if you also select strongly for other traits in the second of the crested populations you would cause the two crested populations to differ at more loci than the first crested population and the non-crested population.
Contrast the Red Jacobin and the English Trumpeter (pictured); Ephrin receptor B2 gene causes the presence of both birds’ crest but the differences are caused by the effects of other genes along the pathway. For one single base change, though, to be the trigger for such an apparent trait really does show how tiny genetic changes can lead to phenotypic differences; differences which could easily impact upon fitness. Such an example shows how micro-evolution could easily generate macro-evolutionary changes; changes that could lead to speciation events. It may even be possible for a single base to make all the difference – it does here.
Shapiro, M.D. et al (2013) Genomic diversity and evolution of the head crest in the rock pigeon. Science 339: 1063-1067