The avian genome uncovered

Our knowledge of avian genomics has increased rapidly over the past few years, culminating in the recent publication of a draft sequence of the chicken genome, a milestone event in avian genetics and evolutionary biology. Comparative analysis reveals a compact avian genome structure containing a similar number of genes as found in mammals but with shorter intergenic DNA sequences and fewer repeats. Recombination is at a higher rate than in mammals, particularly for microchromosomes. These also differ from macrochromosomes in their GC and gene content, and their substitution rate. The avian genome has remained unusually stable during evolution and contrasts sharply with the frequent chromosomal rearrangements seen in the rodent lineage. Detailed analyses of polymorphism levels in chickens, including a genome-wide screening in three chicken breeds yielding a set of 2.8 million SNP markers, reveal unexpectedly high levels of genetic diversity. As a notable exception, the female-specific W chromosome is very low in diversity, a probable consequence of the effect of selection on non-recombining chromosomes. The chicken genome promises to be a useful resource for ecological and evolutionary studies of other bird species.

Introduction

Not long ago, it seemed unrealistic that the complete genetic code of living organisms could be deciphered. Today, however, biology is strongly influenced by our ability to unravel the genome, and this impacts on most aspects of biology. The ‘genomics era’ was entered in real earnest some ten years ago, with the sequencing of small bacterial genomes, and has moved on to ever-larger genomes. The initial draft sequence of the human genome published in 2001 [1] was a remarkable achievement and has been followed by similar reports on large and complex genomes, including mouse Mus domesticus [2] and rat Rattus norwegicus [3]. To this list is now added the first bird genome, that of the chicken Gallus gallus [4]. Significantly, not only has the chicken genome been sequenced once, but it has also been the subject of large-scale re-sequencing in three different breeds, to disclose the genome-wide patterns of polymorphism [5].

Starting with a white paper proposal in 2002 to sequence the chicken genome (http://genome.wustl.edu/projects/chicken/) and the subsequent approval by The National Human Genome Research Institute (http://www.ncbi.nih.gov/) to sponsor such a venture, sequencing of the ∼1.2 billion-bp chicken genome began during March 2003 at the Genome Sequencing Centre at Washington University Medical School in St Louis. A year later, the first draft of the genome sequence was deposited into free public data bases. The bird chosen for genome sequencing was a female red junglefowl G. g. gallus, the wild ancestor to the domestic chicken G. gallus domesticus [6].

Sequencing of the chicken genome was motivated by several factors. As a descendant of the dinosaurs and the first non-mammalian amniote to be sequenced, the chicken is crucially placed in the phylogenetic tree of life. The sequencing of the chicken provides new perspectives on vertebrate genome evolution, genome architecture and molecular evolution. With the chicken as the outgroup, features of mammalian biology that are derived or ancient can now be distinguished. Moreover, the chicken is the main laboratory model for birds, and has been an important model organism for developmental biology, as well as for studies of virology, oncogenesis and immunology [7]. Furthermore, the chicken is an important agriculture animal and the genome sequence will facilitate mapping of quantitative trait loci relating to, for example, production and animal health, as well as investigation of the domestication process. The chicken is the first domestic animal to have its genome sequenced.

Here, I focus on evolutionary aspects of the avian genome. As a result of access to the genome sequence (unless otherwise specified, all data described here are from [4]), what have we learnt about genome evolution, in general, and the composition of the avian genome in particular? First, the small genome size of birds, its peculiar organization into macro- and microchromosomes, and the substitution rate of avian chromosomes are addressed. I ask what polymorphism screenings tell us about the rate and distribution of genetic diversity in a bird. What is the value of the chicken genome for evolutionary studies in other bird species? Currently, there is considerable interest among ecologists and evolutionary biologists in the use of genomic approaches to reveal the genetic basis of traits that are subject to selection in natural populations [8]. Many bird species constitute important models for addressing general questions about behavioural ecology, sexual selection and speciation. How can such studies benefit from knowledge of the chicken genome?