A genome‐wide linkage map for the house sparrow (Passer domesticus) provides insights into the evolutionary history of the avian genome

The house sparrow is an important model species for studying physiological, ecological and evolutionary processes in wild populations. Here, we present a medium density, genome wide linkage map for house sparrow (Passer domesticus) that has aided the assembly of the house sparrow reference genome, and that will provide an important resource for ongoing mapping of genes controlling important traits in the ecology and evolution of this species. Using a custom house sparrow 10 K iSelect Illumina SNP chip we have assigned 6,498 SNPs to 29 autosomal linkage groups, based on a mean of 430 informative meioses per SNP. The map was constructed by combining the information from linkage with that of the physical position of SNPs within scaffold sequences in an iterative process. Averaged between the sexes; the linkage map had a total length of 2,004 cM, with a longer map for females (2,240 cM) than males (1,801 cM). Additionally, recombination rates also varied along the chromosomes. Comparison of the linkage map to the reference genomes of zebra finch, collared flycatcher and chicken, showed a chromosome fusion of the two avian chromosomes 8 and 4A in house sparrow. Lastly, information from the linkage map was utilized to conduct analysis of linkage disequilibrium (LD) in eight populations with different effective population sizes (N_e) in order to quantify the background level LD. Together, these results aid the design of future association studies, facilitate the development of new genomic tools and support the body of research that describes the evolution of the avian genome.     

Genetic mapping of the female mimic morph locus in the ruff

Background

Ruffs (Aves: Philomachus pugnax) possess a genetic polymorphism for male mating behaviour resulting in three permanent alternative male reproductive morphs: (i) territorial ‘Independents’, (ii) non-territorial ‘Satellites’, and (iii) female-mimicking ‘Faeders’. Development into independent or satellite morphs has previously been shown to be due to a single-locus, two-allele autosomal Mendelian mode of inheritance at the Satellite locus. Here, we use linkage analysis to map the chromosomal location of the Faeder locus, which controls development into the Faeder morph, and draw further conclusions about candidate genes, assuming shared synteny with other birds.

Results

Segregation data on the Faeder locus were obtained from captive-bred pedigrees comprising 64 multi-generation families (N?=?381). There was no evidence that the Faeder locus was linked to the Satellite locus, but it was linked with microsatellite marker Ppu020. Comparative mapping of ruff microsatellite markers against the chicken (Gallus gallus) and zebra finch (Taeniopygia guttata) genomes places the Ppu020 and Faeder loci on a region of chromosome 11 that includes the Melanocortin-1 receptor (MC1R) gene, which regulates colour polymorphisms in numerous birds and other vertebrates. Melanin-based colouration varies with life-history strategies in ruffs and other species, thus the MC1R gene is a strong candidate to play a role in alternative male morph determination.

Conclusion

Two unlinked loci appear to control behavioural development in ruffs. The Faeder locus is linked to Ppu020, which, assuming synteny, is located on avian chromosome 11. MC1R is a candidate gene involved in alternative male morph determination in ruffs.

     

Partitioning of genetic variation across the genome using multimarker methods in a wild bird population

The underlying basis of genetic variation in quantitative traits, in terms of the number of causal variants and the size of their effects, is largely unknown in natural populations. The expectation is that complex quantitative trait variation is attributable to many, possibly interacting, causal variants, whose effects may depend upon the sex, age and the environment in which they are expressed. A recently developed methodology in animal breeding derives a value of relatedness among individuals from high‐density genomic marker data, to estimate additive genetic variance within livestock populations. Here, we adapt and test the effectiveness of these methods to partition genetic variation for complex traits across genomic regions within ecological study populations where individuals have varying degrees of relatedness. We then apply this approach for the first time to a natural population and demonstrate that genetic variation in wing length in the great tit (Parus major) reflects contributions from multiple genomic regions. We show that a polygenic additive mode of gene action best describes the patterns observed, and we find no evidence of dosage compensation for the sex chromosome. Our results suggest that most of the genomic regions that influence wing length have the same effects in both sexes. We found a limited amount of genetic variance in males that is attributed to regions that have no effects in females, which could facilitate the sexual dimorphism observed for this trait. Although this exploratory work focuses on one complex trait, the methodology is generally applicable to any trait for any laboratory or wild population, paving the way for investigating sex‐, age‐ and environment‐specific genetic effects and thus the underlying genetic architecture of phenotype in biological study systems.     

Introgression and the fate of domesticated genes in a wild mammal population

When domesticated species are not reproductively isolated from their wild relatives, the opportunity arises for artificially selected variants to be re‐introduced into the wild. However, the evolutionary consequences of introgression of domesticated genes back into the wild are poorly understood. By combining high‐throughput genotyping with 25 years of long‐term ecological field data, we describe the occurrence and consequences of admixture between a primitive sheep breed, the free‐living Soay sheep of St Kilda, and more modern breeds. Utilizing data from a 50 K ovine SNP chip, together with forward simulations of demographic scenarios, we show that admixture occurred between Soay sheep and a more modern breed, consistent with historical accounts, approximately 150 years ago. Haplotype‐sharing analyses with other breeds revealed that polymorphisms in coat colour and pattern in Soay sheep arose as a result of introgression of genetic variants favoured by artificial selection. Because the haplotypes carrying the causative mutations are known to be under natural selection in free‐living Soay sheep, the admixture event created an opportunity to observe the outcome of a ‘natural laboratory’ experiment where ancestral and domesticated genes competed with each other. The haplotype carrying the domesticated light coat colour allele was favoured by natural selection, while the haplotype associated with the domesticated self coat pattern allele was associated with decreased survival. Therefore, we demonstrate that introgression of domesticated alleles into wild populations can provide a novel source of variation capable of generating rapid evolutionary changes.     

Mapping quantitative trait Loci underlying fitness-related traits in a free-living sheep population

We searched for quantitative trait loci (QTL) underlying fitness-related traits in a free-living pedigree of 588 Soay sheep in which a genetic map using 251 markers with an average spacing of 15 cM had been established previously. Traits examined included birth date and weight, considered both as maternal and offspring traits, foreleg length, hindleg length, and body weight measured on animals in August and jaw length and metacarpal length measured on cleaned skeletal material. In some cases the data were split to consider different age classes separately, yielding a total of 15 traits studied. Genetic and environmental components of phenotypic variance were estimated for each trait and, for those traits showing nonzero heritability (N= 12), a QTL search was conducted by comparing a polygenic model with a model including a putative QTL. Support for a QTL at genome-wide significance was found on chromosome 11 for jaw length; suggestive QTL were found on chromosomes 2 and 5 (for birth date as a trait of the lamb), 8 (birth weight as a trait of the lamb), and 15 (adult hindleg length). We discuss the prospects for refining estimates of QTL position and effect size in the study population, and for QTL searches in free-living pedigrees in general.