Background: Comparative genomic studies suggest that the modern day assemblage of ray-finned fishes have descended from an ancestral grouping of fishes that possessed 12-13 linkage groups. All jawed vertebrates are postulated to have experienced two whole genome duplications (WGD) in their ancestry (2R duplication). Salmonids have experienced one additional WGD (4R duplication event) compared to most extant teleosts which underwent a further 3R WGD compared to other vertebrates. We describe the organization of the 4R chromosomal segments of the proto-rayfinned fish karyotype in Atlantic salmon and rainbow trout based upon their comparative syntenies with two model species of 3R ray-finned fishes.

BackgroundThe critical role of Major Histocompatibility Complex (Mhc) genes in disease resistance and their highly polymorphic nature make them exceptional candidates for studies investigating genetic effects on survival, mate choice and conservation. Species that harbor many Mhc loci and high allelic diversity are particularly intriguing as they are potentially under strong selection and studies of such species provide valuable information as to the mechanisms maintaining Mhc diversity. However comprehensive genotyping of complex multilocus systems has been a major challenge to date with the result that little is known about the consequences of this complexity in terms of fitness effects and disease resistance.ResultsIn this study, we genotyped the Mhc class I exon 3 of the great tit (Parus major) from two nest-box breeding populations near Oxford, UK that have been monitored for decades. Characterization of Mhc class I exon 3 was adopted and bidirectional sequencing was carried using the 454 sequencing platform. Full analysis of sequences through a stepwise variant validation procedure allowed reliable typing of more than 800 great tits based on 214,357 reads; from duplicates we estimated the repeatability of typing as 0.94. A total of 862 alleles were detected, and the presence of at least 16 functional loci was shown - the highest number characterized in a wild bird species. Finally, the functional alleles were grouped into 17 supertypes based on their antigen binding affinities.ConclusionsWe found extreme complexity at the Mhc class I of the great tit both in terms of allelic diversity and gene number. The presence of many functional loci was shown, together with a pseudogene family and putatively non-functional alleles; there was clear evidence that functional alleles were under strong balancing selection. This study is the first step towards an in-depth analysis of this gene complex in this species, which will help understanding how parasite-mediated and sexual selection shape and maintain host genetic variation in nature. We believe that study systems like ours can make important contributions to the field of evolutionary biology and emphasize the necessity of integrating long-term field-based studies with detailed genetic analysis to unravel complex evolutionary processes.

The W chromosome is predicted to be subject to strong female-specific selection stemming from its female-limited inheritance and therefore should play an important role in female fitness traits. However, the overall importance of directional selection in shaping the W chromosome is unknown because of the powerful degradative forces that act to decay the nonrecombining sections of the genome. Here we greatly expand the number of known W-linked genes and assess the expression of the W chromosome after >100 generations of different female-specific selection regimens in different breeds of chicken and in the wild ancestor, the Red Jungle Fowl. Our results indicate that female-specific selection has a significant effect on W chromosome gene-expression patterns, with a strong convergent pattern of up-regulation associated with increased female-specific selection. Many of the transcriptional changes in the female-selected breeds are the product of positive selection, suggesting that selection is an important force in shaping the evolution of gene expression on the W chromosome, a finding consistent with both the importance of the W chromosome in female fertility and the haploid nature of the W. Taken together, these data provide evidence for the importance of the sex-limited chromosome in a female heterogametic species and show that sex-specific selection can act to preserve sex-limited chromosomes from degrading forces.

Following the suppression of recombination, gene expression levels decline on the sex-limited chromosome, and this can lead to selection for dosage compensation in the heterogametic sex to rebalance average expression from the X or Z chromosome with average autosomal expression. At the same time, due to their unequal pattern of inheritance in males and females, the sex chromosomes are subject to unbalanced sex-specific selection, which contributes to a nonrandom distribution of sex-biased genes compared to the remainder of the genome. These two forces act against each other, and the relative importance of each is currently unclear. The Gallus gallus Z chromosome provides a useful opportunity to study the importance and trade-offs between sex-specific selection and dosage compensation in shaping the evolution of the genome as it shows incomplete dosage compensation and is also present twice as often in males than females, and therefore predicted to be enriched for male-biased genes. Here, we refine our understanding of the evolution of the avian Z chromosome, and show that multiple strata formed across the chromosome over 130 million years. We then use this evolutionary history to examine the relative strength of selection for sex chromosome dosage compensation vs. the cumulative effects of masculinizing selection on gene expression. We find that male-biased expression increases over time, indicating that selection for dosage compensation is relatively less important than masculinizing selection in shaping Z chromosome gene expression.

In salmonid fishes, life-history changes may often be coupled to early individual growth trajectories. We identified quantitative trait loci (QTL) for body weight (BW), condition factor (K) and age at sexual maturation (MT) in two full-sib families of Arctic charr (Salvelinus alpinus) to ascertain if QTL for MT were confounded with BW QTL intervals. Three significant QTL for BW, three QTL for MT and one significant QTL for K were identified. A BW QTL with major effect was localized to linkage group 8 (AC-8) and explained more than 34% of the phenotypic variation. Markers on AC-8 have previously been identified as being associated with variation in fork length and BW in this species. Similarly, a major QTL (PEV = 23%) with an influence on the female MT was localized to AC-23. Some of these regions are homologous to those in the genomes of rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar), where similar QTL effects have been detected. Our results also suggest the conservation of MT QTL on the homeologous linkage group pair AC-3/24 in Arctic charr. We further identified chromosomal regions that harbor QTL for multiple traits. In particular, markers on AC-4, -20 and -36 had detectable QTL for all traits studied. Significant MT QTL detected on AC-23, -24, and -27 were autonomous of any BW QTL regions, suggesting that the regulation of MT may be more independent of BW control within this species than in other species of salmonids.

BackgroundSomatic growth is a complex process that involves the action and interaction of genes and environment. A number of quantitative trait loci (QTL) previously identified for body weight and condition factor in rainbow trout (Oncorhynchus mykiss), and two other salmonid species, were used to further investigate the genetic architecture of growth-influencing genes in this species. Relationships among previously mapped candidate genes for growth and their co-localization to identified QTL regions are reported. Furthermore, using a comparative genomic analysis of syntenic rainbow trout linkage group clusters to their homologous regions within model teleost species such as zebrafish, stickleback and medaka, inferences were made regarding additional possible candidate genes underlying identified QTL regions.ResultsBody weight (BW) QTL were detected on the majority of rainbow trout linkage groups across 10 parents from 3 strains. However, only 10 linkage groups (i.e., RT-3, -6, -8, -9, -10, -12, -13, -22, -24, -27) possessed QTL regions with chromosome-wide or genome-wide effects across multiple parents. Fewer QTL for condition factor (K) were identified and only six instances of co-localization across families were detected (i.e. RT-9, -15, -16, -23, -27, -31 and RT-2/9 homeologs). Of note, both BW and K QTL co-localize on RT-9 and RT-27. The incidence of epistatic interaction across genomic regions within different female backgrounds was also examined, and although evidence for interaction effects within certain QTL regions were evident, these interactions were few in number and statistically weak. Of interest, however, was the fact that these predominantly occurred within K QTL regions. Currently mapped growth candidate genes are largely congruent with the identified QTL regions. More QTL were detected in male, compared to female parents, with the greatest number evident in an F1 male parent derived from an intercross between domesticated and wild strain of rainbow trout which differed strongly in growth rate.ConclusionsStrain background influences the degree to which QTL effects are evident for growth-related genes. The process of domestication (which primarily selects faster growing fish) may largely reduce the genetic influences on growth-specific phenotypic variation. Although heritabilities have been reported to be relatively high for both BW and K growth traits, the genetic architecture of K phenotypic variation appears less defined (i.e., fewer major contributing QTL regions were identified compared with BW QTL regions).

To identify quantitative trait loci (QTL) influencing early maturation (EM) in rainbow trout (Oncorhynchus mykiss), a genome scan was performed using 100 microsatellite loci across 29 linkage groups. Six inter-strain paternal half-sib families using three inter-strain F 1 brothers (approximately 50 progeny in each family) derived from two strains that differ in the propensity for EM were used in the study. Alleles derived from both parental sources were observed to contribute to the expression of EM in the progeny of the brothers. Four genome-wide significant QTL regions (i.e., were observed. EM QTL detected on RT-8 and -24 demonstrated significant and suggestive QTL effects in both male and female progeny. Furthermore, within both male and female full-sib groupings, QTL on RT-8 and -24 were detected in two or more of the five parents used. Significant genome-wide and several strong chromosome-wide QTL for EM localized to different regions in males and females, suggesting some sex-specific control. Namely, QTL detected on were associated with EM only in females, and those on were associated with EM only in males. Within the QTL regions identified, a comparison of syntenic EST markers from the rainbow trout linkage map with the zebrafish (Danio rerio) genome identified several putative candidate genes that may influence EM.

BackgroundSalmonids are regarded as 4R derivative species, having experienced 4 whole genome duplication events in their ancestry. Many duplicated chromosome regions still share extensive homology with one another which is maintained primarily through male-based homeologous chromosome pairings during meiosis. The formation of quadrivalents during meiosis leads to pseudolinkage. This phenomenon is more prevalent within 5 of the 12 ancestral teleost linkage groups in salmonids.ResultsWe constructed a genetic linkage map for brook charr and used this in combination with the genetic map from Arctic charr, to make comparisons with the genetic map of rainbow trout. Although not all chromosome arms are currently mapped, some homologous chromosome rearrangements were evident between Arctic charr and brook charr. Notably, 10 chromosome arms in brook charr representing 5 metacentric chromosomes in Arctic charr have undergone rearrangements. Three metacentrics have one arm translocated and fused with another chromosome arm in brook charr to a make a new metacentrics while two metacentrics are represented by 4 acrocentric pairs in brook charr. In two cases (i.e., BC-4 and BC-16), an apparent polymorphism was observed with the identification of both a putative metacentric structure (similar to metacentric AC-4 = BC-4 and a joining of acrocentric AC-16 + one arm of AC-28 = BC-16), as well as two separate acrocentric linkage groups evident in the mapping parents. Forty-six of the expected 50 karyotypic arms could be inter-generically assigned. SEX in brook charr (BC-4) was localized to the same homologous linkage group region as in Arctic charr (AC-4). The homeologous affinities detected in the two charr species facilitated the identification of 20 (expected number = 25) shared syntenic regions with rainbow trout, although it is likely that some of these regions were partial or overlapping arm regions.ConclusionsInter-generic comparisons among 2 species of charr (genus Salvelinus) and a trout (genus Oncorhynchus) have identified that linkage group arm arrangements are largely retained among these species. Previous studies have revealed that up to 7 regions of high duplicate marker retention occur between Salmo species (i.e., Atlantic salmon and brown trout) and rainbow trout, with 5 of these regions exhibiting higher levels of pseudolinkage. Pseudolinkage was detected in the charr species (i.e., BC-1/21, AC-12/27, AC-6/23, = RT-2p/29q, RT-12p/16p, and RT-27p/31p, respectively) consistent with three of the five 'salmonid-specific' pseudolinkage regions. Chromosome arms with the highest number of duplicated markers in rainbow trout are the linkage group arms with the highest retention of duplicated markers in both charr species.