Moira M. Ferguson

A Linkage Map for Brown Trout (Salmo trutta): Chromosome Homeologies and Comparative Genome Organization With Other Salmonid Fish

We report on the construction of a linkage map for brown trout (Salmo trutta) and its comparison with those of other tetraploid-derivative fish in the family Salmonidae, including Atlantic salmon (Salmo salar), rainbow trout (Oncorhynchus mykiss), and Arctic char (Salvelinus alpinus). Overall, we identified 37 linkage groups (2n = 80) from the analysis of 288 microsatellite polymorphisms, 13 allozyme markers, and phenotypic sex in four backcross families. Additionally, we used gene–centromere analysis to approximate the position of the centromere for 20 linkage groups and thus relate linkage arrangements to the physical morphology of chromosomes. Sex-specific maps derived from multiple parents were estimated to cover 346.4 and 912.5 cM of the male and female genomes, respectively. As previously observed in other salmonids, recombination rates showed large sex differences (average female-to-male ratio was 6.4), with male crossovers generally localized toward the distal end of linkage groups. Putative homeologous regions inherited from the salmonid tetraploid ancestor were identified for 10 pairs of linkage groups, including five chromosomes showing evidence of residual tetrasomy (pseudolinkage). Map alignments with orthologous regions in Atlantic salmon, rainbow trout, and Arctic char also revealed extensive conservation of syntenic blocks across species, which was generally consistent with chromosome divergence through Robertsonian translocations.

Identification of two QTL influencing upper temperature tolerance in three rainbow trout (Oncorhynchus mykiss) half-sib families

We searched for linkage among 24 polymorphic loci (allozymes, RAPD, microsatellites) in three half-sib backcross families of rainbow trout (Oncorhynchus mykiss) produced by crossing strains divergent for the quantitative trait of upper temperature tolerance. Seven significant and two suggestive pairwise linkage associations between molecular marker loci were observed involving 14 loci clustered into four linkage groups. The association between a pair of allozyme loci (sIDHP-3* and mMEP-2 *) has been reported previously. Recombination rates varied greatly between the sexes and families. Two quantitative trait loci (QTL) were mapped by detecting a significant association between variance in upper temperature tolerance and alleles at the microsatellite loci Omy325UoG and Ssa14DU. The two QTL appear to reside in different linkage groups and account for ≈13 per cent and 9 per cent of the overall additive genetic variance in upper temperature tolerance. No significant interaction was detected between Omy325UoG and Ssa14DU suggesting that the effects of the QTL are additive.

QTL for body weight and condition factor in Atlantic salmon (Salmo salar): comparative analysis with rainbow trout (Oncorhynchus mykiss) and Arctic charr (Salvelinus alpinus).

Genotypes at 91 microsatellite loci in three full-sib families were used to search for QTL affecting body weight (BW) and condition factor in North American Atlantic salmon (Salmo salar). More than one informative marker was identified on 16–18 linkage groups in each family, allowing at least one chromosomal interval to be analyzed per linkage group. Two significant QTL for BW on linkage groups AS-8 and AS-11, and four significant QTL for condition factor on linkage groups AS-2, AS-5, AS-11, and AS-14 were identified. QTL for both BW and condition factor were located on linkage groups AS-1, 6, 8, 11, and 14 when considering both significant and suggestive QTL effects. The largest QTL effects for BW (AS-8) and for condition factor (AS-14) accounted for 20.1 and 24.9% of the trait variation, respectively. Three of the QTL for BW occur on linkage groups where similar effects have been detected on the homologous regions in either rainbow trout (Oncorhynchus mykiss) or Arctic charr (Salvelinus alpinus).

Linkage analysis of quantitative trait loci associated with spawning time in rainbow trout (Oncorhynchus mykiss)

We have used 54 microsatellite markers to search for quantitative trait loci (QTL) associated with spawning time in rainbow trout (Oncorhynchus mykiss). Linkage tests have been conducted in a backcross family produced by crossing spring and fall spawning stains in Ontario, Canada. We have mapped thirteen QTL markers for spawning time representing seven linkage groups. Eight of these QTL markers from five linkage groups show repeatable effects in two sampling years. These results suggest this trait is highly polygenic in rainbow trout.

Distribution of ancestral proto-Actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (Rainbow trout and Atlantic salmon)

BackgroundComparative 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-ray-finned fish karyotype in Atlantic salmon and rainbow trout based upon their comparative syntenies with two model species of 3R ray-finned fishes.ResultsEvidence is presented for the retention of large whole-arm affinities between the ancestral linkage groups of the ray-finned fishes, and the 50 homeologous chromosomal segments in Atlantic salmon and rainbow trout. In the comparisons between the two salmonid species, there is also evidence for the retention of large whole-arm homeologous affinities that are associated with the retention of duplicated markers. Five of the 7 pairs of chromosomal arm regions expressing the highest level of duplicate gene expression in rainbow trout share homologous synteny to the 5 pairs of homeologs with the greatest duplicate gene expression in Atlantic salmon. These regions are derived from proto-Actinopterygian linkage groups B, C, E, J and K.ConclusionTwo chromosome arms in Danio rerio and Oryzias latipes (descendants of the 3R duplication) can, in most instances be related to at least 4 whole or partial chromosomal arms in the salmonid species. Multiple arm assignments in the two salmonid species do not clearly support a 13 proto-linkage group model, and suggest that a 12 proto-linkage group arrangement (i.e., a separate single chromosome duplication and ancestral fusion/fissions/recombination within the putative G/H/I groupings) may have occurred in the more basal soft-rayed fishes. We also found evidence supporting the model that ancestral linkage group M underwent a single chromosome duplication following the 3R duplication. In the salmonids, the M ancestral linkage groups are localized to 5 whole arm, and 3 partial arm regions (i.e., 6 whole arm regions expected). Thus, 3 distinct ancestral linkage groups are postulated to have existed in the G/H and M lineage chromosomes in the ancestor of the salmonids.

Estimates of genetic parameters and genotype by environment interactions for growth traits of rainbow trout (Oncorhynchus mykiss) as inferred using molecular pedigrees

Abstract Genetic correlations between three character sets (early progeny growth; later progeny growth at 8.5 °C; later progeny growth at 15 °C) were determined from within the scope of a working commercial rainbow trout ( Oncorhynchus mykiss ) aquaculture facility. Microsatellite multiplex genotyping systems were used to resolve the molecular pedigrees for groups of progeny with high accuracy (91–95%). The heritability estimates obtained from restricted maximum likelihood (REML) were higher than expected, ranging from 0.360 to 0.719 for the growth traits total length, weight and condition factor. Estimates of genetic correlations were obtained through correlation of single trait estimated breeding values (EBV), correlation of multiple trait EBV, and by estimates of genetic correlations coming directly from multiple trait REML. REML determined genetic correlations were high (0.86±0.026), indicating that early progeny growth is a good predictor of later progeny growth and that the magnitude of genotype by environment interactions (G×E) is low. Genetic correlations estimated from multiple trait EBV (0.84±0.048) were not significantly different from the REML estimates. Both were significantly different from the genetic correlations estimated from single trait EBV (0.60±0.049), suggesting that single trait estimates have limited value. Interestingly, the genetic correlations between condition factor and length or weight of all character sets were significantly different from unity, indicating that condition factor is a trait that is genetically independent of both length and weight.

Quantitative trait loci for upper thermal tolerance in outbred strains of rainbow trout (Oncorhynchus mykiss)

The expression of three putative QTL for upper thermal tolerance (UTT) was examined in two strains of outbred rainbow trout unselected for this trait using simple-sequence repeat (SSR; microsatellite) markers associated with UTT in backcrosses of lines selected on this trait. Two-way diallel lots in the third generation of an outbred pedigree were exposed to an acute thermal challenge. QTL detection was performed separately by each second-generation parent within each diallel lot, incorporating the effects of full sib families and correlated traits. Inheritance of different alleles at the SSR Ssa20.19NUIG from the sire 93-32-1 was strongly associated with the thermal tolerance of his half sib progeny, explaining 7.5% of their phenotypic variance in this trait. A hierarchical linear model incorporating allelic inheritance from all four grandsires of the experimental diallels (in addition to family specific and covariate trait effects) was also used to detect associations between the SSR and thermal tolerance in their third-generation grandprogeny. Ssa20.19NUIG was strongly associated with thermal tolerance in the grandprogeny of the grandsire G0SVM2. The generally stronger marker-trait associations found in male parents may be partially due to reduced chromosomal recombination rates in male salmonids compared to females. These results indicate the effects of a QTL on a fitness-related trait in unselected populations of rainbow trout.

Epistasis in allelic expression at upper temperature tolerance QTL in rainbow trout

Abstract We have mapped the location of QTL affecting upper temperature tolerance in three backcross families of rainbow trout ( Oncorhynchus mykiss ) derived from matings between an F 1 male (high (H)×low (L) temperature tolerance selected lines) and two H and one L line females using variation at 61 microsatellite loci. Physiological epistasis was observed among paternally inherited QTL alleles and this depended upon the genomic background in which the alleles were expressed. A marker allele associated with a QTL leading to enhanced thermal resistance in one background (either H or L) showed the opposite association in the other genomic background. These results suggest that the effectiveness of marker assisted selection (MAS) may be limited without prior knowledge of the performance characteristics of QTL alleles in different genomic backgrounds.

Adaptive peaks and alternative foraging tactics in brook charr: evidence of short-term divergent selection for sitting-and-waiting and actively searching

Abstract Some recently emerged brook charr (Salvelinus fontinalis) inhabiting still-water pools along the sides of streams are sedentary and eat crustaceans from the lower portion of the water column. Others are more active and eat insects from the upper portion of the water column. We provide evidence that this divergent foraging behavior reflects short-term divergent selection brought about by intraspecific competition in the presence of alternative food sources. Rates of encounters and interactions between individuals were density dependent, and encounter and interaction events were closely timed with prey capture attempts. In addition, aggressive fish made more foraging attempts per minute than nonaggressive fish. Aggressive fish were also either inactive or very active, while nonaggressive fish exhibited intermediate levels of activity. Growth rate potential, an important component of fitness during the early life stages of brook charr, was assessed using tissue concentrations of RNA and found to be highest for sedentary fish and for active fish making frequent foraging attempts, and lower for fish exhibiting intermediate levels of activity. Our findings support contentions that individual behavior plays an important role during initial steps in the evolution of resource polymorphisms.

Population genetic structure of Arctic Charr, Salvelinus alpinus from northwest Europe on large and small spatial scales

To examine the population genetic structure of lake‐resident Arctic charr, Salvelinus alpinus from northwest Europe on multiple spatial scales, 2367 individuals from 43 lakes located in three geographical regions (Iceland, the British Isles and Scandinavia) were genotyped at six microsatellite loci. On a large scale, data provided little evidence to support clustering of populations according to geographical region. Hierarchical analysis of molecular variance indicated that, although statistically significant, only 2.17% of the variance in allelic frequencies was partitioned at the among‐region level. Within regions, high levels of genetic differentiation were typically found between lakes regardless of the geographical distance separating them. These results are consistent with the hypothesis of rapid postglacial recolonization of all of northwest Europe from a single charr lineage, with subsequent restriction of gene flow. On a smaller scale, there was evidence for close genetic relationships among lakes from within common drainage basins in Scotland. Thus, interlake genetic structure reflects localized patterns of recent (or contemporary) gene flow superimposed onto a larger scale structure that is largely a result of historical processes. There was also evidence for widespread genetic structuring at the within‐lake level, with sympatric populations detected in 10 lakes, and multilocus heterozygote deficits found in 23 lakes. This evidence of the Wahlund effect was found in all lakes known to contain discrete phenotypic morphs, as well as many others, suggesting that morphs may often represent separate breeding populations, and also that the phenomenon of polymorphism in this species may be more widespread than is currently realized.