The Genetic Architecture of Recombination Rates is Polygenic and Differs Between the Sexes in Wild House Sparrows (Passer domesticus).

Meiotic recombination through chromosomal crossing-over is a fundamental feature of sex and an important driver of genomic diversity. It ensures proper disjunction, allows increased selection responses, and prevents mutation accumulation; however, it is also mutagenic and can break up favorable haplotypes. This cost-benefit dynamic is likely to vary depending on mechanistic and evolutionary contexts, and indeed, recombination rates show huge variation in nature. Identifying the genetic architecture of this variation is key to understanding its causes and consequences. Here, we investigate individual recombination rate variation in wild house sparrows (Passer domesticus). We integrate genomic and pedigree data to identify autosomal crossover counts (ACCs) and intrachromosomal allelic shuffling (r¯intra) in 13,056 gametes transmitted from 2,653 individuals to their offspring. Females had 1.37 times higher ACC, and 1.55 times higher r¯intra than males. ACC and r¯intra were heritable in females and males (ACC h2 = 0.23 and 0.11; r¯intra  h2 = 0.12 and 0.14), but cross-sex additive genetic correlations were low (rA = 0.29 and 0.32 for ACC and r¯intra). Conditional bivariate analyses showed that all measures remained heritable after accounting for genetic values in the opposite sex, indicating that sex-specific ACC and r¯intra can evolve somewhat independently. Genome-wide models showed that ACC and r¯intra are polygenic and driven by many small-effect loci, many of which are likely to act in trans as global recombination modifiers. Our findings show that recombination rates of females and males can have different evolutionary potential in wild birds, providing a compelling mechanism for the evolution of sexual dimorphism in recombination.

The genetic basis of dispersal in a vertebrate metapopulation.

Dispersal affects evolutionary processes by changing population size and genetic composition, influencing the viability and persistence of populations. Investigating which mechanisms underlie variation in dispersal phenotypes and whether populations harbour adaptive potential for dispersal is crucial to understanding the eco-evolutionary dynamics of this important trait. Here, we investigate the genetic architecture of dispersal among successfully recruited individuals in an insular metapopulation of house sparrows. We use an extensive long-term individual-based ecological data set and high-density single-nucleotide polymorphism (SNP) genotypes for over 2500 individuals. We conducted a genome-wide association study (GWAS), and found a relationship between dispersal probability and a SNP located near genes known to regulate circadian rhythm, glycogenesis and exercise performance, among other functions. However, this SNP only explained 3.8% of variance, suggesting that dispersal is a polygenic trait. We then used an animal model to estimate heritable genetic variation (σA 2 ), which composes 10% of the total variation in dispersal probability. Finally, we investigated differences in σA 2 across populations occupying ecologically relevant habitat types (farm vs. non-farm) using a genetic groups animal model. We found different adaptive potentials across habitats, with higher mean breeding value, σA 2 , and heritability for the habitat presenting lower dispersal rates, suggesting also different roles of environmental variation. Our results suggest a complex genetic architecture of dispersal and demonstrate that adaptive potential may be environment dependent in key eco-evolutionary traits. The eco-evolutionary implications of such environment dependence and consequent spatial variation are likely to become ever more important with the increased fragmentation and loss of suitable habitats for many natural populations.

Taming the massive genome of Scots pine with PiSy50k, a new genotyping array for conifer research.

Pinus sylvestris (Scots pine) is the most widespread coniferous tree in the boreal forests of Eurasia, with major economic and ecological importance. However, its large and repetitive genome presents a challenge for conducting genome-wide analyses such as association studies, genetic mapping and genomic selection. We present a new 50K single-nucleotide polymorphism (SNP) genotyping array for Scots pine research, breeding and other applications. To select the SNP set, we first genotyped 480 Scots pine samples on a 407 540 SNP screening array and identified 47 712 high-quality SNPs for the final array (called 'PiSy50k'). Here, we provide details of the design and testing, as well as allele frequency estimates from the discovery panel, functional annotation, tissue-specific expression patterns and expression level information for the SNPs or corresponding genes, when available. We validated the performance of the PiSy50k array using samples from Finland and Scotland. Overall, 39 678 (83.2%) SNPs showed low error rates (mean = 0.9%). Relatedness estimates based on array genotypes were consistent with the expected pedigrees, and the level of Mendelian error was negligible. In addition, array genotypes successfully discriminate between Scots pine populations of Finnish and Scottish origins. The PiSy50k SNP array will be a valuable tool for a wide variety of future genetic studies and forestry applications.

Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation.

Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations.

Variation in generation time reveals density regulation as an important driver of pace of life in a bird metapopulation.

Generation time determines the pace of key demographic and evolutionary processes. Quantified as the weighted mean age at reproduction, it can be studied as a life-history trait that varies within and among populations and may evolve in response to ecological conditions. We combined quantitative genetic analyses with age- and density-dependent models to study generation time variation in a bird metapopulation. Generation time was heritable, and males had longer generation times than females. Individuals with longer generation times had greater lifetime reproductive success but not a higher expected population growth rate. Density regulation acted on recruit production, suggesting that longer generation times should be favoured when populations are closer to carrying capacity. Furthermore, generation times were shorter when populations were growing and longer when populations were closer to equilibrium or declining. These results support classic theory predicting that density regulation is an important driver of the pace of life-history strategies.

Dispersal in a house sparrow metapopulation: An integrative case study of genetic assignment calibrated with ecological data and pedigree information.

Dispersal has a crucial role determining ecoevolutionary dynamics through both gene flow and population size regulation. However, to study dispersal and its consequences, one must distinguish immigrants from residents. Dispersers can be identified using telemetry, capture-mark-recapture (CMR) methods, or genetic assignment methods. All of these methods have disadvantages, such as high costs and substantial field efforts needed for telemetry and CMR surveys, and adequate genetic distance required in genetic assignment. In this study, we used genome-wide 200K Single Nucleotide Polymorphism data and two different genetic assignment approaches (GSI_SIM, Bayesian framework; BONE, network-based estimation) to identify the dispersers in a house sparrow (Passer domesticus) metapopulation sampled over 16 years. Our results showed higher assignment accuracy with BONE. Hence, we proceeded to diagnose potential sources of errors in the assignment results from the BONE method due to variation in levels of interpopulation genetic differentiation, intrapopulation genetic variation and sample size. We show that assignment accuracy is high even at low levels of genetic differentiation and that it increases with the proportion of a population that has been sampled. Finally, we highlight that dispersal studies integrating both ecological and genetic data provide robust assessments of the dispersal patterns in natural populations.

Resistance to gapeworm parasite has both additive and dominant genetic components in house sparrows, with evolutionary consequences for ability to respond to parasite challenge.

Host-parasite relationships are likely to change over the coming decades in response to climate change and increased anthropogenic stressors. Understanding the genetic architecture of parasite resistance will aid prediction of species' responses to intensified parasite challenge. The gapeworm "Syngamus trachea" is prevalent in natural bird populations and causes symptomatic infections ranging from mild to severe. The parasite may affect ecological processes by curtailing bird populations and is important due to its propensity to spread to commercially farmed birds. Our large-scale data set on an insular house sparrow metapopulation in northern Norway includes information on gapeworm prevalence and infection intensity, allowing assessment of the genetics of parasite resistance in a natural system. To determine whether parasite resistance has a heritable genetic component, we performed variance component analyses using animal models. Resistance to gapeworm had substantial additive genetic and dominance variance, and genome-wide association studies to identify single nucleotide polymorphisms associated with gapeworm resistance yielded multiple loci linked to immune function. Together with genome partitioning results, this indicates that resistance to gapeworm is under polygenic control in the house sparrow, and probably in other bird species. Hence, our results provide the foundation needed to study any eco-evolutionary processes related to gapeworm infection, and show that it is necessary to use methods suitable for polygenic and nonadditive genetic effects on the phenotype.

Animal models with group-specific additive genetic variances: extending genetic group models.

BACKGROUND: The animal model is a key tool in quantitative genetics and has been used extensively to estimate fundamental parameters, such as additive genetic variance or heritability. An implicit assumption of animal models is that all founder individuals derive from a single population. This assumption is commonly violated, for instance in crossbred livestock or when a meta-population is split into genetically differentiated subpopulations. Ignoring that base populations are genetically heterogeneous and thus split into different 'genetic groups' may lead to biased parameter estimates, especially for additive genetic variance. To avoid such biases, genetic group animal models, which account for the presence of more than one genetic group, have been proposed. Unfortunately, the method to date is only computationally feasible when the breeding values of the groups are allowed to differ in their means, but not in their variances. RESULTS: We present an extension of the animal model that permits estimation of group-specific additive genetic variances. This is achieved by employing group-specific relatedness matrices for the breeding value components to different genetic groups. We derive these matrices by decomposing the full relatedness matrix via the generalized Cholesky decomposition, and by scaling the respective matrix components for each group. We propose a computationally convenient approximation for the matrix component that encodes for the Mendelian sampling variance, and show that this approximation is not critical. In addition, we explain why segregation variances are often negligible when analyzing the complex polygenic traits that are frequently the focus of evolutionary ecologists and animal breeders. Simulations and an example from an insular meta-population of house sparrows in Norway with three distinct genetic groups illustrate that the method is successful in estimating group-specific additive genetic variances, and that segregation variances are indeed negligible in the empirical example. CONCLUSIONS: Quantifying differences in additive genetic variance within and among populations is of major biological interest in ecology, evolution, and animal and plant breeding. The proposed method allows to estimate such differences for subpopulations that form a connected set of populations, and may thus also be useful to study temporal or spatial variation of additive genetic variances.

Inferences of genetic architecture of bill morphology in house sparrow using a high-density SNP array point to a polygenic basis.

Understanding the genetic architecture of quantitative traits can provide insights into the mechanisms driving phenotypic evolution. Bill morphology is an ecologically important and phenotypically variable trait, which is highly heritable and closely linked to individual fitness. Thus, bill morphology traits are suitable candidates for gene mapping analyses. Previous studies have revealed several genes that may influence bill morphology, but the similarity of gene and allele effects between species and populations is unknown. Here, we develop a custom 200K SNP array and use it to examine the genetic basis of bill morphology in 1857 house sparrow individuals from a large-scale, island metapopulation off the coast of Northern Norway. We found high genomic heritabilities for bill depth and length, which were comparable with previous pedigree estimates. Candidate gene and genomewide association analyses yielded six significant loci, four of which have previously been associated with craniofacial development. Three of these loci are involved in bone morphogenic protein (BMP) signalling, suggesting a role for BMP genes in regulating bill morphology. However, these loci individually explain a small amount of variance. In combination with results from genome partitioning analyses, this indicates that bill morphology is a polygenic trait. Any studies of eco-evolutionary processes in bill morphology are therefore dependent on methods that can accommodate polygenic inheritance of the phenotype and molecular-scale evolution of genetic architecture.

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 (Ne ) 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.

No evidence of prenatal diversifying selection at locus or supertype levels in the dog MHC class II loci.

BACKGROUND: Despite decades of studying, the mechanisms maintaining high diversity in the genes of the Major Histocompatibility Complex (MHC) are still puzzling scientists. In addition to pathogen recognition and other functions, MHC molecules may act prenatally in mate choice and in maternal-foetal interactions. These interactions are potential selective mechanisms that increase genetic diversity in the MHC. During pregnancy, immune response has a dual role: the foetus represents foreign tissue compared to mother, but histo-incompatibility is required for successful pregnancy. We have studied the prenatal selection in MHC class II loci (DLA-DQA1, DLA-DQB1 and DLA-DRB1) in domestic dogs by comparing the observed and expected offspring genotype proportions in 110 dog families. Several potential selection targets were addressed, including the peptide-binding site, the MHC locus, three-locus haplotype and supertype levels. For the supertype analysis, the first canine supertype classification was created based on in silico analysis of peptide-binding amino-acid polymorphism. RESULTS: In most loci and levels, no deviation from the expected genotype frequencies was observed. However, one peptide-binding site in DLA-DRB1 had an excess of heterozygotes among the offspring. In addition, if the father shared a DLA-DRB1 allele with the mother, that allele was inherited by the offspring more frequently than expected, suggesting the selective advantage of a histo-compatible foetus, in contrast to our expectations. CONCLUSIONS: We conclude that there is some evidence of post-copulatory selection at nucleotide site level in the MHC loci of pet dogs. But due to no indication of selection at locus, three-locus, or supertype levels, we estimated that the prenatal selection coefficient is less than 0.3 in domestic dogs and very likely other factors are more important in maintaining the genetic diversity in MHC loci.