Spatial variation in the evolutionary potential and constraints of basal metabolic rate and body mass in a wild bird.

An organism's energy budget is strongly related to resource consumption, performance, and fitness. Hence, understanding the evolution of key energetic traits, such as basal metabolic rate (BMR), in natural populations is central for understanding life-history evolution and ecological processes. Here we used quantitative genetic analyses to study evolutionary potential of BMR in two insular populations of the house sparrow (Passer domesticus). We obtained measurements of BMR and body mass (Mb ) from 911 house sparrows on the islands of Leka and Vega along the coast of Norway. These two populations were the source populations for translocations to create an additional third, admixed 'common garden' population in 2012. With the use of a novel genetic group animal model concomitant with a genetically determined pedigree, we differentiate genetic and environmental sources of variation, thereby providing insight into the effects of spatial population structure on evolutionary potential. We found that the evolutionary potential of BMR was similar in the two source populations, whereas the Vega population had a somewhat higher evolutionary potential of Mb than the Leka population. BMR was genetically correlated with Mb in both populations, and the conditional evolutionary potential of BMR (independent of body mass) was 41% (Leka) and 53% (Vega) lower than unconditional estimates. Overall, our results show that there is potential for BMR to evolve independently of Mb , but that selection on BMR and/or Mb may have different evolutionary consequences in different populations of the same species.

Large-effect loci mediate rapid adaptation of salmon body size after river regulation.

Understanding the potential of natural populations to adapt to altered environments is becoming increasingly relevant in evolutionary research. Currently, our understanding of adaptation to human alteration of the environment is hampered by lack of knowledge on the genetic basis of traits, lack of time series, and little or no information on changes in optimal trait values. Here, we used time series data spanning nearly a century to investigate how the body mass of Atlantic salmon (Salmo salar) adapts to river regulation. We found that the change in body mass followed the change in waterflow, both decreasing to ∼1/3 of their original values. Allele frequency changes at two loci in the regions of vgll3 and six6 predicted more than 80% of the observed body mass reduction. Modeling the adaptive dynamics revealed that the population mean lagged behind its optimum before catching up approximately six salmon generations after the initial waterflow reduction. Our results demonstrate rapid adaptation mediated by large-effect loci and provide insight into the temporal dynamics of evolutionary rescue following human disturbance.

Introgression from farmed escapees affects the full life cycle of wild Atlantic salmon.

After a half a century of salmon farming, we have yet to understand how the influx of genes from farmed escapees affects the full life history of Atlantic salmon (Salmo salar L.) in the wild. Using scale samples of over 6900 wild adult salmon from 105 rivers, we document that increased farmed genetic ancestry is associated with increased growth throughout life and a younger age at both seaward migration and sexual maturity. There was large among-population variation in the effects of introgression. Most saliently, the increased growth at sea following introgression declined with the population's average growth potential. Variation at two major-effect loci associated with age at maturity was little affected by farmed genetic ancestry and could not explain the observed phenotypic effects of introgression. Our study provides knowledge crucial for predicting the ecological and evolutionary consequences of increased aquaculture production worldwide.

Fur colour in the Arctic fox: genetic architecture and consequences for fitness.

Genome-wide association studies provide good opportunities for studying the genetic basis of adaptive traits in wild populations. Yet, previous studies often failed to identify major effect genes. In this study, we used high-density single nucleotide polymorphism and individual fitness data from a wild non-model species. Using a whole-genome approach, we identified the MC1R gene as the sole causal gene underlying Arctic fox Vulpes lagopus fur colour. Further, we showed the adaptive importance of fur colour genotypes through measures of fitness that link ecological and evolutionary processes. We found a tendency for blue foxes that are heterozygous at the fur colour locus to have higher fitness than homozygous white foxes. The effect of genotype on fitness was independent of winter duration but varied with prey availability, with the strongest effect in years of increasing rodent populations. MC1R is located in a genomic region with high gene density, and we discuss the potential for indirect selection through linkage and pleiotropy. Our study shows that whole-genome analyses can be successfully applied to wild species and identify major effect genes underlying adaptive traits. Furthermore, we show how this approach can be used to identify knowledge gaps in our understanding of interactions between ecology and evolution.

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.

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.

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.

Consequences of past climate change and recent human persecution on mitogenomic diversity in the arctic fox.

Ancient DNA provides a powerful means to investigate the timing, rate and extent of population declines caused by extrinsic factors, such as past climate change and human activities. One species probably affected by both these factors is the arctic fox, which had a large distribution during the last glaciation that subsequently contracted at the start of the Holocene. More recently, the arctic fox population in Scandinavia went through a demographic bottleneck owing to human persecution. To investigate the consequences of these processes, we generated mitogenome sequences from a temporal dataset comprising Pleistocene, historical and modern arctic fox samples. We found no evidence that Pleistocene populations in mid-latitude Europe or Russia contributed to the present-day gene pool of the Scandinavian population, suggesting that postglacial climate warming led to local population extinctions. Furthermore, during the twentieth-century bottleneck in Scandinavia, at least half of the mitogenome haplotypes were lost, consistent with a 20-fold reduction in female effective population size. In conclusion, these results suggest that the arctic fox in mainland Western Europe has lost genetic diversity as a result of both past climate change and human persecution. Consequently, it might be particularly vulnerable to the future challenges posed by climate change. This article is part of a discussion meeting issue 'The past is a foreign country: how much can the fossil record actually inform conservation?'

Supplementary stocking selects for domesticated genotypes.

Stocking of hatchery produced fish is common practise to mitigate declines in natural populations and may have unwanted genetic consequences. Here we describe a novel phenomenon arising where broodstock used for stocking may be introgressed with farmed individuals. We test how stocking affects introgression in a wild population of Atlantic salmon (Salmo salar) by quantifying how the number of adult offspring recaptured in a stocked river depend on parental introgression. We found that hatchery conditions favour farmed genotypes such that introgressed broodstock produce up to four times the number of adult offspring compared to non-introgressed broodstock, leading to increased introgression in the recipient spawning population. Our results provide the first empirical evidence that stocking can unintentionally favour introgressed individuals and through selection for domesticated genotypes compromise the fitness of stocked wild populations.

Signatures of genetic adaptation to extremely varied Australian environments in introduced European house sparrows.

Due to its history of multiple introductions to novel environments worldwide, the house sparrow has been used as a model species to study local adaption in invasive avian species. New genomic resources such as a custom 200K SNP array and a house sparrow reference genome provide great prospects for studying rapid local adaptation in this invasive species. Here, we analyse high-density genomewide genetic data collected across an extensive range of temperate, arid and tropical climates, in Australian populations that were introduced from Europe 150 years ago. We used two population differentiation (PD) and two ecological association (EA) methods to identify putative loci subject to selection across these varied climates. A majority of the outlier SNPs were identified through the use of the latent factor mixed models (LFMM) EA method, but the BayeScEnv EA method had the strongest overlap with the outliers from the two PD methods. Out of all the 971 outliers identified across the different methods, 38.3% were physically linked (within 20 kbps) to 575 known protein-coding regions in the house sparrow reference genome. Interestingly, some outlier genes had been previously identified in genome scan studies of broadly distributed species or had strong links to traits that are expected to be important to local adaptation, for example, heat-shock proteins, immune response and HOX genes. However, many outliers still have unknown relevance and some outliers can be false positives. Our results identify an opportunity to use the house sparrow model to further study local adaptation in an invasive species.

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.

The genomic mosaicism of hybrid speciation.

Hybridization is widespread in nature and, in some instances, can result in the formation of a new hybrid species. We investigate the genetic foundation of this poorly understood process through whole-genome analysis of the hybrid Italian sparrow and its progenitors. We find overall balanced yet heterogeneous levels of contribution from each parent species throughout the hybrid genome and identify areas of novel divergence in the hybrid species exhibiting signals consistent with balancing selection. High-divergence areas are disproportionately located on the Z chromosome and overrepresented in gene networks relating to key traits separating the focal species, which are likely involved in reproductive barriers and/or species-specific adaptations. Of special interest are genes and functional groups known to affect body patterning, beak morphology, and the immune system, which are important features of diversification and fitness. We show that a combination of mosaic parental inheritance and novel divergence within the hybrid lineage has facilitated the origin and maintenance of an avian hybrid species.

Controlling for P-value inflation in allele frequency change in experimental evolution and artificial selection experiments.

Experimental evolution studies can be used to explore genomic response to artificial and natural selection. In such studies, loci that display larger allele frequency change than expected by genetic drift alone are assumed to be directly or indirectly associated with traits under selection. However, such studies report surprisingly many loci under selection, suggesting that current tests for allele frequency change may be subject to P-value inflation and hence be anticonservative. One factor known from genomewide association (GWA) studies to cause P-value inflation is population stratification, such as relatedness among individuals. Here, we suggest that by treating presence of an individual in a population after selection as a binary response variable, existing GWA methods can be used to account for relatedness when estimating allele frequency change. We show that accounting for relatedness like this effectively reduces false-positives in tests for allele frequency change in simulated data with varying levels of population structure. However, once relatedness has been accounted for, the power to detect causal loci under selection is low. Finally, we demonstrate the presence of P-value inflation in allele frequency change in empirical data spanning multiple generations from an artificial selection experiment on tarsus length in two free-living populations of house sparrow and correct for this using genomic control. Our results indicate that since allele frequencies in large parts of the genome may change when selection acts on a heritable trait, such selection is likely to have considerable and immediate consequences for the eco-evolutionary dynamics of the affected populations.

The easy road to genome-wide medium density SNP screening in a non-model species: development and application of a 10 K SNP-chip for the house sparrow (Passer domesticus).

With the advent of next generation sequencing, new avenues have opened to study genomics in wild populations of non-model species. Here, we describe a successful approach to a genome-wide medium density Single Nucleotide Polymorphism (SNP) panel in a non-model species, the house sparrow (Passer domesticus), through the development of a 10 K Illumina iSelect HD BeadChip. Genomic DNA and cDNA derived from six individuals were sequenced on a 454 GS FLX system and generated a total of 1.2 million sequences, in which SNPs were detected. As no reference genome exists for the house sparrow, we used the zebra finch (Taeniopygia guttata) reference genome to determine the most likely position of each SNP. The 10 000 SNPs on the SNP-chip were selected to be distributed evenly across 31 chromosomes, giving on average one SNP per 100 000 bp. The SNP-chip was screened across 1968 individual house sparrows from four island populations. Of the original 10 000 SNPs, 7413 were found to be variable, and 99% of these SNPs were successfully called in at least 93% of all individuals. We used the SNP-chip to demonstrate the ability of such genome-wide marker data to detect population sub-division, and compared these results to similar analyses using microsatellites. The SNP-chip will be used to map Quantitative Trait Loci (QTL) for fitness-related phenotypic traits in natural populations.

Phylogeography of the prehensile-tailed skink Corucia zebrata on the Solomon Archipelago.

The biogeography of islands is often strongly influenced by prior geological events. Corucia zebrata (Squamata: Scincidae) is endemic to the geologically complex Solomon Archipelago in Northern Melanesia. We examined the level of divergence for different island populations of C. zebrata and discussed these patterns in light of Pleistocene land bridges, island isolation, and island age. Corucia zebrata was sampled from 14 locations across the Solomon Archipelago and sequenced at two mitochondrial genes (ND2 and ND4; 1697 bp in total) and four nuclear loci (rhodopsin, an unknown intron, AKAP9, and PTPN12). Measures of genetic divergence, analyses of genetic variation, and Bayesian phylogenetic inference were used and the data assessed in light of geological information. Populations of C. zebrata on separate islands were found to be genetically different from each other, with reciprocal monophyly on mitochondrial DNA. Populations on islands previously connected by Pleistocene land bridges were marginally less divergent from each other than from populations on other nearby but isolated islands. There are indications that C. zebrata has radiated across the eastern islands of the archipelago within the last 1-4 million years. Nuclear loci were not sufficiently informative to yield further information about the phylogeography of C. zebrata on the Solomon Archipelago. Analyses of the mitochondrial data suggest that dispersal between islands has been very limited and that there are barriers to gene flow within the major islands. Islands that have been isolated during the Pleistocene glacial cycles are somewhat divergent in their mitochondrial genotypes, however, isolation by distance (IBD) and recent colonization of isolated but geologically younger islands appear to have had stronger effects on the phylogeography of C. zebrata than the Pleistocene glacial cycles. This contrasts with patterns reported for avian taxa, and highlights the fact that biogeographic regions for island species cannot be directly extrapolated among taxa of differing dispersal ability.