Traits In Natural Populations Research Articles

Mapping of quantitative trait loci for life history traits segregating within common frog populations.

The evolution of complex traits is often shaped by adaptive divergence. However, very little is known about the number, effect size, and location of the genomic regions influencing the variation of these traits in natural populations. Based on a dense linkage map of the common frog, Rana temporaria, we have localized, for the first time in amphibians, three significant and nine suggestive quantitative trait loci (QTLs) for metabolic rate, growth rate, development time, and weight at metamorphosis, explaining 5.6-18.9% of the overall phenotypic variation in each trait. We also found a potential pleiotropic QTL between development time and size at metamorphosis that, if confirmed, might underlie the previously reported genetic correlation between these traits. Furthermore, we demonstrate that the genetic variation linked to fitness-related larval traits segregates within Rana temporaria populations. This study provides the first insight into the genomic regions that affect larval life history traits in anurans, providing a valuable resource to delve further into the genomic basis of evolutionary change in amphibians.

Eco‐evolutionary dynamics of sexual selection and sexual conflict

AbstractThe research framework of eco‐evolutionary dynamics is increasing in popularity, as revealed by a steady stream of review articles and a recent and influential book, but primary empirical research is lagging behind. Moreover, the few empirical case studies demonstrating eco‐evolutionary dynamics might not be entirely representative.Much current research on eco‐evolutionary dynamics is focused on how ecological interactions lead to natural selection on phenotypic traits (“eco‐evo”), and in turn how the evolutionary change in such traits feed back on ecological dynamics (“evo‐eco”). A key feature of eco‐evolutionary dynamics is thus a feedback loop between ecology (e.g., population dynamics) and evolution (i.e., genetic change).In contrast to previous research on eco‐evolutionary dynamics driven by natural selection, the role of eco‐evolutionary feedbacks in sexual selection and sexual conflict is largely unknown. Here, I review theory and the limited empirical evidence in this area and identify some promising future lines of research.I update a past review on contemporary evolution of secondary sexual traits in natural populations and formulate six explicit and rigorous criteria for contemporary evolution of secondary sexual traits by natural or sexual selection or sexual conflict. I then discuss the other key prediction of eco‐evolutionary dynamics (i.e., evolution by sexual selection or sexual conflict shapes ecological dynamics). My overview reveals that our current knowledge in this area is limited and mainly come from theoretical models and laboratory experiments.A major challenge in eco‐evolutionary dynamics is therefore to link ecological and population dynamics with sexual selection and sexual conflict. This is not an easy task but might be possible with carefully chosen study systems and methods.Aplain language summaryis available for this article.

Natural selection on plasticity of thermal traits in a highly seasonal environment.

For ectothermic species with broad geographical distributions, latitudinal/altitudinal variation in environmental temperatures (averages and extremes) is expected to shape the evolution of physiological tolerances and the acclimation capacity (i.e., degree of phenotypic plasticity) of natural populations. This can create geographical gradients of selection in which environments with greater thermal variability (e.g., seasonality) tend to favor individuals that maximize performance across a broader range of temperatures compared to more stable environments. Although thermal acclimation capacity plays a fundamental role in this context, it is unknown whether natural selection targets this trait in natural populations. Additionally, understanding whether and how selection acts on thermal physiological plasticity is also highly relevant to climate change and biological conservation. Here, we addressed such an important gap in our knowledge in the northernmost population of the four‐eyed frog, Pleurodema thaul. We measured plastic responses of critical thermal limits for activity, behavioral thermal preference, and thermal sensitivity of metabolism to acclimation at 10 and 20°C. We monitored survival during three separate recapture efforts and used mark‐recapture integrated into an information‐theoretic approach to evaluate the relationship between survivals as a function of the plasticity of thermal traits. Overall, we found no evidence that thermal acclimation in this population is being targeted by directional selection, although there might be signals of selection on individual traits. According to the most supported models, survival increased in individuals with higher tolerance to cold when cold‐acclimated, probably because daily low extremes are frequent during the cooler periods of the year. Furthermore, survival increased with body size. However, in both cases, the directional selection estimates were nonsignificant, and the constraints of our experimental design prevented us from evaluating more complex models (i.e., nonlinear selection).

Sexual selection contributes to partial restoration of phenotypic robustness in a butterfly

Phenotypic variation is the raw material for selection that is ubiquitous for most traits in natural populations, yet the processes underlying phenotypic evolution or stasis often remain unclear. Here, we report phenotypic evolution in a mutant line of the butterfly Bicyclus anynana after outcrossing with the genetically polymorphic wild type population. The comet mutation modifies two phenotypic traits known to be under sexual selection in this butterfly: the dorsal forewing eyespots and the pheromone-producing structures. The original comet mutant line was inbred and remained phenotypically stable for at least seven years, but when outcrossed to the wild type population the outcrossed comet line surprisingly recovered the wild type phenotype within 8 generations at high (27 °C), but not at low (20 °C), developmental temperatures. Male mating success experiments then revealed that outcrossed comet males with the typical comet phenotype suffered from lower mating success, while mating success of outcrossed comet males resembling wild types was partially restored. We document a fortuitous case where the addition of genetic polymorphism around a spontaneous mutation could have allowed partial restoration of phenotypic robustness. We further argue that sexual selection through mate choice is likely the driving force leading to phenotypic robustness in our system.

Development of Target Sequence Capture and Estimation of Genomic Relatedness in a Mixed Oak Stand.

Anticipating the evolutionary responses of long-lived organisms, such as trees, to environmental changes, requires the assessment of genetic variation of adaptive traits in natural populations. To this end, high-density markers are needed to calculate genomic relatedness between individuals allowing to estimate the genetic variance of traits in wild populations. We designed a targeted capture-based, next-generation sequencing assay based on the highly heterozygous pedunculate oak (Quercus robur) reference genome, for the sequencing of 3 Mb of genic and intergenic regions. Using a mixed stand of 293 Q. robur and Q. petraea genotypes we successfully captured over 97% of the target sequences, corresponding to 0.39% of the oak genome, with sufficient depth (97×) for the detection of about 190,000 SNPs evenly spread over the targeted regions. We validated the technique by evaluating its reproducibility, and comparing the genomic relatedness of trees with their known pedigree relationship. We explored the use of the technique on other related species and highlighted the advantages and limitations of this approach. We found that 92.07% of target sequences in Q. suber and 70.36% of sequences in Fagus sylvatica were captured. We used this SNP resource to estimate genetic relatedness in the mixed oak stand. Mean pairwise genetic relatedness was low within each species with a few values exceeding 0.25 (half-sibs) or 0.5 (full-sibs). Finally, we applied the technique to a long-standing issue in population genetics of trees regarding the relationship between inbreeding and components of fitness. We found very weak signals for inbreeding depression for reproductive success and no signal for growth within both species.

Structure of the phenotypic variability of fruit and seed traits in natural populations of Eugenia dysenterica dc. (Myrtaceae)

Abstract Eugenia dysenterica DC. (cagaita tree) is a fruit tree native to the Brazilian Cerrado. It is a promising species for cultivation, but little basic information exists on the phenotypic diversity and quantitative variation of its fruits and seeds at a population scale. Thus, the present study proposes to estimate the phenotypic parameters of the species’ fruits and seeds based on the variability among mother plants and among subpopulations, thereby aiming to increase knowledge for breeding and conservation of the species. For this, 25 natural subpopulations (local populations) were sampled in five Brazilian states. Within each subpopulation, 20 fruits were collected from each of six sampled mother plants. Data for biomass, transverse and longitudinal lengths of the fruits and seeds were subjected to estimates of descriptive parameters, correlation and hierarchical analysis of variance (ANOVA). Significant variation, including high levels of phenotypic variation, was observed among mother plants within the subpopulations and between the subpopulations. The high variation and the formation of phenotypically divergent groups are important elements for the breeding of cagaita tree, whose mother plants can now be selected for the traits studied. Phenotypic divergence between populations (PST) can be used as an indicator of the structuring of the phenotypic variation of the species in its natural area of occurrence.

Phenotypic plasticity in response to temperature fluctuations is genetically variable, and relates to climatic variability of origin, in Arabidopsis thaliana.

Under current climate change, increasing mean temperatures are not only causing hotter summers, but temperature variability is increasing as well. Phenotypic plasticity can help plants to overcome negative effects of temperature variability and allow them to rapidly adjust traits to adverse conditions. Moreover, genetic variation in such plasticity could provide potential for adaptive evolution in response to changing climate variability. Here, we conducted an experiment with 11 Arabidopsis thaliana genotypes to investigate intraspecific variation in plant responses to two aspects of variable temperature stress: timing and frequency. We found that the timing but not frequency of temperature stress affected the phenology, growth, reproduction and allocation strategy of plants, and that genotypes differed substantially in their responses. Moreover, trait plasticity was positively related to precipitation variability of origin, suggesting an adaptive role of plasticity. Our results indicate that the developmental stage of a plant during heat stress is a key determinant of its response, and that plasticity to temperature variability is an evolving and possibly adaptive trait in natural populations of A. thaliana. More generally, our study demonstrates the usefulness of studying plant responses to climatic variability per se, given that climatic variability is predicted to increase in the future.

Within-individual variation in signal production limits female choice in noisy treefrog choruses

In acoustically communicating animals such as anurans and orthopterans, individual signalers can display remarkable variation in signal traits, even within a single bout of calling. This within-individual variation has the potential to “mask” the between-individual variation that is the target of sexual selection. Thus, receivers may not always be able to discriminate among males based on properties of their acoustic signals, even when female choice is well documented in the lab. The effect of within-individual variation may be compounded by noise generated by breeding choruses of conspecifics, which can prevent signal detection or discrimination. We manipulated within-individual variation in two signal traits (call rate and pulse rate) that are critically important for mate choice in Hyla chrysoscelis, Cope’s gray treefrog. We replicated our design at three realistic levels of chorus noise. Within-individual variation in signal traits reduced the strength of sexual selection on one of two traits, and receivers were less likely to discriminate against lower-quality signals under conditions of realistic chorus noise. Our results suggest that preference functions generated using stimuli that lack within-individual variation, under ideal listening conditions, may chronically over-estimate the strength of sexual selection on signal traits in natural populations.

A multilocus association analysis method integrating phenotype and expression data reveals multiple novel associations to flowering time variation in wild-collected Arabidopsis thaliana.

The adaptation to a new habitat often results in a confounding between genomewide genotype and beneficial alleles. When the confounding is strong, or the allelic effects is weak, it is a major statistical challenge to detect the adaptive polymorphisms. We describe a novel approach to dissect polygenic traits in natural populations. First, candidate adaptive loci are identified by screening for loci directly associated with the adaptive trait or the expression of genes known to affect it. Then, a multilocus genetic architecture is inferred using a backward elimination association analysis across all candidate loci with an adaptive false discovery rate-based threshold. Effects of population stratification are controlled by accounting for genomic kinship in both steps of the analysis and also by simultaneously testing all candidate loci in the multilocus model. We illustrate the method by exploring the polygenic basis of an important adaptive trait, flowering time in Arabidopsis thaliana, using public data from the 1,001 genomes project. We revealed associations between 33 (29) loci and flowering time at 10 (16)°C in this collection of natural accessions, where standard genomewide association analysis methods detected five (3) loci. The 33 (29) loci explained approximately 55.1 (48.7)% of the total phenotypic variance of the respective traits. Our work illustrates how the genetic basis of highly polygenic adaptive traits in natural populations can be explored in much greater detail using new multilocus mapping approaches taking advantage of prior biological information, genome and transcriptome data.

Sex differences in adult mortality rate mediated by early-life environmental conditions.

Variation in sex differences is affected by both genetic and environmental variation, with rapid change in sex differences being more likely due to environmental change. One case of rapid change in sex differences is human lifespan, which has become increasingly female-biased in recent centuries. Long-term consequences of variation in the early-life environment may, in part, explain such variation in sex differences, but whether the early-life environment mediates sex differences in life-history traits is poorly understood in animals. Combining longitudinal data on 60 cohorts of pre-industrial Finns with environmental data, we show that the early-life environment is associated with sex differences in adult mortality and expected lifespan. Specifically, low infant survival rates and high rye yields (an important food source) in early-life are associated with female-bias in adult lifespan. These results support the hypothesis that environmental change has the potential to affect sex differences in life-history traits in natural populations of long-lived mammals.

The Genetic Architecture of Ovariole Number in Drosophila melanogaster: Genes with Major, Quantitative, and Pleiotropic Effects.

Ovariole number has a direct role in the number of eggs produced by an insect, suggesting that it is a key morphological fitness trait. Many studies have documented the variability of ovariole number and its relationship to other fitness and life-history traits in natural populations of Drosophila. However, the genes contributing to this variability are largely unknown. Here, we conducted a genome-wide association study of ovariole number in a natural population of flies. Using mutations and RNAi-mediated knockdown, we confirmed the effects of 24 candidate genes on ovariole number, including a novel gene, anneboleyn (formerly CG32000), that impacts both ovariole morphology and numbers of offspring produced. We also identified pleiotropic genes between ovariole number traits and sleep and activity behavior. While few polymorphisms overlapped between sleep parameters and ovariole number, 39 candidate genes were nevertheless in common. We verified the effects of seven genes on both ovariole number and sleep: bin3, blot, CG42389, kirre, slim, VAChT, and zfh1. Linkage disequilibrium among the polymorphisms in these common genes was low, suggesting that these polymorphisms may evolve independently.

SNP Discovery and Genetic Variation of Candidate Genes Relevant to Heat Tolerance and Agronomic Traits in Natural Populations of Sand Rice (Agriophyllum squarrosum).

The extreme stress tolerance and high nutritional value of sand rice (Agriophyllum squarrosum) make it attractive for use as an alternative crop in response to concerns about ongoing climate change and future food security. However, a lack of genetic information hinders understanding of the mechanisms underpinning the morphological and physiological adaptations of sand rice. In the present study, we sequenced and analyzed the transcriptomes of two individuals representing semi-arid [Naiman (NM)] and arid [Shapotou (SPT)] sand rice genotypes. A total of 105,868 pairwise single nucleotide polymorphisms (SNPs) distributed in 24,712 Unigenes were identified among SPT and NM samples; the average SNP frequency was 0.3% (one SNP per 333 base pair). Characterization of gene annotation demonstrated that variations in genes involved in DNA recombination were associated with the survival of the NM population in the semi-arid environment. A set of genes predicted to be relevant to heat stress response and agronomic traits was functionally annotated using the accumulated knowledge from Arabidopsis and several crop plants, including rice, barley, maize, and sorghum. Four candidate genes related to heat tolerance (heat-shock transcription factor, HsfA1d), seed size (DA1-Related, DAR1), and flowering (early flowering 3, ELF3 and late elongated hypocotyl, LHY) were subjected to analysis of the genetic diversity in 10 natural populations, representing the core germplasm resource across the area of sand rice distribution in China. Only one SNP was detected in each of HsfA1d and DAR1, among 60 genotypes, with two in ELF3 and four in LHY. Nucleotide diversity ranged from 0.00032 to 0.00118. Haplotype analysis indicated that the NM population carried a specific allele for all four genes, suggesting that divergence has occurred between NM and other populations. These four genes could be further analyzed to determine whether they are associated with phenotype variation and identify alleles favorable for sand rice breeding.

Within-season variation in sexual selection on flight performance and flight-related traits in a damselfly

While selection is a key mechanism of evolution, our understanding of within-season variation in sexual selection remains limited. Here, we studied within-season sexual selection on two key performance traits, flight speed and flight endurance, and a set of morphological and physiological phenotypic traits in a natural population of the territorial damselfly Chalcolestes viridis. We applied a path analysis approach to address whether the flight-related traits affected mating success directly or indirectly through their effect on the flight performance traits, and whether these selection patterns differed between the first and second half of the reproductive season. While some trait means did not differ between both parts of the season (flight speed, wing loading and non-allometric wing shape), most traits showed within-season differences (flight endurance, fat content, flight muscle ratio, wing centroid size, body mass and the allometric wing shape). Despite the within-season temporal differences in flight endurance, sexual selection consistently favoured males with a higher flight endurance. None of the detected patterns of sexual selection on the flight-related traits were consistently significant in both periods: while we detected selection on wing loading and wing centroid size in the first half of the season, we detected selection on body mass in the second half of the season. More studies focusing on understudied traits such as performance traits are needed to refine our knowledge of the temporal dynamics of selection patterns in nature. This is important to arrive at a better understanding of the adaptive evolutionary dynamics of traits in natural populations.

Social environment affects female preference for male body color during development in artificially selected varieties of Poecilia latipinna

This study provides evidence for an effect of social environment on color morph preference during development in two artificially selected varieties of the live-bearing fish Poecilia latipinna. Black-colored females reared exclusively in the presence of white-colored adults preferred to associate with white vs black males when tested using a standard dichotomous choice design. Similarly, white females reared exclusively in the presence of black adults showed a preference for black males in identical dichotomous choice tests. However, both black and white females when reared separately in the presence of a mix of black and white adults showed no preference for either male color variety. A second round of testing revealed that their preferences (or lack thereof), although significantly weaker, persisted for at least a week after the initial tests during which the model groups were altered; groups reared in the presence of opposite-colored adults were exposed to mixed-color adults, while groups reared in the presence of mixed-color adults were exposed to opposite-color models. Taken together, these data indicate that the females’ social environment during the first 2 months of life affected the development of preferences for male body color and further suggest such social learning could potentially influence mate and/or shoaling preferences for color and perhaps other traits in natural populations of P. latipinna.

Limited Contribution of DNA Methylation Variation to Expression Regulation in Arabidopsis thaliana.

The extent to which epigenetic variation affects complex traits in natural populations is not known. We addressed this question using transcriptome and DNA methylation data from a sample of 135 sequenced A. thaliana accessions. Across individuals, expression was significantly associated with cis-methylation for hundreds of genes, and many of these associations remained significant after taking SNP effects into account. The pattern of correlations differed markedly between gene body methylation and transposable element methylation. The former was usually positively correlated with expression, and the latter usually negatively correlated, although exceptions were found in both cases. Finally, we developed graphical models of causality that adapt to a sample with heavy population structure, and used them to show that while methylation appears to affect gene expression more often than expression affects methylation, there is also strong support for both being independently controlled. In conclusion, although we find clear evidence for epigenetic regulation, both the number of loci affected and the magnitude of the effects appear to be small compared to the effect of SNPs.

Evolutionary potential in the Alpine: trait heritabilities and performance variation of the dwarf willow Salix herbacea from different elevations and microhabitats.

Alpine ecosystems are seriously threatened by climate change. One of the key mechanisms by which plants can adapt to changing environmental conditions is through evolutionary change. However, we still know little about the evolutionary potential in wild populations of long‐lived alpine plants. Here, we investigated heritabilities of phenological traits, leaf size, and performance traits in natural populations of the long‐lived alpine dwarf shrub Salix herbacea using relatedness estimates inferred from SSR (Simple Sequence Repeat) markers. Salix herbacea occurs in early‐ and late‐snowmelt microhabitats (ridges and snowbeds), and we assessed how performance consequences of phenological traits and leaf size differ between these microhabitats in order to infer potential for evolutionary responses. Salix herbacea showed low, but significant, heritabilities of leaf size, clonal and sexual reproduction, and moderate heritabilities of phenological traits. In both microhabitats, we found that larger leaves, longer intervals between snowmelt and leaf expansion, and longer GDD (growing‐degree days) until leaf expansion resulted in a stronger increase in the number of stems (clonal reproduction). In snowbeds, clonal reproduction increased with a shorter GDD until flowering, while the opposite was found on ridges. Furthermore, the proportion of flowering stems increased with GDD until flowering in both microhabitats. Our results suggest that the presence of significant heritable variation in morphology and phenology might help S. herbacea to adapt to changing environmental conditions. However, it remains to be seen if the rate of such an evolutionary response can keep pace with the rapid rate of climate change.

Variation in needle and cone traits in natural populations of Pinus yunnanensis

Pinus yunnanensis Franch. is a major component of coniferous forests in southwestern China. Little is known about its intraspecific variation. Morphological variations in needle and cone traits of P. yunnanensis were analyzed to quantify variability among and within natural populations. Seven traits were measured on 10 needles collected from 30 trees in each of the 18 sampled populations of P. yunnanensis. Four cone traits were measured in 221 individual trees from nine populations. The results showed that there were significant differences (p < 0.01) both among populations and within populations in each needle and cone trait. The proportion of phenotypic variation of nearly all needle and cone traits was over 50 % within populations, which showed trees within populations accounted for a majority of the total variation. The needle traits showed higher variability within population than cone traits. Variability in the needle traits was correlated with geo-climatic parameters (longitude, latitude, altitude, temperature, and precipitation). Needle length and the ratio of needle length to fascicle sheath length showed clinal variation in response to latitudinal and altitudinal gradients. A hierarchical classification of all populations based on needle traits led to the formation of four major groups. The findings provide important genetic information for the evaluation of variation. Moreover, it will assist in management of genetic diversity of P. yunnanensis.

Transcriptomics of colour patterning and coloration shifts in crows.

Animal coloration is one of the most conspicuous phenotypic traits in natural populations and has important implications for adaptation and speciation. Changes in coloration can occur over surprisingly short evolutionary timescales, while recurrence of similar colour patterns across large phylogenetic distances is also common. Even though the genetic basis of pigment production is well understood, little is known about the mechanisms regulating colour patterning. In this study, we shed light on the molecular elements regulating regional pigment production in two genetically near-identical crow taxa with striking differences in a eumelanin-based phenotype: black carrion and grey-coated hooded crows. We produced a high-quality genome annotation and analysed transcriptome data from a 2×2 design of active melanogenic feather follicles from head (black in both taxa) and torso (black in carrion and grey in hooded crow). Extensive, parallel expression differences between body regions in both taxa, enriched for melanogenesis genes (e.g. ASIP, CORIN, and ALDH6), indicated the presence of cryptic prepatterning also in all-black carrion crows. Meanwhile, colour-specific expression (grey vs. black) was limited to a small number of melanogenesis genes in close association with the central transcription factor MITF (most notably HPGDS, NDP and RASGRF1). We conclude that colour pattern differences between the taxa likely result from an interaction between divergence in upstream elements of the melanogenesis pathway and genes that provide an underlying prepattern across the body through positional information. A model of evolutionary stable prepatterns that can be exposed and masked through simple regulatory changes may explain the phylogenetically independent recurrence of colour patterns that is observed across corvids and many other vertebrate groups.

Effects of spring temperatures on the strength of selection on timing of reproduction in a long-distance migratory bird.

Climate change has differentially affected the timing of seasonal events for interacting trophic levels, and this has often led to increased selection on seasonal timing. Yet, the environmental variables driving this selection have rarely been identified, limiting our ability to predict future ecological impacts of climate change. Using a dataset spanning 31 years from a natural population of pied flycatchers (Ficedula hypoleuca), we show that directional selection on timing of reproduction intensified in the first two decades (1980–2000) but weakened during the last decade (2001–2010). Against expectation, this pattern could not be explained by the temporal variation in the phenological mismatch with food abundance. We therefore explored an alternative hypothesis that selection on timing was affected by conditions individuals experience when arriving in spring at the breeding grounds: arriving early in cold conditions may reduce survival. First, we show that in female recruits, spring arrival date in the first breeding year correlates positively with hatch date; hence, early-hatched individuals experience colder conditions at arrival than late-hatched individuals. Second, we show that when temperatures at arrival in the recruitment year were high, early-hatched young had a higher recruitment probability than when temperatures were low. We interpret this as a potential cost of arriving early in colder years, and climate warming may have reduced this cost. We thus show that higher temperatures in the arrival year of recruits were associated with stronger selection for early reproduction in the years these birds were born. As arrival temperatures in the beginning of the study increased, but recently declined again, directional selection on timing of reproduction showed a nonlinear change. We demonstrate that environmental conditions with a lag of up to two years can alter selection on phenological traits in natural populations, something that has important implications for our understanding of how climate can alter patterns of selection in natural populations.

Heterogeneity of genetic architecture of body size traits in a free-living population.

Knowledge of the underlying genetic architecture of quantitative traits could aid in understanding how they evolve. In wild populations, it is still largely unknown whether complex traits are polygenic or influenced by few loci with major effect, due to often small sample sizes and low resolution of marker panels. Here, we examine the genetic architecture of five adult body size traits in a free‐living population of Soay sheep on St Kilda using 37 037 polymorphic SNPs. Two traits (jaw and weight) show classical signs of a polygenic trait: the proportion of variance explained by a chromosome was proportional to its length, multiple chromosomes and genomic regions explained significant amounts of phenotypic variance, but no SNPs were associated with trait variance when using GWAS. In comparison, genetic variance for leg length traits (foreleg, hindleg and metacarpal) was disproportionately explained by two SNPs on chromosomes 16 (s23172.1) and 19 (s74894.1), which each explained >10% of the additive genetic variance. After controlling for environmental differences, females heterozygous for s74894.1 produced more lambs and recruits during their lifetime than females homozygous for the common allele conferring long legs. We also demonstrate that alleles conferring shorter legs have likely entered the population through a historic admixture event with the Dunface sheep. In summary, we show that different proxies for body size can have very different genetic architecture and that dense SNP helps in understanding both the mode of selection and the evolutionary history at loci underlying quantitative traits in natural populations.