QTL analysis of clinical-chemical traits in an F₂ intercross between Landrace and Korean native pigs

Clinical-chemical traits are essential when examining the health status of individuals. The aim of this study was to identify quantitative trait loci (QTL) and the associated positional candidate genes affecting clinical-chemical traits in a reciprocal F(2) intercross between Landrace and Korean native pigs. Following an overnight fast, 25 serum phenotypes related to clinical-chemical traits (e.g., hepatic function parameters, renal function parameters, electrolyte, lipids) were measured in >970 F(2) progeny. All experimental samples were subjected to genotyping analysis using 165 microsatellite markers located across the genome. We identified eleven genome-wide significant QTL in six chromosomal regions (SSC 2, 7, 8, 13, 14, and 15) and 59 suggestive QTL in 17 chromosomal regions (SSC 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 12, 13, 14, 15, 16, 17, and 18). We also observed significant effects of reciprocal crosses on some of the traits, which would seem to result from maternal effect, QTL on sex chromosomes, imprinted genes, or genetic difference in mitochondrial DNA. The role of genomic imprinting in clinical-chemical traits also was investigated. Genome-wide analysis revealed a significant evidence for an imprinted QTL in SSC4 affecting serum amylase levels. Additionally, a series of bivariate linkage analysis provided strong evidence that QTL in SSC 2, 13, 15, and 18 have a pleiotropic effect on clinical-chemical traits. In conclusion, our study detected both novel and previously reported QTL influencing clinical-chemical traits in pigs. The identified QTL together with the positional candidate genes identified here could play an important role in elucidating the genetic structure of clinical-chemical phenotype variation in humans and swine.     

Sexual dimorphism in the quantitative-genetic architecture of floral, leaf, and allocation traits in Silene latifolia

Many species exhibit sexual dimorphism in a variety of characters, and the underlying genetic architecture of dimorphism potentially involves sex-specific differences in the additive-genetic variance-covariance matrix (G) of dimorphic traits. We investigated the quantitative-genetic structure of dimorphic traits in the dioecious plant Silene latifolia by estimating G (including within-sex matrices, G(m), G(f), and the between-sex variance-covariance matrix, B), and the phenotypic variance-covariance matrix (P) for seven traits. Flower number was the most sexually dimorphic trait, and was significantly genetically correlated with all traits within each sex. Negative genetic correlations between flower size and number suggested a genetic trade-off in investment, but positive environmental correlations between the same traits resulted in no physical evidence for a trade-off in the phenotype. Between-sex genetic covariances for homologous traits were always greater than 0 but smaller than 1, showing that some, but not all, of the variation in traits is caused by genes or alleles with sex-limited expression. Using common principal-components analysis (CPCA), a maximum-likelihood (ML) estimation approach, and element-by-element comparison to compare matrices, we found that G(m) and G(f) differed significantly in eigenstructure because of dissimilarity in covariances involving leaf traits, suggesting the presence of variation in sex-limited genes with pleiotropic effects and/or linkage between sex-limited loci. The sex-specific structure of G is expected to cause differences in the correlated responses to selection within each sex, promoting the further evolution and maintenance of dimorphism.     

Idiosyncratic evolution of maternal effects in response to juvenile malnutrition in Drosophila

Maternal effects often affect fitness traits, but there is little experimental evidence pertaining to their contribution to response to selection imposed by novel environments. We studied the evolution of maternal effects in Drosophila populations selected for tolerance to chronic larval malnutrition. To this end, we performed pairwise reciprocal F₁ crosses between six selected (malnutrition tolerant) populations and six unselected control populations and assessed the effect of cross direction on larval growth and developmental rate, adult weight and egg‐to‐adult viability expressed under the malnutrition regime. Each pair of reciprocal crosses revealed large maternal effects (possibly including cytoplasmic genetic effects) on at least one trait, but the magnitude, sign and which traits were affected varied among populations. Thus, maternal effects contributed significantly to the response to selection imposed by the malnutrition regime, but these changes were idiosyncratic, suggesting a rugged adaptive landscape. Furthermore, although the selected populations evolved both faster growth and higher viability, the maternal effects on growth rate and viability were negatively correlated across populations. Thus, genes mediating maternal effects can evolve to partially counteract the response to selection mediated by the effects of alleles on their own carriers’ phenotype, and maternal effects may contribute to evolutionary trade‐offs between components of offspring fitness.     

The locus of sexual selection: moving sexual selection studies into the post‐genomics era

Sexual selection drives fundamental evolutionary processes such as trait elaboration and speciation. Despite this importance, there are surprisingly few examples of genes unequivocally responsible for variation in sexually selected phenotypes. This lack of information inhibits our ability to predict phenotypic change due to universal behaviours, such as fighting over mates and mate choice. Here, we discuss reasons for this apparent gap and provide recommendations for how it can be overcome by adopting contemporary genomic methods, exploiting underutilized taxa that may be ideal for detecting the effects of sexual selection and adopting appropriate experimental paradigms. Identifying genes that determine variation in sexually selected traits has the potential to improve theoretical models and reveal whether the genetic changes underlying phenotypic novelty utilize common or unique molecular mechanisms. Such a genomic approach to sexual selection will help answer questions in the evolution of sexually selected phenotypes that were first asked by Darwin and can furthermore serve as a model for the application of genomics in all areas of evolutionary biology.     

Evolutionary genetics of sex-limited traits under fluctuating selection

Ultimately based on the different gamete size and the resulting sex roles, most animal species have acquired traits that occur only in one of the sexes. For those sex-limited traits the impact of a single selection event is reduced, because the genes coding for these traits also occur unexpressed in the other sex and are therefore partly hidden to selection. All sex-limited traits thus show a storage effect analogous to a seed bank. This storage effect has to be considered when measuring the effect of fluctuating selection on sex-limited traits. Here, I develop appropriate equations to measure the ability of an allele to invade a population when fluctuating selection acts on sex-limited traits. A comparison of the equations for X-chromosomal and autosomal traits gives the following result: the evolution of traits limited to the heterogametic sex should preferentially involve X-chromosomal genes and the evolution of traits limited to the homogametic sex should preferentially involve autosomal genes. This difference between the sexes may contribute to explain (1) the large effect of X-chromosomal genes in causing hybrid sterility in the heterogametic sex and (2) the large effect of X-chromosomal genes on sexually selected traits in heterogametic males.     

Sex-linked expression of a sexually selected trait in the stalk-eyed fly, Cyrtodiopsis dalmanni

Recent theoretical and empirical work has suggested that the X chromosome may play a special role in the evolution of sexually dimorphic traits. We tested this idea by quantifying sex chromosome influence on male relative eyespan, a dramatically sexually selected trait in the stalk-eyed fly, Cyrtodiopsis dalmanni. After 31 generations of artificial sexual selection on eyespan:body length ratio, we reciprocally crossed high- with low-line flies and found no evidence for maternal effects; the relative eyespan of F1 females from high- and low-line dams did not differ. However, F1 male progeny from high-line dams had longer relative eyespan than male progeny from low-line dams, indicating X-linkage. Comparison of progeny from a backcross involving reciprocal F1 males and control line females confirmed X-linked inheritance and indicated no effect of the Y chromosome on relative eyespan. We estimated that the X chromosome accounts for 25% (SE = 6%) of the change in selected lines, using the average difference between reciprocal F1 males divided by the difference between parental males, or 34%, using estimates of the number of effective factors obtained from reciprocal crosses between a high and low line. These estimates exceed the relative size of the X in the diploid genome of a male, 11.9% (SE = 0.3%), as measured from mitotic chromosome lengths. However, they match expectations if X-linked genes in males exhibit dosage compensation by twofold hyperactivation, as has been observed in other flies. Therefore, sex-linked expression of relative eyespan is likely to be commensurate with the size of the X chromosome in this dramatically dimorphic species.     

A HIGH‐DENSITY SCAN OF THE Z CHROMOSOME IN FICEDULA FLYCATCHERS REVEALS CANDIDATE LOCI FOR DIVERSIFYING SELECTION

Theoretical and empirical data suggest that genes located on sex chromosomes may play an important role both for sexually selected traits and for traits involved in the build‐up of hybrid incompatibilities. We investigated patterns of genetic variation in 73 genes located on the Z chromosomes of two species of the flycatcher genus Ficedula, the pied flycatcher and the collared flycatcher. Sequence data were evaluated for signs of selection potentially related to genomic differentiation in these young sister species, which hybridize despite reduced fitness of hybrids. Seven loci were significantly more divergent between the two species than expected under neutrality and they also displayed reduced nucleotide diversity, consistent with having been influenced by directional selection. Two of the detected candidate regions contain genes that are associated with plumage coloration in birds. Plumage characteristics play an important role in species recognition in these flycatchers suggesting that the detected genes may have been involved in the evolution of sexual isolation between the species.     

Consequences of genetic linkage for the maintenance of sexually antagonistic polymorphism in hermaphrodites

When selection differs between males and females, pleiotropic effects among genes expressed by both sexes can result in sexually antagonistic selection (SA), where beneficial alleles for one sex are deleterious for the other. For hermaphrodites, alleles with opposing fitness effects through each sex function represent analogous genetic constraints on fitness. Recent theory based on single‐locus models predicts that the maintenance of SA genetic variation should be greatly reduced in partially selfing populations. However, selfing also reduces the effective rate of recombination, which should facilitate selection on linked allelic combinations and expand opportunities for balancing selection in a multilocus context. Here, I develop a two‐locus model of SA selection for simultaneous hermaphrodites, and explore the joint influence of linkage, self‐fertilization, and dominance on the maintainance of SA polymorphism. I find that the effective reduction in recombination caused by selfing significantly expands the parameter space where SA polymorphism can be maintained relative to single‐locus models. In particular, linkage facilitates the invasion of male‐beneficial alleles, partially compensating for the “female‐bias” in the net direction of selection created by selfing. I discuss the implications of accounting for linkage among SA loci for the maintenance of SA genetic variation and mixed mating systems in hermaphrodites.     

Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots

To date, few studies have investigated the effects of inbreeding on sexually selected traits, although inbreeding depression on such traits can play an important role in the evolution and ecology of wild populations. Sexually selected traits such as ornamentation and courtship behaviour may not be primary fitness characters, but selection and dominance coefficients of their mutations will resemble those of traits under natural selection. Strong directional selection, for instance, through female mate-choice, purges all but the most recessive deleterious mutations, and the remaining dominance variation will result in inbreeding depression once populations undergo bottlenecks. We analysed the effects of inbreeding on sexually selected traits (colour pattern and courtship behaviour) in the male guppy, Poecilia reticulata, from Trinidad, and found a significant decline in the frequency of mating behaviour and colour spots. Such effects occurred although the genetic basis of these traits, many of which are Y-linked and hemizygous, would be expected to leave relatively little scope for inbreeding depression. Findings suggest that these sexually selected traits could reflect the genetic condition or health of males, and thus may be informative mate-cue characters for female choice as suggested by the 'good genes' model.     

Genetic Architecture of Sexual Selection: QTL Mapping of Male Song and Female Receiver Traits in an Acoustic Moth

Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to non-random mate choice or physical linkage. Such linkage disequilibria can accelerate the evolution of traits and preferences to exaggerated levels. Both theory and recent empirical findings on species recognition suggest that such linkage disequilibria may result from physical linkage or pleiotropy, but very little work has addressed this possibility within the context of sexual selection. We studied the genetic architecture of sexually selected traits by analyzing signals and preferences in an acoustic moth, Achroia grisella, in which males attract females with a train of ultrasound pulses and females prefer loud songs and a fast pulse rhythm. Both male signal characters and female preferences are repeatable and heritable traits. Moreover, female choice is based largely on male song, while males do not appear to provide direct benefits at mating. Thus, some genetic correlation between song and preference traits is expected. We employed a standard crossing design between inbred lines and used AFLP markers to build a linkage map for this species and locate quantitative trait loci (QTL) that influence male song and female preference. Our analyses mostly revealed QTLs of moderate strength that influence various male signal and female receiver traits, but one QTL was found that exerts a major influence on the pulse-pair rate of male song, a critical trait in female attraction. However, we found no evidence of specific co-localization of QTLs influencing male signal and female receiver traits on the same linkage groups. This finding suggests that the sexual selection process would proceed at a modest rate in A. grisella and that evolution toward exaggerated character states may be tempered. We suggest that this equilibrium state may be more the norm than the exception among animal species.     

Maternal effect genes and the evolution of sociality in haplo-diploid organisms

Maternal care and female-biased sex ratios are considered by many to be essential prerequisites for the evolution of eusocial behaviors among the hymenoptera. Using population genetic models, I investigate the evolution of genes that have positive maternal effects but negative, direct effects on offspring fitness. I find that, under many conditions, such genes evolve more easily in haplo-diploids than in diplo-diploids. In fact, the conditions are less restrictive than those of kin selection theory, which postulate genes with negative direct effects but positive sib-social effects. For example, the conditions permitting the evolution of maternal effect genes are not affected if females mate multiply, whereas multiple mating reduces the efficacy of kin selection by reducing genetic relatedness within colonies. Inbreeding also differentially facilitates evolution of maternal effect genes in haplo-diploids relative to diplo-diploids, although it does not differentially affect the evolution of sib-altruism genes. Furthermore, when the direct, deleterious pleiotropic effect is restricted to sons, a maternal effect gene can evolve when the beneficial maternal effect is less than half (with inbreeding, much less) of the deleterious effect on sons. For kin selection, however, the sib-social benefits must always exceed the direct costs because genetic relatedness is always less than or equal to 1.0. The results suggest that haplo-diploidy facilitates (1) the evolution of maternal care, and (2) the evolution of maternal effect genes with antagonistic pleiotropic effects on sons. The latter effect may help explain the tendency toward female-biased sex ratios in haplo-diploids, especially those with inbreeding. I conclude that haplo-diploidy not only facilitates the evolution of sister-sister altruism by kin selection but also facilitates the evolution of maternal care and female-biased sex ratios, two prerequisites for eusociality.     

SEX CHROMOSOME LINKED GENETIC VARIANCE AND THE EVOLUTION OF SEXUAL DIMORPHISM OF QUANTITATIVE TRAITS

Theory predicts that sex chromsome linkage should reduce intersexual genetic correlations thereby allowing the evolution of sexual dimorphism. Empirical evidence for sex linkage has come largely from crosses and few studies have examined how sexual dimorphism and sex linkage are related within outbred populations. Here, we use data on an array of different traits measured on over 10,000 individuals from two pedigreed populations of birds (collared flycatcher and zebra finch) to estimate the amount of sex‐linked genetic variance (h²_z). Of 17 traits examined, eight showed a nonzero h²_Z estimate but only four were significantly different from zero (wing patch size and tarsus length in collared flycatchers, wing length and beak color in zebra finches). We further tested how sexual dimorphism and the mode of selection operating on the trait relate to the proportion of sex‐linked genetic variance. Sexually selected traits did not show higher h²_Z than morphological traits and there was only a weak positive relationship between h²_Z and sexual dimorphism. However, given the relative scarcity of empirical studies, it is premature to make conclusions about the role of sex chromosome linkage in the evolution of sexual dimorphism.     

Sex chromosomes and male ornaments: a comparative evaluation in ray-finned fishes

Theory predicts that the mechanism of genetic sex determination can substantially influence the evolution of sexually selected traits. For example, female heterogamety (ZZ/ZW) can favour the evolution of extreme male traits under Fisher's runaway model of sexual selection. We empirically test whether the genetic system of sex determination has played a role in the evolution of exaggerated male ornaments in actinopterygiian fishes, a clade in which both female-heterogametic and male-heterogametic systems of sex determination have evolved multiple times. Using comparative methods both uncorrected and corrected for phylogenetic non-independence, we detected no significant correlation between sex-chromosome systems and sexually selected traits in males. Results suggest that sex-determination mechanism is at best a relatively minor factor affecting the outcomes of sexual selection in ray-finned fishes.     

The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good- and sexy-sperm?

The good-sperm and sexy-sperm (GS-SS) hypotheses predict that female multiple mating (polyandry) can fuel sexual selection for heritable male traits that promote success in sperm competition. A major prediction generated by these models, therefore, is that polyandry will benefit females indirectly via their sons' enhanced fertilization success. Furthermore, like classic 'good genes' and 'sexy son' models for the evolution of female preferences, GS-SS processes predict a genetic correlation between genes for female mating frequency (analogous to the female preference) and those for traits influencing fertilization success (the sexually selected traits). We examine the premise for these predictions by exploring the genetic basis of traits thought to influence fertilization success and female mating frequency. We also highlight recent debates that stress the possible genetic constraints to evolution of traits influencing fertilization success via GS-SS processes, including sex-linked inheritance, nonadditive effects, interacting parental genotypes, and trade-offs between integrated ejaculate components. Despite these possible constraints, the available data suggest that male traits involved in sperm competition typically exhibit substantial additive genetic variance and rapid evolutionary responses to selection. Nevertheless, the limited data on the genetic variation in female mating frequency implicate strong genetic maternal effects, including X-linkage, which is inconsistent with GS-SS processes. Although the relative paucity of studies on the genetic basis of polyandry does not allow us to draw firm conclusions about the evolutionary origins of this trait, the emerging pattern of sex linkage in genes for polyandry is more consistent with an evolutionary history of antagonistic selection over mating frequency. We advocate further development of GS-SS theory to take account of the complex evolutionary dynamics imposed by sexual conflict over mating frequency.     

X chromosome influences sperm length in the stalk-eyed fly Cyrtodiopsis dalmanni

Whether sexually selected traits are sex linked can have profound effects on their evolution. In the diopsid stalk-eyed fly, Cyrtodiopsis dalmanni, sperm length and female reproductive tract morphology have coevolved across species, postcopulatory sexual selection is known to occur, and X-linked genes affect female ventral sperm receptacle size. Here, we estimate the location of quantitative trait loci (QTL) for spermatocyst tail length by using F2 progeny segregating for an X-linked factor that causes sex-ratio meiotic drive. We found two QTL, including a major X-linked QTL responsible for 25% of the variation in spermatocyst tail length 2.1 cM from the sex-ratio element and 0.8 cM from a major eye span QTL. Sex-ratio males produce shorter spermatocyst tails and shorter eye spans. Thus, X-linked factors affect both pre- and postcopulatory traits, and linkage between the alleles for short eye span and short spermatocyst tail length allow pre- and postcopulatory sexual selection to potentially act in concert against the transmission bias caused by the sex-ratio chromosome.     

VARIATION IN SEED CHARACTERS IN NEMOPHILA MENZIESII: EVIDENCE OF A GENETIC BASIS FOR MATERNAL EFFECT

A growing body of evidence indicates that phenotypic selection on juvenile traits of both plants and animals may be considerable. Because juvenile traits are typically subject to maternal effects and often have low heritabilities, adaptive responses to natural selection on these traits may seem unlikely. To determine the potential for evolutionary response to selection on juvenile traits of Nemophila menziesii (Hydrophyllaceae), we conducted two quantitative genetic studies. A reciprocal factorial cross, involving 16 parents and 1960 progeny, demonstrated a significant maternal component of variance in seed mass and additive genetic component of variance in germination time. This experiment also suggested that interaction between parents, though small, provides highly significant contributions to the variance of both traits. Such a parental interaction could arise by diverse mechanisms, including dependence of nuclear gene expression on cytoplasmic genotype, but the design of this experiment could not distinguish this from other possible causes, such as effects on progeny phenotype of interaction between the environmental conditions of both parents. The second experiment, spanning three generations with over 11,000 observations, was designed for investigation of the additive genetic variance in maternal effect, assessment of paternal effects, as well as further partitioning of the parental interaction identified in the reciprocal factorial experiment. It yielded no consistent evidence of paternal effects on seed mass, nor of parental interactions. Our inference of such interaction effects from the first experiment was evidently an artifact of failing to account for the substantial variance among fruits within crosses. The maternal effect was found to have a large additive genetic component, accounting for at least 20% of the variation in individual seed mass. This result suggests that there is appreciable potential for response to selection on seed mass through evolution of the maternal effect. We discuss aspects that may nevertheless limit response to individual selection on seed mass, including trade-offs between the size of individual seeds and germination time and between the number of seeds a maternal plant can mature and their mean size.     

SEX LINKAGE,SEX‐SPECIFIC SELECTION,AND THE ROLE OF RECOMBINATION IN THE EVOLUTION OF SEXUALLY DIMORPHIC GENE EXPRESSION

Sex‐biased genes—genes that are differentially expressed within males and females—are nonrandomly distributed across animal genomes, with sex chromosomes and autosomes often carrying markedly different concentrations of male‐ and female‐biased genes. These linkage patterns are often gene‐ and lineage‐dependent, differing between functional genetic categories and between species. Although sex‐specific selection is often hypothesized to shape the evolution of sex‐linked and autosomal gene content, population genetics theory has yet to account for many of the gene‐ and lineage‐specific idiosyncrasies emerging from the empirical literature. With the goal of improving the connection between evolutionary theory and a rapidly growing body of genome‐wide empirical studies, we extend previous population genetics theory of sex‐specific selection by developing and analyzing a biologically informed model that incorporates sex linkage, pleiotropy, recombination, and epistasis, factors that are likely to vary between genes and between species. Our results demonstrate that sex‐specific selection and sex‐specific recombination rates can generate, and are compatible with, the gene‐ and species‐specific linkage patterns reported in the genomics literature. The theory suggests that sexual selection may strongly influence the architectures of animal genomes, as well as the chromosomal distribution of fixed substitutions underlying sexually dimorphic traits.     

Genetic architecture of ovary size and asymmetry in European honeybee workers

The molecular basis of complex traits is increasingly understood but a remaining challenge is to identify their co-regulation and inter-dependence. Pollen hoarding (pln) in honeybees is a complex trait associated with a well-characterized suite of linked behavioral and physiological traits. In European honeybee stocks bidirectionally selected for pln, worker (sterile helper) ovary size is pleiotropically affected by quantitative trait loci that were initially identified for their effect on foraging behavior. To gain a better understanding of the genetic architecture of worker ovary size in this model system, we analyzed a series of crosses between the selected strains. The crossing results were heterogeneous and suggested non-additive effects. Three significant and three suggestive quantitative trait loci of relatively large effect sizes were found in two reciprocal backcrosses. These loci are not located in genome regions of known effects on foraging behavior but contain several interesting candidate genes that may specifically affect worker-ovary size. Thus, the genetic architecture of this life history syndrome may be comprised of pleiotropic, central regulators that influence several linked traits and other genetic factors that may be downstream and trait specific.     

Genomic evidence for a large-Z effect

The 'large-X effect' suggests that sex chromosomes play a disproportionate role in adaptive evolution. Theoretical work indicates that this effect may be most pronounced in genetic systems with female heterogamety under both good-genes and Fisher's runaway models of sexual selection (males ZZ, females ZW). Here, I use a comparative genomic approach (alignments of several thousands of chicken-zebra finch-human-mouse-opossum orthologues) to show that avian Z-linked genes are highly overrepresented among those bird-mammalian orthologues that show evidence of accelerated rate of functional evolution in birds relative to mammals; the data suggest a twofold excess of such genes on the Z chromosome. A reciprocal analysis of genes accelerated in mammals found no evidence for an excess of X-linkage. This would be compatible with theoretical expectations for differential selection on sex-linked genes under male and female heterogamety, although the power in this case was not sufficient to statistically show that 'large-Z' was more pronounced than 'large-X'. Accelerated Z-linked genes include a variety of functional categories and are characterized by higher non-synonymous to synonymous substitution rate ratios than both accelerated autosomal and non-accelerated genes. This points at a genomic 'large-Z effect', which is widespread and of general significance for adaptive divergence in birds.