Drift,selection and adaptive variation in small populations of a threatened rattlesnake

An important goal of conservation genetics is to determine if the viability of small populations is reduced by a loss of adaptive variation due to genetic drift. Here, we assessed the impact of drift and selection on direct measures of adaptive variation (toxin loci encoding venom proteins) in the eastern massasauga rattlesnake (Sistrurus catenatus), a threatened reptile that exists in small isolated populations. We estimated levels of individual polymorphism in 46 toxin loci and 1,467 control loci across 12 populations of this species, and compared the results with patterns of selection on the same loci following speciation of S. catenatus and its closest relative, the western massasauga (S. tergeminus). Multiple lines of evidence suggest that both drift and selection have had observable impacts on standing adaptive variation. In support of drift effects, we found little evidence for selection on toxin variation within populations and a significant positive relationship between current levels of adaptive variation and long‐ and short‐term estimates of effective population size. However, we also observed levels of directional selection on toxin loci among populations that are broadly similar to patterns predicted from interspecific selection analyses that pre‐date the effects of recent drift, and that functional variation in these loci persists despite small short‐term effective sizes. This suggests that much of the adaptive variation present in populations may represent an example of “drift debt,” a nonequilibrium state where present‐day levels of variation overestimate the amount of functional genetic diversity present in future populations.     

GENETIC ARCHITECTURE AND POSTZYGOTIC REPRODUCTIVE ISOLATION: EVOLUTION OF BATESON–DOBZHANSKY–MULLER INCOMPATIBILITIES IN A POLYGENIC MODEL

The Bateson–Dobzhansky–Muller model predicts that postzygotic isolation evolves due to the accumulation of incompatible epistatic interactions, but few studies have quantified the relationship between genetic architecture and patterns of reproductive divergence. We examined how the direction and magnitude of epistatic interactions in a polygenic trait under stabilizing selection influenced the evolution of hybrid incompatibilities. We found that populations evolving independently under stabilizing selection experienced suites of compensatory allelic changes that resulted in genetic divergence between populations despite the maintenance of a stable, high‐fitness phenotype. A small number of loci were then incompatible with multiple alleles in the genetic background of the hybrid and the identity of these incompatibility loci changed over the evolution of the populations. For F₁ hybrids, reduced fitness evolved in a window of intermediate strengths of epistatic interactions, but F₂ and backcross hybrids evolved reduced fitness across weak and moderate strengths of epistasis due to segregation variance. Strong epistatic interactions constrained the allelic divergence of parental populations and prevented the development of reproductive isolation. Because many traits with varying genetic architectures must be under stabilizing selection, our results indicate that polygenetic drift is a plausible hypothesis for the evolution of postzygotic reproductive isolation.     

Elucidation of the genetic differences in Trialeurodes vaporariorum populations under vegetable greenhouse conditions by using the allozyme approach

Genetic differentiation of Trialeurodes vaporariorum (Westwood 1856) populations was examined using biochemical and allozyme analysis. For biochemical analysis, general esterase and glutathion‐S‐transferase were tested. Allozyme genetic variability in 11 populations of T. vaporariorum was investigated using five loci from four enzyme systems. Although there are large variations between populations, T. vaporariorum is grouped into two populations with geographic barriers, based on Nei's genetic distance in the Baekdudaegan Mountains. Within these two groups, low migration and linkage disequilibrium reveal that populations tend to be influenced by gene drift rather than uniform selection pressures. The effect of genetic drift is greater than the effect of uniform selection by insecticides or host plant resistance, which is suggested by the F_ST estimates in this study. Based on this basic research, more effective whitefly control programs could be built in the future.     

The effect of non-additive genetic interactions on selection in multi-locus genetic models

Additive genetic variance might usually be expected to decrease in a finite population because of genetic drift. However, both theoretical and empirical studies have shown that the additive genetic variance of a population could, in some cases, actually increase owing to the action of genetic drift in presence of non-additive effects. We used Monte-Carlo simulations to address a less-well-studied issue: the effects of directional truncation selection on a trait affected by non-additive genetic variation. We investigated the effects on genetic variance and the response to selection. We compared two different genetic models, representing various numbers of loci. We found that the additive genetic variance could also increase in the case of truncation selection, when dominance and epistasis was present. Additive-by-additive epistatic effects generally gave a higher increase in additive variance compared to dominance. However, the magnitude of the increase differed depending on the particular model and on the number of loci.     

Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction‐site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small N_e (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome‐wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high F_ST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high F_ST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small N_e in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.     

Microsatellite and major histocompatibility complex variation in an endangered rattlesnake,the Eastern Massasauga (Sistrurus catenatus)

Genetic diversity is fundamental to maintaining the long‐term viability of populations, yet reduced genetic variation is often associated with small, isolated populations. To examine the relationship between demography and genetic variation, variation at hypervariable loci (e.g., microsatellite DNA loci) is often measured. However, these loci are selectively neutral (or near neutral) and may not accurately reflect genomewide variation. Variation at functional trait loci, such as the major histocompatibility complex (MHC), can provide a better assessment of adaptive genetic variation in fragmented populations. We compared patterns of microsatellite and MHC variation across three Eastern Massasauga (Sistrurus catenatus) populations representing a gradient of demographic histories to assess the relative roles of natural selection and genetic drift. Using 454 deep amplicon sequencing, we identified 24 putatively functional MHC IIB exon 2 alleles belonging to a minimum of six loci. Analysis of synonymous and nonsynonymous substitution rates provided evidence of historical positive selection at the nucleotide level, and Tajima's D provided support for balancing selection in each population. As predicted, estimates of microsatellite allelic richness, observed, heterozygosity, and expected heterozygosity varied among populations in a pattern qualitatively consistent with demographic history and abundance. While MHC allelic richness at the population and individual levels revealed similar trends, MHC nucleotide diversity was unexpectedly high in the smallest population. Overall, these results suggest that genetic variation in the Eastern Massasauga populations in Illinois has been shaped by multiple evolutionary mechanisms. Thus, conservation efforts should consider both neutral and functional genetic variation when managing captive and wild Eastern Massasauga populations.     

Characterizing the evolution of genetic variance using genetic covariance tensors

Determining how genetic variance changes under selection in natural populations has proved to be a very resilient problem in evolutionary genetics. In the same way that understanding the availability of genetic variance within populations requires the simultaneous consideration of genetic variance in sets of functionally related traits, determining how genetic variance changes under selection in natural populations will require ascertaining how genetic variance–covariance (G) matrices evolve. Here, we develop a geometric framework using higher-order tensors, which enables the empirical characterization of how G matrices have diverged among populations. We then show how divergence among populations in genetic covariance structure can then be associated with divergence in selection acting on those traits using key equations from evolutionary theory. Using estimates of G matrices of eight male sexually selected traits from nine geographical populations of Drosophila serrata, we show that much of the divergence in genetic variance occurred in a single trait combination, a conclusion that could not have been reached by examining variation among the individual elements of the nine G matrices. Divergence in G was primarily in the direction of the major axes of genetic variance within populations, suggesting that genetic drift may be a major cause of divergence in genetic variance among these populations.     

Does natural selection alter genetic architecture? An evaluation of quantitative genetic variation among populations of Allonemobiussocius and A. fasciatus

To make long-term predictions using present quantitative genetic theory it is necessary to assume that the genetic variance–covariance matrix ( G ) remains constant or at least changes by a constant fraction. In this paper we examine the stability of the genetic architecture of two traits known to be subject to natural selection; femur length and ovipositor length in two species of the cricket Allonemobius. Previous studies have shown that in A. fasciatus and A. socius natural selection favours an increased body size southwards but a decreased ovipositor length. Such countergradient selection should tend to favour a change in G . In the total sample of eight populations of A. socius and one of A. fasciatus we show that there is significant variation in all genetic covariance components, i.e. V_A for body size, V_A for ovipositor length, and Cov_A. This variation results entirely from an increase in the covariances of A. fasciatus. However, although larger, these components are approximately proportionally increased, thereby leading to no statistically significant change in the genetic correlation. A proportional increase in the covariance components is consistent with changes resulting from genetic drift. On the other hand, the genetic covariance components are significantly correlated with the length of the growing season suggesting that the change in the genetic architecture is the result of selection and drift.     

The evolutionary consequences of habitat fragmentation: Body morphology and coloration differentiation among brook trout populations of varying size

A reduction in population size due to habitat fragmentation can alter the relative roles of different evolutionary mechanisms in phenotypic trait differentiation. While deterministic (selection) and stochastic (genetic drift) mechanisms are expected to affect trait evolution, genetic drift may be more important than selection in small populations. We examined relationships between mature adult traits and ecological (abiotic and biotic) variables among 14 populations of brook trout. These naturally fragmented populations have shared ancestry but currently exhibit considerable variability in habitat characteristics and population size (49 < N_c < 10,032; 3 < N_b < 567). Body size, shape, and coloration differed among populations, with a tendency for more variation among small populations in both trait means and CV when compared to large populations. Phenotypic differences were more frequently and directly linked to habitat variation or operational sex ratio than to population size, suggesting that selection may overcome genetic drift at small population size. Phenotype–environment associations were also stronger in females than males, suggesting that natural selection due to abiotic conditions may act more strongly on females than males. Our results suggest that natural and sexual‐selective pressures on phenotypic traits change during the process of habitat fragmentation, and that these changes are largely contingent upon existing habitat conditions within isolated fragments. Our study provides an improved understanding of the ecological and evolutionary consequences of habitat fragmentation and lends insight into the ability of some small populations to respond to selection and environmental change.     

Spatially and temporally varying selection on intrapopulation quantitative trait loci for a life history trade-off in Mimulus guttatus

Why do populations remain genetically variable despite strong continuous natural selection? Mutation reconstitutes variation eliminated by selection and genetic drift, but theoretical and experimental studies each suggest that mutation‐selection balance insufficient to explain extant genetic variation in most complex traits. The alternative hypothesis of balancing selection, wherein selection maintains genetic variation, is an aggregate of multiple mechanisms (spatial and temporal heterogeneity in selection, frequency‐dependent selection, antagonistic pleiotropy, etc.). Most of these mechanisms have been demonstrated for Mendelian traits, but there is little comparable data for loci affecting quantitative characters. Here, we report a 3‐year field study of selection on intrapopulation quantitative trait loci (QTL) of flower size, a highly polygenic trait in Mimulus guttatus. The QTL exhibit antagonistic pleiotropy: alleles that increase flower size, reduce viability, but increase fecundity. The magnitude and direction of selection fluctuates yearly and on a spatial scale of metres. This study provides direct evidence of balancing selection mechanisms on QTL of an ecologically relevant trait.     

The Action of Purifying Selection,Mutation and Drift on Fitness Epistatic Systems

For different fitness mutational models, with epistasis introduced, we simulated the consequences of drift (D scenario) or mutation, selection, and drift (MSD scenario) in populations at the MSD balance subsequently subjected to bottlenecks of size N = 2, 10, 50 during 100 generations. No “conversion” of nonadditive into additive variance was observed, all components of the fitness genetic variance initially increasing with the inbreeding coefficient F and subsequently decreasing to zero (D) or to an equilibrium value (MSD). In the D scenario, epistasis had no appreciable effect on inbreeding depression and that on the temporal change of variance components was relevant only for high rates of strong epistatic mutation. In parallel, between-line differentiation in mean fitness accelerated with F and that in additive variance reached a maximum at F ∼ 0.6–0.7, both processes being intensified by strong epistasis. In the MSD scenario, however, the increase in additive variance was smaller, as it was used by selection to purge inbreeding depression (N ≥ 10), and selection prevented between-line differentiation. Epistasis, either synergistic or antagonistic (this leading to multiple adaptive peaks), had no appreciable effect on MSD results nor, therefore, on the evolutionary rate of fitness change.THE roles of genetic drift and natural selection in shaping the genetic variation of fitness due to segregation at epistatic loci have often been discussed since Wright''s (1931) pioneering treatment of the subject. In general, the pertinent analyses have been usually elaborated within an analytical framework where changes in the mean and the components of the genetic variance exclusively due to drift were first considered, this being followed by an examination of the conditions that may subsequently allow for a more rapid selection response and/or facilitate the movement of populations to new adaptive peaks.Theoretically, it is well known that the contribution of neutral additive loci to the additive genetic variance of metric traits in populations decreases linearly as the inbreeding coefficient F increases, until it ultimately vanishes when fixation is attained (Wright 1951). For neutral nonadditive loci, however, that contribution may initially increase until a critical F value is reached and then subsequently decline to zero. This is the case of simple dominant loci (Robertson 1952; Willis and Orr 1993), and it also applies to two-locus models showing either additive × additive epistasis (Cockerham and Tachida 1988; Goodnight 1988) or more complex epistasis involving dominance at the single-locus level (Cheverud and Routman 1996; López-Fanjul et al. 1999, 2000; Goodnight 2000). Furthermore, those models have been extended to cover multiple additive × additive epistatic systems (Barton and Turelli 2004, López-Fanjul et al. 2006).In parallel, laboratory experiments have also studied the impact of population bottlenecks on the additive variance of metric traits (see reviews by López-Fanjul et al. 2003 and Van Buskirk and Willi 2006). For morphological traits not strongly correlated with fitness, a decrease in their additive variance together with little or no inbreeding depression was often observed, both results being compatible with the corresponding additive expectations and suggesting that the standing variation of those traits is mainly controlled by quasi-neutral additive alleles. Using typical estimates of mutational parameters, Zhang et al. (2004) showed that these experimental results can be explained by assuming a model of pleiotropic and real stabilizing selection acting on the pertinent trait. On the other hand, life-history traits closely connected to fitness usually show strong inbreeding depression and a dramatic increase in additive variance after a brief period of inbreeding or bottlenecking, indicating that much of that variance should be due to deleterious recessive alleles segregating at low frequencies. However, it should be kept in mind that experimental results cannot discern between simple dominance and dominance with additional epistasis as causes of inbreeding-induced changes in the additive variance.In their discussion of the shifting-balance theory (Wright 1931), Wade and Goodnight emphasized the evolutionary importance of the “conversion” of epistatic variance into additive variance, proposing that drift-induced excesses in the additive variance for fitness available to selection could enhance the potential for local adaptation, a phenomenon that was not discussed in the original formulation of Wright''s theory (Wade and Goodnight 1998; Goodnight and Wade 2000; but see Coyne et al. 1997, 2000). However, the additive variance is inflated only under restrictive conditions that often involve low-frequency deleterious recessive alleles (Robertson 1952; López-Fanjul et al. 2002), so that a drift-induced excess in the additive variance of fitness will be associated with inbreeding depression and, therefore, it is unlikely to produce a net increase in the adaptive potential of populations. In addition, previous considerations were based on the theoretical analysis of the behavior of neutral genetic variation after bottlenecks, and the role of selection acting on epistatic systems controlling fitness has not been studied.In this article we used analytical and simulation methods to investigate the contribution of epistatic systems to the change in the mean and the genetic components of variance of fitness during bottlenecking, due to the joint action of mutation, natural selection, and genetic drift (MSD). To develop a biologically reasonable model, we assumed that mutations show a distribution of homozygous and heterozygous effects close to those experimentally observed in Drosophila melanogaster, and we imposed different types of epistasis on this basic system. The pattern and strength of epistatic effects on fitness is largely unknown, but synergism between homozygous deleterious mutations at different loci has often been reported in Drosophila mutation-accumulation experiments (Mukai 1969; Ávila et al. 2006). Therefore, we studied the consequences of synergistic epistasis in pairs of loci by increasing the deleterious effect of the double homozygote above that expected from the deleterious effects of the homozygotes at both loci involved. However, to explore the consequences of bottlenecking in a multiple-peak adaptive surface, we also considered cases of antagonistic epistasis where, at each pair of loci, the fitness of the double homozygote for the deleterious alleles was larger than expected. Of course, other epistatic models could also be considered, including those showing higher-order interaction effects, but the severe shortage of relevant empirical data makes the choice highly subjective and, consequently, we restricted our analysis to the simplest case. On the other hand, our procedure has the practical advantage of allowing the definition of epistasis by the addition of a single parameter to those describing the properties of individual loci.Our aim was to describe and analyze drift-induced changes in the components of the genetic variance of fitness, where neutral predictions will be reliable only during extreme and brief bottlenecks. For moderate bottleneck sizes or long-term inbreeding, it becomes necessary to consider the concurrent effects of natural selection both on the standing variation and on that arisen by new mutation. Moreover, the nature of the genetic variability of fitness in the base population, arisen by mutation and shaped by natural selection and drift, is critical for the assessment of the consequences of subsequent bottlenecks. For nonepistatic models, the genetic properties of the trait can be theoretically inferred from the pertinent mutational parameters and effective population sizes by assuming a balance between mutation, selection, and drift. This can be numerically achieved using diffusion theory, and reliable approximations can be easily calculated by analytical methods (García-Dorado 2007). Notwithstanding, the analytical study of the contribution of epistasis to the genetic properties of fitness at the MSD balance becomes particularly difficult and it must be complemented with computer simulation.     

Incomplete loss of a conserved trait: function,latitudinal cline,and genetic constraints

Retention of nonfunctional traits over evolutionary time is puzzling, because the cost of trait production should drive loss. Indeed, several studies have found nonfunctional traits are rapidly eliminated by selection. However, theory suggests that complex genetic interactions and a lack of genetic variance can constrain evolution, including trait loss. In the mustard family Brassicaceae the conserved floral condition includes four long and two short stamens, but we show that short stamens in the highly self‐pollinating mustard Arabidopsis thaliana do not significantly increase selfed seed set, suggesting that the trait has lost most or all of its function after the transition to selfing. We find that short stamen loss is common in native populations. Loss is incomplete and decreases with increasing latitude, a cline unexplained by correlations with flowering time or ovule count (which also vary with latitude). Using recombinant inbred lines derived from a cross between plants at the latitudinal extremes of the native range, we found three QTLs affecting short stamen number, with epistasis among them constraining stamen loss. Constraints on stamen loss from both epistasis and low genetic variance may be augmented by high selfing rates, suggesting that these kinds of constraints may be common in inbred species.     

Selection on life‐history traits and genetic population divergence in rotifers

A combination of founder effects and local adaptation – the Monopolization hypothesis – has been proposed to reconcile the strong population differentiation of zooplankton dwelling in ponds and lakes and their high dispersal abilities. The role genetic drift plays in genetic differentiation of zooplankton is well documented, but the impact of natural selection has received less attention. Here, we compare differentiation in neutral genetic markers (F_ST) and in quantitative traits (Q_ST) in six natural populations of the rotifer Brachionus plicatilis to assess the importance of natural selection in explaining genetic differentiation of life‐history traits. Five life‐history traits were measured in four temperature × salinity combinations in common‐garden experiments. Population differentiation for neutral genetic markers – 11 microsatellite loci – was very high (F_ST = 0.482). Differentiation in life‐history traits was higher in traits related to sexual reproduction than in those related to asexual reproduction. Q_ST values for diapausing egg production (a trait related to sexual reproduction) were higher than their corresponding F_ST in some pairs of populations. Our results indicate the importance of divergent natural selection in these populations and suggest local adaptation to the unpredictability of B. plicatilis habitats.     

THE OPPORTUNITY FOR BALANCING SELECTION IN EXPERIMENTAL POPULATIONS OF CAENORHABDITIS ELEGANS

The role of balancing selection in maintaining diversity during the evolution of sexual populations to novel environments is poorly understood. To address this issue, we studied the impact of two mating systems, androdioecy and dioecy, on genotype distributions during the experimental evolution of Caenorhabditis elegans. We analyzed the temporal trajectories of 334 single nucleotide polymorphisms, covering 1/3 of the genome, and found extensive allele frequency changes and little loss of heterozygosities after 100 generations. As modeled with numerical simulations, SNP differentiation was consistent with genetic drift and average fitness effects of 2%, assuming that selection acted independently at each locus. Remarkably, inbreeding by self‐fertilization was of little consequence to SNP differentiation. Modeling selection on deleterious recessive alleles suggests that the initial evolutionary dynamics can be explained by associative overdominance, but not the later stages because much lower heterozygosities would be maintained during experimental evolution. By contrast, models with selection on true overdominant loci can explain the heterozygote excess observed at all periods, particularly when negative epistasis or independent fitness effects were considered. Overall, these findings indicate that selection at single loci, including purging of recessive alleles, underlies most of the genetic differentiation accomplished during the experiment. Nonetheless, they also imply that maintenance of genetic diversity may in large part be due to balancing selection at multiple loci.     

Maintaining evolvability

Although molecular methods, such as QTL mapping, have revealed a number of loci with large effects, it is still likely that the bulk of quantitative variability is due to multiple factors, each with small effect. Typically, these have a large additive component. Conventional wisdom argues that selection, natural or artificial, uses up additive variance and thus depletes its supply. Over time, the variance should be reduced, and at equilibrium be near zero. This is especially expected for fitness and traits highly correlated with it. Yet, populations typically have a great deal of additive variance, and do not seem to run out of genetic variability even after many generations of directional selection. Long-term selection experiments show that populations continue to retain seemingly undiminished additive variance despite large changes in the mean value. I propose that there are several reasons for this. (i) The environment is continually changing so that what was formerly most fit no longer is. (ii) There is an input of genetic variance from mutation, and sometimes from migration. (iii) As intermediate-frequency alleles increase in frequency towards one, producing less variance (as p → 1, p(1 − p) → 0), others that were originally near zero become more common and increase the variance. Thus, a roughly constant variance is maintained. (iv) There is always selection for fitness and for characters closely related to it. To the extent that the trait is heritable, later generations inherit a disproportionate number of genes acting additively on the trait, thus increasing genetic variance. For these reasons a selected population retains its ability to evolve. Of course, genes with large effect are also important. Conspicuous examples are the small number of loci that changed teosinte to maize, and major phylogenetic changes in the animal kingdom. The relative importance of these along with duplications, chromosome rearrangements, horizontal transmission and polyploidy is yet to be determined. It is likely that only a case-by-case analysis will provide the answers. Despite the difficulties that complex interactions cause for evolution in Mendelian populations, such populations nevertheless evolve very well. Longlasting species must have evolved mechanisms for coping with such problems. Since such difficulties do not arise in asexual populations, a comparison of epistatic patterns in closely related sexual and asexual species might provide some important insights.     

Variation in aggressiveness components of Zymoseptoria tritici populations in Iran

Zymoseptoria tritici, the causal agent of Septoria tritici blotch, has emerged and evolved as a pathogen on wheat in the Fertile Crescent. Iran is located in this region, and study on the ancient pathogen populations in the country can improve our understanding on adaptive potential of aggressiveness, the role of local adaptation in shaping population structure and the involvement of selection and genetic drift in favouring aggressiveness adaptation to environments. To this aim, three aggressiveness components including days until first lesion (DUFL), days until first pycnidia (DUFP) and percentage of leaf area covered by pycnidia, in five populations of the pathogen collected from different provinces of Iran were compared in greenhouse conditions. All populations except for Golestan showed high within‐population diversity for the examined traits. No difference in aggressiveness components was found between fungal collections from Khuzestan and Fars; however, significant variation was evident among the populations originated from other provinces. Comparisons of estimated Q_ST values to F_ST indicated that genetic differentiation in pycnidial coverage has been the result of selection imposed by different variables; however, the divergence found for DUFL and DUFP has been achieved by genetic drift. The possible mechanisms involved in aggressiveness diversity of the pathogen populations and the impact of these findings on breeding programs for quantitative resistance are discussed.     

The change in quantitative genetic variation with inbreeding

Inbreeding is known to reduce heterozygosity of neutral genetic markers, but its impact on quantitative genetic variation is debated. Theory predicts a linear decline in additive genetic variance (V(A)) with increasing inbreeding coefficient (F) when loci underlying the trait act additively, but a nonlinear hump-shaped relationship when dominance and epistasis are important. Predictions for heritability (h2) are similar, although the exact shape depends on the value of h2 in the absence of inbreeding. We located 22 published studies in which the level of genetic variation in experimentally inbred populations (measured by V(A) or h2) was compared with that in outbred control populations. For life-history traits, the data strongly supported a nonlinear change in genetic variation with increasing F. V(A) and h2 were, respectively, 244% and 50% higher at F = 0.4 than in outbred populations, and dominance plus epistatic variance together exceeded additive variance by a factor of four. For nonfitness traits the decline was linear and estimates of nonadditive variance were small. These results confirm that population bottlenecks frequently increase V(A) in some traits, and imply that life-history traits are underlain by substantial dominance or epistasis. However, the importance of drift-induced genetic variation in conservation or evolutionary biology is questionable, in part because inbreeding depression usually accompanies inbreeding.     

Integration of Random Forest with population‐based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha)

Anadromous Chinook salmon populations vary in the period of river entry at the initiation of adult freshwater migration, facilitating optimal arrival at natal spawning. Run timing is a polygenic trait that shows evidence of rapid parallel evolution in some lineages, signifying a key role for this phenotype in the ecological divergence between populations. Studying the genetic basis of local adaptation in quantitative traits is often impractical in wild populations. Therefore, we used a novel approach, Random Forest, to detect markers linked to run timing across 14 populations from contrasting environments in the Columbia River and Puget Sound, USA. The approach permits detection of loci of small effect on the phenotype. Divergence between populations at these loci was then examined using both principle component analysis and F_ST outlier analyses, to determine whether shared genetic changes resulted in similar phenotypes across different lineages. Sequencing of 9107 RAD markers in 414 individuals identified 33 predictor loci explaining 79.2% of trait variance. Discriminant analysis of principal components of the predictors revealed both shared and unique evolutionary pathways in the trait across different lineages, characterized by minor allele frequency changes. However, genome mapping of predictor loci also identified positional overlap with two genomic outlier regions, consistent with selection on loci of large effect. Therefore, the results suggest selective sweeps on few loci and minor changes in loci that were detected by this study. Use of a polygenic framework has provided initial insight into how divergence in a trait has occurred in the wild.     

The effects of selection,drift and genetic variation on life‐history trait divergence among insular populations of natterjack toad,Bufo calamita

Although loss of genetic variation is frequently assumed to be associated with loss of adaptive potential, only few studies have examined adaptation in populations with little genetic variation. On the Swedish west coast, the northern fringe populations of the natterjack toad Bufo calamita inhabit an atypical habitat consisting of offshore rock islands. There are strong among‐population differences in the amount of neutral genetic variation, making this system suitable for studies on mechanisms of trait divergence along a gradient of within‐population genetic variation. In this study, we examined the mechanisms of population divergence using Q_ST–F_ST comparisons and correlations between quantitative and neutral genetic variation. Our results suggest drift or weak stabilizing selection across the six populations included in this study, as indicated by low Q_ST–F_ST values, lack of significant population × temperature interactions and lack of significant differences among the islands in breeding pond size. The six populations included in this study differed in both neutral and quantitative genetic variation. Also, the correlations between neutral and quantitative genetic variation tended to be positive, however, the relatively small number of populations prevents any strong conclusions based on these correlations. Contrary to the majority of Q_ST–F_ST comparisons, our results suggest drift or weak stabilizing selection across the examined populations. Furthermore, the low heritability of fitness‐related traits may limit evolutionary responses in some of the populations.     

Epistatic partners of neurogenic genes modulate Drosophila olfactory behavior

The extent to which epistasis affects the genetic architecture of complex traits is difficult to quantify, and identifying variants in natural populations with epistatic interactions is challenging. Previous studies in Drosophila implicated extensive epistasis between variants in genes that affect neural connectivity and contribute to natural variation in olfactory response to benzaldehyde. In this study, we implemented a powerful screen to quantify the extent of epistasis as well as identify candidate interacting variants using 203 inbred wild‐derived lines with sequenced genomes of the Drosophila melanogaster Genetic Reference Panel (DGRP). We crossed the DGRP lines to P[GT1]‐element insertion mutants in Sema‐5c and neuralized (neur), two neurodevelopmental loci which affect olfactory behavior, and to their coisogenic wild‐type control. We observed significant variation in olfactory responses to benzaldehyde among F₁ genotypes and for the DGRP line by mutant genotype interactions for both loci, showing extensive nonadditive genetic variation. We performed genome‐wide association analyses to identify the candidate modifier loci. None of these polymorphisms were in or near the focal genes; therefore, epistasis is the cause of the nonadditive genetic variance. Candidate genes could be placed in interaction networks. Several candidate modifiers are associated with neural development. Analyses of mutants of candidate epistatic partners with neur (merry‐go‐round (mgr), prospero (pros), CG10098, Alhambra (Alh) and CG12535) and Sema‐5c (CG42540 and bruchpilot (brp)) showed aberrant olfactory responses compared with coisogenic controls. Thus, integrating genome‐wide analyses of natural variants with mutations at defined genomic locations in a common coisogenic background can unmask specific epistatic modifiers of behavioral phenotypes.