Generation of a neutral FST baseline for testing local adaptation on gill raker number within and between European whitefish ecotypes in the Baltic Sea basin

Divergent selection at ecologically important traits is thought to be a major factor driving phenotypic differentiation between populations. To elucidate the role of different evolutionary processes shaping the variation in gill raker number of European whitefish (Coregonus lavaretus sensu lato) in the Baltic Sea basin, we assessed the relationships between genetic and phenotypic variation among and within three whitefish ecotypes (sea spawners, river spawners and lake spawners). To generate expected neutral distribution of F_ST and to evaluate whether highly variable microsatellite loci resulted in deflated F_ST estimates compared to less variable markers, we performed population genetic simulations under finite island and hierarchical island models. The genetic divergence observed among (F_CT = 0.010) and within (F_ST = 0.014–0.041) ecotypes was rather low. The divergence in gill raker number, however, was substantially higher between sea and river spawners compared to observed microsatellite data and simulated neutral baseline (P_CT > F_CT). This suggests that the differences in gill raker number between sea and river spawners are likely driven by divergent natural selection. We also found strong support for divergent selection on gill raker number among different populations of sea spawners (P_ST > F_ST), most likely caused by highly variable habitat use and diverse diet. The putative role of divergent selection within lake spawners initially inferred from empirical microsatellite data was not supported by simulated F_ST distributions. This work provides a first formal test of divergent selection on gill raker number in Baltic whitefish, and demonstrates the usefulness of population genetic simulations to generate informative neutral baselines for P_ST–F_ST analyses helping to disentangle the effects of stochastic evolutionary processes from natural selection.     

Genetic and Morphological Divergence in Three Strains of Brook Trout Salvelinus fontinalis Commonly Stocked in Lake Superior

Fitness related traits often show spatial variation across populations of widely distributed species. Comparisons of genetic variation among populations in putatively neutral DNA markers and in phenotypic traits susceptible to selection (Q_ST F_ST analysis) can be used to determine to what degree differentiation among populations can be attributed to selection or genetic drift. Traditionally, Q_ST F_ST analyses require a large number of populations to achieve sufficient statistical power; however, new methods have been developed that allow Q_ST F_ST comparisons to be conducted on as few as two populations if their pedigrees are informative. This study compared genetic and morphological divergence in three strains of brook trout Salvelinus fontinalis that were historically or currently used for stocking in the Lake Superior Basin. Herein we examined if morphological divergence among populations showed temporal variation, and if divergence could be attributed to selection or was indistinguishable from genetic drift. Multivariate Q_ST F_ST analysis showed evidence for divergent selection between populations. Univariate analyses suggests that the pattern observed in the multivariate analyses was largely driven by divergent selection for length and weight, and moreover by divergence between the Assinica strain and each of the Iron River and Siskiwit strains rather than divergent selection between each population pair. While it could not be determined if divergence was due to natural selection or inadvertent artificial selection in hatcheries, selected differences were consistent with patterns of domestication commonly found in salmonids.     

Post‐glacial colonization routes coincide with a life‐history breakpoint along a latitudinal gradient

Although adaptive divergence along environmental gradients has repeatedly been demonstrated, the role of post‐glacial colonization routes in determining phenotypic variation along gradients has received little attention. Here, we used a hierarchical Q_ST–F_ST approach to separate the roles of adaptive and neutral processes in shaping phenotypic variation in moor frog (Rana arvalis) larval life histories along a 1,700 km latitudinal gradient across northern Europe. This species has colonized Scandinavia via two routes with a contact zone in northern Sweden. By using neutral SNP and common garden phenotypic data from 13 populations at two temperatures, we showed that most of the variation along the gradient occurred between the two colonizing lineages. We found little phenotypic divergence within the lineages; however, all phenotypic traits were strongly diverged between the southern and northern colonization routes, with higher growth and development rates and larger body size in the north. The Q_ST estimates between the colonization routes were four times higher than F_ST, indicating a prominent role for natural selection. Q_ST within the colonization routes did not generally differ from F_ST, but we found temperature‐dependent adaptive divergence close to the contact zone. These results indicate that lineage‐specific variation can account for much of the adaptive divergence along a latitudinal gradient.     

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.     

Adaptive differentiation in floral traits in the presence of high gene flow in scarlet gilia (Ipomopsis aggregata)

Plant–pollinator interactions are thought to be major drivers of floral trait diversity. However, the relative importance of divergent pollinator‐mediated selection vs. neutral processes in floral character evolution has rarely been explored. We tested for adaptive floral trait evolution by comparing differentiation at neutral genetic loci to differentiation at quantitative floral traits in a putative Ipomopsis aggregata hybrid zone. Typical I. aggregata subsp. candida displays slender white tubular flowers that are typical of flowers pollinated by hawkmoths, and subsp. collina displays robust red tubular flowers typical of flowers pollinated by hummingbirds; yet, hybrid flower morphs are abundant across the East Slope of the Colorado Rockies. We estimated genetic differentiation (F_ST) for nuclear and chloroplast microsatellite loci and used a half‐sib design to calculate quantitative trait divergence (Q_ST) from collection sites across the morphological hybrid zone. We found little evidence for population structure and estimated mean F_ST to be 0.032. Q_ST values for several floral traits including corolla tube length and width, colour, and nectar volume were large and significantly greater than mean F_ST. We performed multivariate comparisons of neutral loci to genetic correlations within and between populations and found a strong signal for divergent selection, suggesting that specific combinations of floral display and reward traits may be the targets of selection. Our results show little support for historical subspecies categories, yet floral traits are more diverged than expected due to drift alone. Non‐neutral divergence for multivariate quantitative traits suggests that selection by pollinators is maintaining a correlation between display and reward traits.     

Ecological genetics of range size variation in Boechera spp. (Brassicaceae)

Many taxonomic groups contain both rare and widespread species, which indicates that range size can evolve quickly. Many studies have compared molecular genetic diversity, plasticity, or phenotypic traits between rare and widespread species; however, a suite of genetic attributes that unites rare species remains elusive. Here, using two rare and two widespread Boechera (Brassicaceae) species, we conduct a simultaneous comparison of quantitative trait diversity, genetic diversity, and population structure among species with highly divergent range sizes. Consistent with previous studies, we do not find strong associations between range size and within‐population genetic diversity. In contrast, we find that both the degree of phenotypic plasticity and quantitative trait structure (Q_ST) were positively correlated with range size. We also found higher F_ST: Q_ST ratios in rare species, indicative of either a greater response to stabilizing selection or a lack of additive genetic variation. While widespread species occupy more ecological and climactic space and have diverged at both traits and markers, rare species display constrained levels of population differentiation and phenotypic plasticity. Combined, our results provide evidence for a specialization–generalization trade‐off across three orders of magnitude of range size variation in the ecological model genus, Boechera.     

Molecular and quantitative trait variation within and among small fragmented populations of the endangered plant species Psilopeganum sinense

Background and Aims

Natural selection and genetic drift are important evolutionary forces in determining genetic and phenotypic differentiation in plant populations. The extent to which these two distinct evolutionary forces affect locally adaptive quantitative traits has been well studied in common plant and animal species. However, we know less about how quantitative traits respond to selection pressures and drift in endangered species that have small population sizes and fragmented distributions. To address this question, this study assessed the relative strengths of selection and genetic drift in shaping population differentiation of phenotypic traits in Psilopeganum sinense, a naturally rare and recently endangered plant species.

Methods

Population differentiation at five quantitative traits (Q_ST) obtained from a common garden experiment was compared with differentiation at putatively neutral microsatellite markers (F_ST) in seven populations of P. sinense. Q_ST estimates were derived using a Bayesian hierarchical variance component method.

Key Results

Trait-specific Q_ST values were equal to or lower than F_ST. Neutral genetic diversity was not correlated with quantitative genetic variation within the populations of P. sinense.

Conclusions

Despite the prevalent empirical evidence for Q_ST > F_ST, the results instead suggest a definitive role of stabilizing selection and drift leading to phenotypic differentiation among small populations. Three traits exhibited a significantly lower Q_ST relative to F_ST, suggesting that populations of P. sinense might have experienced stabilizing selection for the same optimal phenotypes despite large geographical distances between populations and habitat fragmentation. For the other two traits, Q_ST estimates were of the same magnitude as F_ST, indicating that divergence in these traits could have been achieved by genetic drift alone. The lack of correlation between molecular marker and quantitative genetic variation suggests that sophisticated considerations are required for the inference of conservation measures of P. sinense from neutral genetic markers.     

Size differentiation in Finnish house sparrows follows Bergmann's rule with evidence of local adaptation

Bergmann's rule predicts that individuals are larger in more poleward populations and that this size gradient has an adaptive basis. Hence, phenotypic divergence in size traits between populations (P_ST) is expected to exceed the level of divergence by drift alone (F_ST). We measured 16 skeletal traits, body mass and wing length in 409 male and 296 female house sparrows Passer domesticus sampled in 12 populations throughout Finland, where the species has its northernmost European distributional margin. Morphometric differentiation across populations (P_ST) was compared with differentiation in 13 microsatellites (F_ST). We find that twelve traits phenotypically diverged more than F_ST in both sexes, and an additional two traits diverged in males. The phenotypic divergence exceeded F_ST in several traits to such a degree that findings were robust also to strong between‐population environmental effects. Divergence was particularly strong in dimensions of the bill, making it a strong candidate for the study of adaptive molecular genetic divergence. Divergent traits increased in size in more northern populations. We conclude that house sparrows show evidence of an adaptive latitudinal size gradient consistent with Bergmann's rule on the modest spatial scale of ca. 600 km.     

Phenotypic divergence of the common toad (Bufo bufo) along an altitudinal gradient: evidence for local adaptation

Variation in the environment can induce different patterns of genetic and phenotypic differentiation among populations. Both neutral processes and selection can influence phenotypic differentiation. Altitudinal phenotypic variation is of particular interest in disentangling the interplay between neutral processes and selection in the dynamics of local adaptation processes but remains little explored. We conducted a common garden experiment to study the phenotypic divergence in larval life-history traits among nine populations of the common toad (Bufo bufo) along an altitudinal gradient in France. We further used correlation among population pairwise estimates of quantitative trait (Q_ST) and neutral genetic divergence (F_ST from neutral microsatellite markers), as well as altitudinal difference, to estimate the relative role of divergent selection and neutral genetic processes in phenotypic divergence. We provided evidence for a neutral genetic differentiation resulting from both isolation by distance and difference in altitude. We found evidence for phenotypic divergence along the altitudinal gradient (faster development, lower growth rate and smaller metamorphic size). The correlation between pairwise Q_STs–F_STs and altitude differences suggested that this phenotypic differentiation was most likely driven by altitude-mediated selection rather than by neutral genetic processes. Moreover, we found different divergence patterns for larval traits, suggesting that different selective agents may act on these traits and/or selection on one trait may constrain the evolution on another through genetic correlation. Our study highlighted the need to design more integrative studies on the common toad to unravel the underlying processes of phenotypic divergence and its selective agents in the context of environmental clines.     

Contrasting patterns of morphological and neutral genetic divergence among geographically proximate populations of sockeye salmon Oncorhynchus nerka in Lake Aleknagik,Alaska

Levels of differentiation in morphological traits (age at maturity, body length at age, egg mass and body depth) and spawning time were examined in sockeye salmon Oncorhynchus nerka from three geographically proximate but physically distinct creeks in Lake Aleknagik, Alaska. Happy Creek fish had significantly greater values for most measured morphological traits, and Eagle Creek fish spawned significantly later than fish in the other creeks. Phenotypic differentiation between creeks, measured as P_ST, was then compared with microsatellite marker differentiation between creeks, measured as F_ST. No correlations were apparent between P_ST and F_ST values, and P_ST values were generally significantly larger than zero (P_ST= 0·0018–0·31) whereas F_ST values were not (F_ST=?0·0004 to 0·0016). The insignificant pair‐wise F_ST values between creek samples indicated that gene flow occurs between creeks, assuming the creek populations have reached migration–drift equilibrium. However, the strong homing behaviour of sockeye salmon precludes a scenario in which fish from the three creeks constitute a single population that segregates by body size. Rather, significant phenotypic differentiation suggests that strong divergent selection occurs on the phenotypic traits despite the homogenizing effects of gene flow.     

Are QST–FST comparisons for natural populations meaningful?

Comparisons between putatively neutral genetic differentiation amongst populations, F_ST, and quantitative genetic variation, Q_ST, are increasingly being used to test for natural selection. However, we find that approximately half of the comparisons that use only data from wild populations confound phenotypic and genetic variation. We urge the use of a clear distinction between narrow‐sense Q_ST, which can be meaningfully compared with F_ST, and phenotypic divergence measured between populations, P_ST, which is inadequate for comparisons in the wild. We also point out that an unbiased estimate of Q_ST can be found using the so‐called ‘animal model’ of quantitative genetics.     

Divergence at neutral and non-neutral loci in Drosophila buzzatii populations and their hybrids

The impact of intraspecific hybridisation on fitness and morphological traits depends on the history of natural selection and genetic drift, which may have led to differently coadapted gene-complexes in the parental populations. The divergence at neutral and non-neutral loci between populations can be evaluated by estimating F_ST and Q_ST respectively, and hence give an estimate of drift and selection in the populations. Here we investigate (1) whether divergence between populations in quantitative traits (wing size and shape) can be attributed to selection or drift alone, (2) The impact of intraspecific hybridisation on estimators for divergence at neutral (F_ST) and non-neutral loci (Q_ST) in hybrids, (3) If measurement of shape is more informative than size in order to detect divergence in quantitative traits between populations. The aims were addressed by performing two hybridisations between three populations of Drosophila buzzatii, one between populations from Argentina and the Canary Islands (separated for 200 years), and the other between populations from Argentina and Australia (separated for 80 years). We observed the highest divergence at neutral loci between the Argentinean and Canary Island populations, but highest morphological divergence between the Argentinean and Australian populations, indicating that natural selection is acting on the wings. Divergence based on Q_ST measures in the hybrids was sensitive towards increased phenotypic variance (σ²p) within groups and should be used with care when σ²p of populations differ. Our results indicate that measures of shape give a better estimate of divergence at the underlying quantitative traits loci than measures of size.     

The joint effects of selection and dominance on the QST - FST contrast

Q_ST measures the differentiation of quantitative traits between populations. It is often compared to F_ST, which measures population differentiation at neutral marker loci due to drift, migration, and mutation. When Q_ST is different from F_ST, it is usually taken as evidence that selection has either restrained or accelerated the differentiation of the quantitative trait relative to neutral markers. However, a number of other factors such as inbreeding, dominance, and epistasis may also affect the Q_ST − F_ST contrast. In this study, we examine the effects of dominance, selection, and inbreeding on Q_ST − F_ST. We compare Q_ST with F_ST at selected and neutral loci for populations at equilibrium between selection, drift, mutation, and migration using both analytic and simulation approaches. Interestingly, when divergent selection is acting on a locus, inbreeding and dominance generally inflate Q_ST relative to F_ST when they are both measured at the quantitative locus at equilibrium. As a consequence, dominance is unlikely to hide the signature of divergent selection on the Q_ST − F_ST contrast. However, although in theory dominance and inbreeding affect the expectation for Q_ST − F_ST, of most concern is the very large variance in both Q_ST and F_ST, suggesting that we should be cautious in attributing small differences between Q_ST and F_ST to selection.     

Population genetic structure and a possible role for selection in driving phenotypic divergence in a rainbowfish (Melanotaeniidae)

Quantitative genetic divergence may be driven by drift or selection. The rainbowfish Melanotaenia australis exhibits phenotypic divergence among populations in Western Australia, although the mechanisms driving this divergence are unknown. We used microsatellites to assess neutral genetic divergence (F_ST), and found a hierarchical pattern of subdivision consistent with low divergence between upstream and downstream populations (within drainages), moderate divergence between drainages (within regions), and high divergence between regions. Using a common‐garden approach, we measured quantitative genetic divergence in phenotypic traits (Q_ST). By comparing this to expectations from neutral processes (F_ST), we concluded that the effect of selection varies depending on the spatial scale considered. Within drainages, selection may be causing divergence between upstream and downstream phenotypes but, between regions, selection appears to homogenize phenotypes. This highlights the importance of spatial scale in studies of this kind, and suggests that, because variance in selection pressures can drive speciation, polymorphism in M. australis may represent speciation in action. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 144–160.     

Remarkable life history polymorphism may be evolving under divergent selection in the silverleaf sunflower

Substantial intraspecific variation in life history is rare and potentially a signal of incipient ecological speciation, if variation is driven by geographically heterogenous natural selection. We present the first report of extensive life history polymorphism in Helianthus argophyllus, the silverleaf sunflower, and examine evidence for its evolution by divergent selection. In 18 populations sampled from across the species range and grown in a common garden, most quantitative traits covaried such that individuals could be assigned to two distinct life history syndromes: tall and late flowering with small initial flowerheads, or short and early flowering with larger initial flowerheads. Helianthus argophyllus exhibits regional genetic structure, but this population structure does not closely correspond with patterns of phenotypic variation. The early‐flowering syndrome is primarily observed in populations from coastal barrier islands, while populations from the nearby mainland coast, although geographically and genetically close, are primarily late flowering. Additionally, several traits are more differentiated among regions than expected based on neutral genetic divergence (Q_ST > F_ST), including the first principal component score corresponding with life history syndrome. This discordance between patterns of phenotypic and genetic variation suggests that divergent selection is driving genetic differences in life history across the species range. If so, the silverleaf sunflower may be in early stages of ecological speciation.     

Low levels of quantitative and molecular genetic differentiation among natural populations of Medicago ciliaris Kroch. (Fabaceae) of different Tunisian eco-geographical origin

In this paper, we analyze the genetic variability in four Tunisian natural populations of Medicago ciliaris using 19 quantitative traits and six polymorphic microsatellite loci. We investigated the amplification transferability of 30 microsatellites developed in the model legume M. truncatula to M. ciliaris. Results revealed that about 56.66% of analyzed markers are valuable genetic markers for M. ciliaris. The most genetic diversity at quantitative traits and microsatellite loci was found to occur within populations (>80%). Low differentiations among populations at quantitative traits Q _ST  = 0.146 and molecular markers F _ST  = 0.18 were found. The majority of measured traits exhibited no significant difference in the level of Q _ST and F _ST . Furthermore, significant correlations established between these traits and eco-geographical factors suggested that natural selection should be invoked to explain the level of phenotypic divergence among populations rather than drift. There was no significant correlation between population differentiation at quantitative traits and molecular markers. Significant spatial genetic structure consistent with models of isolation by distance was detected within all studied populations. The site-of-origin environmental factors explain about 9.07% of total phenotypic genetic variation among populations. The eco-geographical factors that influence more the variation of measured traits among populations are the soil texture and altitude. Nevertheless, there were no consistent pattern of associations between gene diversity (He) and environmental factors.     

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.     

Comparison of genetic differentiation at marker loci and quantitative traits

The comparison of the degree of differentiation in neutral marker loci and genes coding quantitative traits with standardized and equivalent measures of genetic differentiation (F_ST and Q_ST, respectively) can provide insights into two important but seldom explored questions in evolutionary genetics: (i) what is the relative importance of random genetic drift and directional natural selection as causes of population differentiation in quantitative traits, and (ii) does the degree of divergence in neutral marker loci predict the degree of divergence in genes coding quantitative traits? Examination of data from 18 independent studies of plants and animals using both standard statistical and meta‐analytical methods revealed a number of interesting points. First, the degree of differentiation in quantitative traits (Q_ST) typically exceeds that observed in neutral marker genes (F_ST), suggesting a prominent role for natural selection in accounting for patterns of quantitative trait differentiation among contemporary populations. Second, the F_ST – Q_ST difference is more pronounced for allozyme markers and morphological traits, than for other kinds of molecular markers and life‐history traits. Third, very few studies reveal situations were Q_ST < F_ST, suggesting that selection pressures, and hence optimal phenotypes, in different populations of the same species are unlikely to be often similar. Fourth, there is a strong correlation between Q_ST and F_ST indices across the different studies for allozyme (r=0.81), microsatellite (r=0.87) and combined (r=0.75) marker data, suggesting that the degree of genetic differentiation in neutral marker loci is closely predictive of the degree of differentiation in loci coding quantitative traits. However, these interpretations are subject to a number of assumptions about the data and methods used to derive the estimates of population differentiation in the two sets of traits.     

Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides

The impacts of drought are expanding worldwide as a consequence of climate change. However, there is still little knowledge of how species respond to long‐term selection in seasonally dry ecosystems. In this study, we used Q_ST‐F_ST comparisons to investigate (i) the role of natural selection on population genetic differentiation for a set of functional traits related to drought resistance in the seasonally dry tropical oak Quercus oleoides and (ii) the influence of water availability at the site of population origin and in experimental treatments on patterns of trait divergence. We conducted a thorough phenotypic characterization of 1912 seedlings from ten populations growing in field and greenhouse common gardens under replicated watering treatments. We also genotyped 218 individuals from the same set of populations using eleven nuclear microsatellites. Q_ST distributions for leaf lamina area, specific leaf area, leaf thickness and stomatal pore index were higher than F_ST distribution. Results were consistent across growth environments. Genetic differentiation among populations for these functional traits was associated with the index of moisture at the origin of the populations. Together, our results suggest that drought is an important selective agent for Q. oleoides and that differences in length and severity of the dry season have driven the evolution of genetic differences in functional traits.     

Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish

Divergent selection acting on several different traits that cause multidimensional shifts are supposed to promote speciation, but the outcome of this process is highly dependent on the balance between the strength of selection vs. gene flow. Here, we studied a pair of sister species of Lake Victoria cichlids at a location where they hybridize and tested the hypothesis that divergent selection acting on several traits can maintain phenotypic differentiation despite gene flow. To explore the possible role of selection we tested for correlations between phenotypes and environment and compared phenotypic divergence (P_ST) with that based on neutral markers (F_ST). We found indications for disruptive selection acting on male breeding colour and divergent selection acting on several morphological traits. By performing common garden experiments we also separated the environmental and heritable components of divergence and found evidence for phenotypic plasticity in some morphological traits contributing to species differences.