Determinants of Genetic Structure in a Nonequilibrium Metapopulation of the Plant Silene latifolia

Population genetic differentiation will be influenced by the demographic history of populations, opportunities for migration among neighboring demes and founder effects associated with repeated extinction and recolonization. In natural populations, these factors are expected to interact with each other and their magnitudes will vary depending on the spatial distribution and age structure of local demes. Although each of these effects has been individually identified as important in structuring genetic variance, their relative magnitude is seldom estimated in nature. We conducted a population genetic analysis in a metapopulation of the angiosperm, Silene latifolia, from which we had more than 20 years of data on the spatial distribution, demographic history, and extinction and colonization of demes. We used hierarchical Bayesian methods to disentangle which features of the populations contributed to among population variation in allele frequencies, including the magnitude and direction of their effects. We show that population age, long-term size and degree of connectivity all combine to affect the distribution of genetic variance; small, recently-founded, isolated populations contributed most to increase F _ST in the metapopulation. However, the effects of population size and population age are best understood as being modulated through the effects of connectivity to other extant populations, i.e. F _ST diminishes as populations age, but at a rate that depends how isolated the population is. These spatial and temporal correlates of population structure give insight into how migration, founder effect and within-deme genetic drift have combined to enhance and restrict genetic divergence in a natural metapopulation.     

THE INFLUENCE OF DISPERSAL PATTERNS AND MATING SYSTEM ON GENETIC DIFFERENTIATION WITHIN AND BETWEEN POPULATIONS OF THE RED HOWLER MONKEY (ALOUATTA SENICULUS)

The relationship between social structure and partitioning of genetic variance was examined in two red howler monkey populations (W and G) in Venezuela, one of which (G) was undergoing rapid growth through colonization by new troops. Rates and patterns of gene flow had been determined through radiotelemetry and direct observation data on solitary migrants, and 10 years of troop censusing. Standard electrophoresis techniques were used to examine 29 loci in blood samples taken from 137 of the study animals. Analysis of genetic variance demonstrated: (1) a significantly high level of genetic variation among troops within populations (F_ST = 0.225 for W and 0.142 for G), and (2) a significant excess of heterozygosity within troops relative to expected (F_IS = -0.136 for W and -0.064 for G), despite relatively high levels of observed and inferred inbreeding in W. Differences between the populations in F_ST values conformed to those predicted based on differences in colonization rate. Comparison of partitioning of genetic variance among different genealogical subsets of troops demonstrated that the pattern of genetic differentiation observed among troops within populations was promoted by an essentially single-male harem breeding structure, a very low rate of random exchange of breeding males among troops, and a high degree of relatedness among troop females. Between-troop genetic differentiation (F_ST) was thereby increased relative to that expected from other types of social organization, while the correlation between uniting gametes within troops (F_IS) was decreased. Genetic differentiation between populations (2%) corresponded to that predicted from migration rates. Such a mosaic of genetic variation, combined with differences in reproductive success observed among troops and a high troop failure rate, create conditions in which interdemic selection could result in more rapid spread of advantageous gene combinations than would be expected in a panmictic population, particularly in a colonizing situation in which the founder population is small.     

A clever solution to a vexing problem

F_ST (as well as related measures such as G_ST) has long been used both as a measure of the relative amount of genetic variation between populations and as an indicator of the amount of gene flow among populations. Unfortunately, F_ST and its clones are also sensitive to mutation, particularly when the mutation rate per locus is greater than the migration rate among populations. Relatively high mutation rates cause estimates of F_ST and G_ST to be much lower than researchers sometimes expect, when migration rates are low in the studied species. Several recent suggestions for dealing with this problem have been unsatisfactory for one reason or another, and no general solution exists (if we are not to abandon these otherwise useful measures of differentiation). In an important article in this issue, Jinliang Wang (2015) shows that it is possible to identify whether the genetic markers in a given study are likely to give estimates of F_ST that are strongly affected by mutation. The proposed test is simple and elegant, and with it, molecular ecologists can determine whether the F_ST from their makers can be depended on for further inference about their species’ genome and the demographic forces which shaped its patterns.     

PHASE III OF WRIGHT'S SHIFTING BALANCE PROCESS AND THE VARIANCE AMONG DEMES IN MIGRATION RATE

Interdemic selection by the differential migration of individuals out from demes of high fitness and into demes of low fitness (Phase III) is one of the most controversial aspects of Wright's Shifting Balance Theory. I derive a relationship between Phase III migration and the interdemic selection differential, S, and show its potential effect on F_ST. The relationship reveals a diversifying effect of interdemic selection by Phase III migration on the genetic structure of a metapopulation. Using experimental metapopulations, I explored the effect of Phase III migration on F_ST by comparing the genetic variance among demes for two different patterns of migration: (1) island model migration and (2) Wright's Phase III migration. Although mean migration rates were the same, I found that the variance among demes in migration rate was significantly higher with Phase III than with island model migration. As a result, F_ST for the frequency of a neutral marker locus was higher with Phase III than it was with island model migration. By increasing F_ST, Phase III enhanced the genetic differentiation among demes for traits not subject to interdemic selection. This feature makes Wright's process different from individual selection which, by reducing effective population size, decreases the genetic variance within demes for all other traits. I discussed this finding in relation to the efficacy of Phase III and random migration for effecting peak shifts, and the contribution of genes with indirect effects to among‐deme variation.     

Genetic structure of Brandt’s vole (<Emphasis Type="Italic">Lasiopodomys brandtii</Emphasis>) populations in Inner Mongolia,China, based on microsatellite analysis

Brandt’s vole (Lasiopodomys brandtii) distribution is discontinuous in Inner Mongolia with some populations isolated from others. Recently, some isolated populations have suffered extinction, and the factors responsible remain elusive. Genetic drift is one of the processes affecting population genetic differentiation, and can play a substantial role in the divergence of small, isolated populations. Using seven microsatellite markers, we genotyped four geographically isolated populations of Brandt’s vole, all of which exhibit episodic fluctuations in population density. The results showed a strong genetic differentiation among the geographically distinct populations (total F _ST = 0.124) and in particular, one population (Zhengxiangbaiqi) was isolated from all others (F _ST values were greatest between Zhengxiangbaiqi and other populations). Furthermore, high levels of inbreeding (F _IS values ranged from 0.205 to 0.290) within each distinct population suggest that inbreeding has and is likely occurring in Brandt’s vole populations. These processes can decrease average individual fitness and consequently increase the risk of extinction of the species.     

Population Structure of the Giant Garter Snake, Thamnophis gigas

The giant garter snake, Thamnophis gigas, is a threatened species endemic to California’s Central Valley. We tested the hypothesis that current watershed boundaries have caused genetic differentiation among populations of T. gigas. We sampled 14 populations throughout the current geographic range of T. gigas and amplified 859 bp from the mitochondrial gene ND4 and one nuclear microsatellite locus. DNA sequence variation from the mitochondrial gene indicates there is some genetic structuring of the populations, with high F_ST values and unique haplotypes occurring at high frequency in several populations. We found that clustering populations by watershed boundary results in significant between-region genetic variance for mtDNA. However, analysis of allele frequencies at the microsatellite locus NSU3 reveals very low F_ST values and little between-region variation in allele frequencies. The discordance found between mitochondrial and microsatellite data may be explained by aspects of molecular evolution and/or T. gigas life history characteristics. Differences in effective population size between mitochondrial and nuclear DNA, or male-biased gene flow, result in a lower migration rate of mitochondrial haplotypes relative to nuclear alleles. However, we cannot exclude homoplasy as one explanation for homogeneity found for the single microsatellite locus. The mitochondrial nucleotide sequence data supports conservation practices that identify separate management units for T. gigas.     

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.     

Retrotransposon‐based genetic diversity of Deschampsia antarctica Desv. from King George Island (Maritime Antarctic)

Deschampsia antarctica Desv. can be found in diverse Antarctic habitats which may vary considerably in terms of environmental conditions and soil properties. As a result, the species is characterized by wide ecotypic variation in terms of both morphological and anatomical traits. The species is a unique example of an organism that can successfully colonize inhospitable regions due to its phenomenal ability to adapt to both the local mosaic of microhabitats and to general climatic fluctuations. For this reason, D. antarctica has been widely investigated in studies analyzing morphophysiological and biochemical responses to various abiotic stresses (frost, drought, salinity, increased UV radiation). However, there is little evidence to indicate whether the observed polymorphism is accompanied by the corresponding genetic variation. In the present study, retrotransposon‐based iPBS markers were used to trace the genetic variation of D. antarctica collected in nine sites of the Arctowski oasis on King George Island (Western Antarctic). The genotyping of 165 individuals from nine populations with seven iPBS primers revealed 125 amplification products, 15 of which (12%) were polymorphic, with an average of 5.6% polymorphic fragments per population. Only one of the polymorphic fragments, observed in population 6, was represented as a private band. The analyzed specimens were characterized by low genetic diversity (uH_e = 0.021, I = 0.030) and high population differentiation (F_ST = 0.4874). An analysis of Fu's F_S statistics and mismatch distribution in most populations (excluding population 2, 6 and 9) revealed demographic/spatial expansion, whereas significant traces of reduction in effective population size were found in three populations (1, 3 and 5). The iPBS markers revealed genetic polymorphism of D. antarctica, which could be attributed to the mobilization of random transposable elements, unique features of reproductive biology, and/or geographic location of the examined populations.     

Empirical Distributions of F ST from Large-Scale Human Polymorphism Data

Studies of the apportionment of human genetic variation have long established that most human variation is within population groups and that the additional variation between population groups is small but greatest when comparing different continental populations. These studies often used Wright’s F _ST that apportions the standardized variance in allele frequencies within and between population groups. Because local adaptations increase population differentiation, high-F _ST may be found at closely linked loci under selection and used to identify genes undergoing directional or heterotic selection. We re-examined these processes using HapMap data. We analyzed 3 million SNPs on 602 samples from eight worldwide populations and a consensus subset of 1 million SNPs found in all populations. We identified four major features of the data: First, a hierarchically F _ST analysis showed that only a paucity (12%) of the total genetic variation is distributed between continental populations and even a lesser genetic variation (1%) is found between intra-continental populations. Second, the global F _ST distribution closely follows an exponential distribution. Third, although the overall F _ST distribution is similarly shaped (inverse J), F _ST distributions varies markedly by allele frequency when divided into non-overlapping groups by allele frequency range. Because the mean allele frequency is a crude indicator of allele age, these distributions mark the time-dependent change in genetic differentiation. Finally, the change in mean-F _ST of these groups is linear in allele frequency. These results suggest that investigating the extremes of the F _ST distribution for each allele frequency group is more efficient for detecting selection. Consequently, we demonstrate that such extreme SNPs are more clustered along the chromosomes than expected from linkage disequilibrium for each allele frequency group. These genomic regions are therefore likely candidates for natural selection.     

Demographic factors and genetic variation influence population persistence under environmental change

Population persistence has been studied in a conservation context to predict the fate of small or declining populations. Persistence models have explored effects on extinction of random demographic and environmental fluctuations, but in the face of directional environmental change they should also integrate factors affecting whether a population can adapt. Here, we examine the population‐size dependence of demographic and genetic factors and their likely contributions to extinction time under scenarios of environmental change. Parameter estimates were derived from experimental populations of the rainforest species, Drosophila birchii, held in the lab for 10 generations at census sizes of 20, 100 and 1000, and later exposed to five generations of heat‐knockdown selection. Under a model of directional change in the thermal environment, rapid extinction of populations of size 20 was caused by a combination of low growth rate (r) and high stochasticity in r. Populations of 100 had significantly higher reproductive output, lower stochasticity in r and more additive genetic variance (V_A) than populations of 20, but they were predicted to persist less well than the largest size class. Even populations of 1000 persisted only a few hundred generations under realistic estimates of environmental change because of low V_A for heat‐knockdown resistance. The experimental results document population‐size dependence of demographic and adaptability factors. The simulations illustrate a threshold influence of demographic factors on population persistence, while genetic variance has a more elastic impact on persistence under environmental change.     

GENETIC STRUCTURE OF NATURAL POPULATIONS IN THE RED ALGAE GELIDIUM CANARIENSE (GELIDIALES,RHODOPHYTA) INVESTIGATED BY RANDOM AMPLIFIED POLYMORPHIC DNA (RAPD) MARKERS1

Random amplified polymorphic DNA (RAPD) marker variation was analyzed in female gametophytes in natural populations of Gelidium canariense (Grunow) Seoane‐Camba ex Haroun, Gil‐Rodríguez, Diaz de Castro et Prud'Homme van Reine from the Canary Islands to estimate the degree and distribution of genetic variability and differentiation. A total of 190 haploid individuals were analyzed with 60 polymorphic RAPDs bands which produced 190 distinct multilocus genotypes. A high level of polymorphism was detected in all populations analyzed. Within‐population gene diversity ranged from 0.156 to 0.264. The populations on the island of Gran Canaria showed higher genetic variation than the other populations analyzed. The partitioning of molecular variance by analysis of molecular variance showed that most genetic variation resides within populations (68.85%). These results suggest that sexual reproduction is the predominant mode of reproduction for G. canariense gametophytic populations, and the main determinant in reaching high levels of genetic diversity. The Neighbor‐Joining tree and FCA analysis displayed two subclusters that correspond to the populations from the western islands (Tenerife, La Palma, Gomera) and the eastern island (Gran Canaria). In addition, we have detected a significant relationship between F_ST/(1?F_ST) and geographical distance consistent with data on water circulation and age of islands. The results obtained agree with an isolation by distance model, with gene flow from eastern to the western islands, and a high level of genetic differentiation between populations (F_ST=0.311, P<0.001).     

Moderately and Highly Polymorphic Microsatellites Provide Discordant Estimates of Population Divergence in Sockeye Salmon, Oncorhynchus nerka

Mutation rate can vary widely among microsatellite loci. This variation may cause discordant single-locus and multi-locus estimates of F_ST, the commonly used measure of population divergence. We use 16 microsatellite and five allozyme loci from 14 sockeye salmon populations to address two questions about the affect of mutation rate on estimates of F_ST: (1) does mutation rate influence F_ST estimates from all microsatellites to a similar degree relative to allozymes?; (2) does the influence of mutation rate on F_ST estimates from microsatellites vary with geographic scale in spatially structured populations? For question one we find that discordant estimates of F_ST among microsatellites as well as between the two marker classes are correlated with mean within-population heterozygosity (H_S) and thus are likely due to differences in mutation rate. Highly polymorphic microsatellites (H_S > 0.84) provide significantly lower estimates of F_ST than moderately polymorphic microsatellites and allozymes (H_S < 0.60). Estimates of F_ST from binned allele frequency data and R_ST provide more accurate measures of population divergence for highly polymorphic but not for moderately polymorphic microsatellites. We conclude it is more important to pool loci of like H_S rather than marker class when estimating F_ST. For question two we find the F_ST values for moderately and highly polymorphic loci, while significantly different, are positively correlated for geographically proximate but not geographically distant population pairs. These results are consistent with expectations from the equilibrium approximation of Wright's infinite island model and confirm that the influence of mutation on estimates of F_ST can vary in spatially structured populations presumably because the rate of migration varies inversely with geographic scale.     

GENETIC DIFFERENTIATION AMONG CHEWING LOUSE POPULATIONS (MALLOPHAGA: TRICHODECTIDAE) IN A POCKET GOPHER CONTACT ZONE (RODENTIA: GEOMYIDAE)

Genetic variation among populations of chewing lice (Geomydoecus actuosi) was examined in relation to chromosomal and electrophoretic variation among populations of their hosts (Thomomys bottae) at a contact zone. Louse demes were characterized by low levels of genetic heterozygosity (H? = 0.039) that may result from founder effects during primary infestation of hosts, compounded by seasonal reductions in louse population size. Louse populations sampled from different hosts showed high levels of genetic structuring both within and among host localities. Microgeographic differentiation of louse populations is high (mean F_ST = 0.092) suggesting that properties of this host–parasite system promote differentiation of louse populations living on different individual hosts. Among-population differentiation in lice (F_ST = 0.240) was similar to that measured among host populations (F_ST = 0.236), suggesting a close association between gene flow in pocket gophers and gene flow in their lice.     

Genetic diversity and population structure in Elephantopus scaber (Asteraceae) from South China as revealed by ISSR markers

Abstract

We used inter-simple sequence repeat (ISSR) markers to investigate genetic variation in eight natural populations of Elephantopus scaber from South China, including Guangdong, Hainan and Hong Kong. Eleven primers produced 247 bands across all 184 individuals, of which 243 (98.4%) were polymorphic. The average genetic diversity at the species and population levels was estimated to be 0.283 and 0.103, respectively, using mean expected heterozygosity. The average gene differentiation (F _ST) among populations was 0.725. AMOVA analysis showed that the partition of molecular variation between and within populations was 72.5% and 27.5%, respectively. The effective number of migrants among populations based on the F _ST was relatively low (N _m = 0.095). Cluster analysis based on Nei's genetic distance and the neighbour-joining method revealed the genetic relationships among the populations of E. scaber. The Mantel test indicated that there was no significant correlation between population genetic and geographic distances. The results obtained from the AMOVA analysis, the cluster analysis, and the Mantel test all suggested that fragmented local environments and human disturbance might play important roles in shaping the population structure of E. scaber.     

Genetic diversity and population differentiation in the yellow drum Nibea albiflora along the coast of the China Sea

Nibea albiflora (yellow drum) is an important seafood fish species in East Asia. We explored the population genetic variation of N. albiflora along the coastal waters of the China Sea using microsatellite markers to facilitate a selective breeding programme that is undertaken in China. A total of 256 alleles were detected at 12 loci in four wild populations. A high level of genetic diversity was observed with the mean number of alleles and the observed and expected heterozygosity in each population ranging from 7.917 to 14.083, 0.701 to 0.764 and 0.765 to 0.841, respectively. Pairwise fixation index (F_ST) analysis indicated significant but weak genetic differentiation among populations from four localities (F_ST?=?0.030, P?<?0.01), which was also confirmed by analysis of molecular variance (AMOVA). Significant genetic differentiation was detected between Ningde and the other populations (F_ST?=?0.047–0.056, P?<?0.01). Structure analysis suggested that N. albiflora within the examined range might be composed of two stocks. The data of the present study revealed high genetic diversity and low genetic differentiation among the N. albiflora populations along the coast of the China Sea. This baseline information could be valuable for future selective breeding programmes of N. albiflora.     

Comparative population structure of Chinese sumac aphid <Emphasis Type="Italic">Schlechtendalia chinensis</Emphasis> and its primary host-plant <Emphasis Type="Italic">Rhus chinensis</Emphasis>

Most of our current understanding of comparative population structure has been come from studies of parasite–host systems, whereas the genetic comparison of gallnut-aphids and their host-plants remain poorly documented. Here, we examined the population genetic structure of the Chinese sumac aphid Schlechtendalia chinensis and its unique primary host-plant Rhus chinensis in a mountainous province in western China using inter-simple sequence repeat (ISSR) markers. Despite being sampled from a mountainous geographic range, analysis of molecular variance (AMOVA) showed that the majority of genetic variation occurred among individuals within populations of both the aphid and its host. The aphid populations were found to be structured similarly to their primary host populations (F _ST values were 0.239 for the aphid and 0.209 for its host), suggesting that there are similar patterns of gene flow between the populations of the aphid and between populations of its host-plant. The genetic distances (F _ST/1 − F _ST) between the aphid populations and between its host-plant populations were uncorrelated, indicating that sites with genetically similar host-plant populations may not always have genetically similar aphid populations. The lack of relationships between genetic and geographical distance matrices suggested that isolation by distance (IBD) played a negligible role at this level. This may be mainly attributed to the founder effect, genetic drift and the relative small spatial scale between populations. Zhumei Ren and Bin Zhu contributed equally to this work.     

Is local selection so widespread in river organisms? Fractal geometry of river networks leads to high bias in outlier detection

Identifying local adaptation is crucial in conservation biology to define ecotypes and establish management guidelines. Local adaptation is often inferred from the detection of loci showing a high differentiation between populations, the so‐called F_ST outliers. Methods of detection of loci under selection are reputed to be robust in most spatial population models. However, using simulations we showed that F_ST outlier tests provided a high rate of false‐positives (up to 60%) in fractal environments such as river networks. Surprisingly, the number of sampled demes was correlated with parameters of population genetic structure, such as the variance of F_STs, and hence strongly influenced the rate of outliers. This unappreciated property of river networks therefore needs to be accounted for in genetic studies on adaptation and conservation of river organisms.     

Background selection and FST: Consequences for detecting local adaptation

Background selection is a process whereby recurrent deleterious mutations cause a decrease in the effective population size and genetic diversity at linked loci. Several authors have suggested that variation in the intensity of background selection could cause variation in F_ST across the genome, which could confound signals of local adaptation in genome scans. We performed realistic simulations of DNA sequences, using recombination maps from humans and sticklebacks, to investigate how variation in the intensity of background selection affects F_ST and other statistics of population differentiation in sexual, outcrossing species. We show that, in populations connected by gene flow, Weir and Cockerham's (1984; Evolution, 38 , 1358) estimator of F_ST is largely insensitive to locus‐to‐locus variation in the intensity of background selection. Unlike F_ST, however, d_XY is negatively correlated with background selection. Moreover, background selection does not greatly affect the false‐positive rate in F_ST outlier studies in populations connected by gene flow. Overall, our study indicates that background selection will not greatly interfere with finding the variants responsible for local adaptation.     

Genetic Variation and Differentiation among Populations of Chum Salmon Oncorhynchus ketaWalbaum from Southern Russian Far East

Allozyme variation of populations of chum salmon Oncorhynchus ketafrom southern Russian Far East was examined. Of 55 loci screened, 31 were polymorphic. Within-population variation accounted for most of the allele diversity; F _STaveraged over loci was 0.052. Linkage disequilibrium was found in less than 5% of locus pairs in the chum population examined. Analysis of within- and among-population variance components of linkage disequilibrium using D-statistics (Ohta, 1982) showed that most genetic variation was distributed among populations.