Genetic architecture and adaptive significance of the selfing syndrome in Capsella

The transition from outcrossing to predominant self-fertilization is one of the most common evolutionary transitions in flowering plants. This shift is often accompanied by a suite of changes in floral and reproductive characters termed the selfing syndrome. Here, we characterize the genetic architecture and evolutionary forces underlying evolution of the selfing syndrome in Capsella rubella following its recent divergence from the outcrossing ancestor C. grandiflora. We conduct genotyping by multiplexed shotgun sequencing and map floral and reproductive traits in a large (N= 550) F2 population. Our results suggest that in contrast to previous studies of the selfing syndrome, changes at a few loci, some with major effects, have shaped the evolution of the selfing syndrome in Capsella. The directionality of QTL effects, as well as population genetic patterns of polymorphism and divergence at 318 loci, is consistent with a history of directional selection on the selfing syndrome. Our study is an important step toward characterizing the genetic basis and evolutionary forces underlying the evolution of the selfing syndrome in a genetically accessible model system.     

Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana

Introduced species frequently show geographic differentiation, and when differentiation mirrors the ancestral range, it is often taken as evidence of adaptive evolution. The mouse-ear cress (Arabidopsis thaliana) was introduced to North America from Eurasia 150-200 years ago, providing an opportunity to study parallel adaptation in a genetic model organism. Here, we test for clinal variation in flowering time using 199 North American (NA) accessions of A. thaliana, and evaluate the contributions of major flowering time genes FRI, FLC, and PHYC as well as potential ecological mechanisms underlying differentiation. We find evidence for substantial within population genetic variation in quantitative traits and flowering time, and putatively adaptive longitudinal differentiation, despite low levels of variation at FRI, FLC, and PHYC and genome-wide reductions in population structure relative to Eurasian (EA) samples. The observed longitudinal cline in flowering time in North America is parallel to an EA cline, robust to the effects of population structure, and associated with geographic variation in winter precipitation and temperature. We detected major effects of FRI on quantitative traits associated with reproductive fitness, although the haplotype associated with higher fitness remains rare in North America. Collectively, our results suggest the evolution of parallel flowering time clines through novel genetic mechanisms.     

Escape from floral herbivory by early flowering in Arabidopsis halleri subsp. gemmifera

Natural selection on flowering phenology has been studied primarily in terms of plant–pollinator interactions and effects of abiotic conditions. Little is known, however, about geographic variation in other biotic factors such as herbivores and its consequence for differential selection on flowering phenology among populations. Here, we examine selection by floral herbivores on the flowering phenology of Arabidopsis halleri subsp. gemmifera using two adjacent populations with contrasting herbivory regimes. Intensive floral herbivory by the leaf beetle Phaedon brassicae occurs in one population, while the beetle is absent in another population. We tested the hypothesis that the two populations experience differential selection on flowering time that is attributable to the presence or absence of floral herbivory. A two-year field study showed that early flowering was favoured in the population under intensive floral herbivory, whereas selection for early flowering was not found in one year in the population where floral herbivory was absent. Selection for early flowering disappeared when the abundance of floral herbivores was artificially decreased in a field experiment. Thus, the heterogeneous distribution of P. brassicae was a major agent for differential selection on flowering time. However, flowering time did not differ between the two populations when plants were grown in the laboratory. The lack of genetic differentiation in flowering time may be explained by ongoing gene flow or recent invasion of P. brassicae. This study illustrates that the role of floral herbivory in shaping geographic variation in selection on flowering phenology may be more important than previously thought.     

The influence of population structure on gene expression and flowering time variation in the ubiquitous weed Capsella bursa‐pastoris (Brassicaceae)

Population structure is a potential problem when testing for adaptive phenotypic differences among populations. The observed phenotypic differences among populations can simply be due to genetic drift, and if the genetic distance between them is not considered, the differentiation may be falsely interpreted as adaptive. Conversely, adaptive and demographic processes might have been tightly associated and correcting for the population structure may lead to false negatives. Here, we evaluated this problem in the cosmopolitan weed Capsella bursa‐pastoris. We used RNA‐Seq to analyse gene expression differences among 24 accessions, which belonged to a much larger group that had been previously characterized for flowering time and circadian rhythm and were genotyped using genotyping‐by‐sequencing (GBS) technique. We found that clustering of accessions for gene expression retrieved the same three clusters that were obtained with GBS data previously, namely Europe, the Middle East and Asia. Moreover, the three groups were also differentiated for both flowering time and circadian rhythm variation. Correction for population genetic structure when analysing differential gene expression analysis removed all differences among the three groups. This may suggest that most differences are neutral and simply reflect population history. However, geographical variation in flowering time and circadian rhythm indicated that the distribution of adaptive traits might be confounded by population structure. To bypass this confounding effect, we compared gene expression differentiation between flowering ecotypes within the genetic groups. Among the differentially expressed genes, FLOWERING LOCUS C was the strongest candidate for local adaptation in regulation of flowering time.     

Microsatellite variation and structure of 28 populations of the common wetland plant, Lychnis flos-cuculi L., in a fragmented landscape

Habitat fragmentation is known to cause genetic differentiation between small populations of rare species and decrease genetic variation within such populations. However, common species with recently fragmented populations have rarely been studied in this context. We investigated genetic variation and its relationship to population size and geographical isolation of populations of the common plant species, Lychnis flos-cuculi L., in fragmented fen grasslands. We analysed 467 plants from 28 L. flos-cuculi populations of different sizes (60 000-54 000 flowering individuals) in northeastern Switzerland using seven polymorphic microsatellite loci. Genetic differentiation between populations is small (F(ST) = 0.022; amova; P < 0.001), suggesting that gene flow among populations is still high or that habitat fragmentation is too recent to result in pronounced differentiation. Observed heterozygosity (H(O) = 0.44) significantly deviates from Hardy-Weinberg equilibrium, and within-population inbreeding coefficient F(IS) is high (0.30-0.59), indicating a mixed mating breeding system with substantial inbreeding in L. flos-cuculi. Gene diversity is the only measure of genetic variation which decreased with decreasing population size (R = 0.42; P < 0.05). While our results do not indicate pronounced effects of habitat fragmentation on genetic variation in the still common L. flos-cuculi, the lower gene diversity of smaller populations suggests that the species is not entirely unaffected.     

Variation in Capsella (shepherd's purse): an example of intraspecific functional diversity

The extent of functional trait diversity is quantified for 157 different Capsella bursa-pastoris (L.) medic (shepherd's purse) accessions. These individuals encompass replicate progeny generated from seed of 53 different Capsella 'maternal lines' that were isolated at random as they emerged from soil cores (used to estimate baseline seed bank numbers and weed diversity) at 34 different arable sites across the United Kingdom. The replicate progeny were subject to ex situ characterisation for traits determining life history and architecture. Seven leaf-type classes were identified and representative parents of each leaf type were distinguishable using four different simple sequence repeat markers. Life-history traits were only loosely associated with leaf shape, and cluster analysis grouped the accessions into three broad types: small plants that flowered early with intermediate reproductive output; large plants, with intermediate time to flowering and a high reproductive output; late-flowering plants, of intermediate size and low reproductive output. The most common leaf-type variants (83% of accessions) demonstrated a short time to flowering (ca. 70 days), while rarer variants included those that flowered after 140 days, accumulated more nitrogen and produced less seed: possibly representing advantageous and disadvantageous traits (respectively), in modern arable rotations. A wide trait variation was therefore found in Capsella bursa-pastoris despite decades of agricultural intensification, the range of time-to-flowering for C. bursa-pastoris being as broad the mean flowering times of the commoner annual and winter annual arable species. We propose the use of traits, rather than species, as the accounting unit to quantify functional biodiversity in arable systems.     

Catching a 'hopeful monster': shepherd's purse (Capsella bursa-pastoris) as a model system to study the evolution of flower development

Capsella is a small genus within the mustard family (Brassicaceae). Its three species, however, show many evolutionary trends also observed in other Brassicaceae (including Arabidopsis) and far beyond, including transitions from a diploid, self-incompatible, obligatory outcrossing species with comparatively large and attractive flowers but a restricted distribution to a polyploid, self-compatible, predominantly selfing, invasive species with floral reductions. All these evolutionary transitions may have contributed to the fact that Capsella bursa-pastoris (shepherd's purse) has become one of the most widely distributed flowering plants on our planet. In addition, Capsella bursa-pastoris shows a phenomenon that, although rare, could be of great evolutionary importance, specifically the occurrence of a homeotic variety found in relatively stable populations in the wild. Several lines of evidence suggest that homeotic changes played a considerable role in floral evolution, but how floral homeotic varieties are established in natural populations has remained a highly controversial topic among evolutionary biologists. Due to its close relationship with the model plant Arabidopsis thaliana, numerous experimental tools are available for studying the genus Capsella, and further tools are currently being developed. Hence, Capsella provides great opportunities to investigate the evolution of flower development from molecular developmental genetics to field ecology and biogeography, and from morphological refinements to major structural transitions.     

Evolutionary analysis of a key floral trait in aquilegia canadensis (ranunculaceae): genetic variation in herkogamy and its effect on the mating system

The mating system of flowering plant populations evolves through selection on genetically based phenotypic variation in floral traits. The physical separation of anthers and stigmas within flowers (herkogamy) is expected to be an important target of selection to limit self-fertilization. We investigated the pattern of phenotypic and genetic variation in herkogamy and its effect of self-fertilization in a broad sample of natural populations of Aquilegia canadensis, a species that is highly selfing despite strong inbreeding depression. Within natural populations, plants exhibit substantial phenotypic variation in herkogamy caused primarily by variation in pistil length rather than stamen length. Compared to other floral traits, herkogamy is much more variable and a greater proportion of variation is distributed among rather than within individuals. We tested for a genetic component of this marked phenotypic variation by growing naturally pollinated seed families from five populations in a common greenhouse environment. For three populations, we detected a significant variation in herkogamy among families, and a positive regression between parental herkogamy measured in the field and progeny herkogamy in the greenhouse, suggesting that there is often genetic variation in herkogamy within natural populations. We estimated levels of self-fertilization for groups of flowers that differed in herkogamy and show that, as expected, herkogamy was associated with reduced selfing in 13 of 19 populations. In six of these populations, we performed floral emasculations to show that this decrease in selfing is due to decreased autogamy (within-flower selfing), the mode of selfing that herkogamy should most directly influence. Taken together, these results suggest that increased herkogamy should be selected to reduce the production of low-quality selfed seed. The combination of high selfing and substantial genetic variation for herkogamy in A. canadensis is enigmatic, and reconciling this observation will require a more integrated analysis of how herkogamy influences not only self-fertilization, but also patterns of outcross pollen import and export.     

Pollinator behavior and deceptive pollination: learning process and floral evolution

Some species of flowering plants engage in nonmodel deceptive pollination, attracting pollinators by large nonmimetic floral displays and providing no reward. Pollinators can learn to avoid deceptive plants and to favor nectariferous species. The reproductive success of these species is expected to be density dependent for two opposite reasons: the commoner cheating flowers are, the easier they are to avoid and the lower the quality of the patch, making it more difficult to recognize that unrewarding flowers are not profitable. When a deceptive species is made up of multiple floral variants, pollinators' learning could decrease the reproductive success of any particularly common floral variant. Within a population of deceptive plants, mean reproductive success could, therefore, vary with the number of floral variants. We investigate these three hypotheses by modeling the behavior of pollinators foraging in communities of deceptive and rewarding flowers. Simulations revealed that the reproductive success of deceptive flowers varies in a density-dependent manner and that floral variants can be submitted to negative frequency-dependent selection. We compare density dependence in nonmodel deceptive species to what is expected in Batesian mimics and discuss possible selection of morphological variants. Finally, we survey how pollinators' learning capacities can make mean reproductive success depend on morphological variability within a population.     

Selection on flowering time and floral display in an alpine and a lowland population of Arabidopsis lyrata

To determine whether population differentiation in flowering time is consistent with differences in current selection, we quantified phenotypic selection acting through female reproductive success on flowering phenology and floral display in two Scandinavian populations of the outcrossing, perennial herb Arabidopsis lyrata in two years. One population was located in an alpine environment strongly affected by grazing, whereas the other was close to sea level and only moderately affected by herbivory. Multiple regression models indicated directional selection for early end of flowering in one year in the lowland population, and directional selection for early start of flowering in one year in the alpine population. As expected, there was selection for more inflorescences in the lowland population. However, in the alpine population, plants with many inflorescences were selectively grazed and the number of inflorescences produced was negatively related to female fitness in one year and not significantly related to female fitness in the second year. The results are consistent with the hypothesis that genetic differentiation in flowering phenology between the study populations is adaptive, and indicate that interactions with selective grazers may strongly influence selection on floral display in A. lyrata.     

Enzyme polymorphism, morphometric variation and population structure in a restricted endemic, Silene diclinis (Caryophyllaceae)

Silene diclinis is a dioecious perennial herb, restricted to a small area of the SE Spanish province of Valencia. Polyacrylamide gel electrophoresis and morphometric analysis were carried out on cultivated material derived from seed collected from the main population of S. diclinis at Játiva. Only two out of 26 inferred enzyme loci showed substantial variation. There was some indication of population subdivision in both. The esterase locus also showed homozygote excess within the population as a whole and within one subpopulation. Morphological characters showed significant differentiation between subpopulations.
Low allozyme variability characterizes populations of most endemic species that have been investigated. Isolation and historical events may have been as important as population size or edaphic specialization in causing this low variability. But S. diclinis resembles other outbreeding plants in showing population structure and homozygote excess, suggesting restricted within-population gene flow. Mechanisms that may restrict gene flow in S. diclinis include environmentally-induced differences in flowering time, poor seed dispersal and possibly short pollinator foraging distances. Morphological variability and the incidence of developmental abnormalities are speculatively linked with homozygosity. Storage of genetic diversity in space can occur in restricted as well as widespread species and sampling for gene banking should then be spatially representative. Silene diclinis is threatened by continued habitat loss and consequent genetic erosion; its long-term future may depend on the gene bank and the botanic garden.     

Genetic structure and gene flow in a metapopulation of an endangered plant species,Silene tatarica

We investigated the distribution of genetic variation within and between seven subpopulations in a riparian population of Silene tatarica in northern Finland by using amplified fragment length polymorphism (AFLP) markers. A Bayesian approach-based clustering program indicated that the marker data contained not only one panmictic population, but consisted of seven clusters, and that each original sample site seems to consist of a distinct subpopulation. A coalescent-based simulation approach shows recurrent gene flow between subpopulations. Relative high FST values indicated a clear subpopulation differentiation. However, amova analysis and UPGMA-dendrogram did not suggest any hierarchical regional structuring among the subpopulations. There was no correlation between geographical and genetic distances among the subpopulations, nor any correlation between the subpopulation census size and amount of genetic variation. Estimates of gene flow suggested a low level of gene flow between the subpopulations, and the assignment tests proposed a few long-distance bidirectional dispersal events between the subpopulations. No apparent difference was found in within-subpopulation genetic diversity among upper, middle and lower regions along the river. Relative high amounts of linkage disequilibrium at subpopulation level indicated recent population bottlenecks or admixture, and at metapopulation levels a high subpopulation turnover rate. The overall pattern of genetic variation within and between subpopulations also suggested a 'classical' metapopulation structure of the species suggested by the ecological surveys.     

Floral visitation and reproductive traits of <Emphasis Type="Italic">Stamenoid petals</Emphasis>, a naturally occurring floral homeotic variant of <Emphasis Type="Italic">Capsella bursa-pastoris</Emphasis> (Brassicaceae)

Homeotic changes played a considerable role during the evolution of flowers, but how floral homeotic mutants initially survive in nature has remained enigmatic. To better understand the evolutionary potential of floral homeotic mutants, we established as a model system Stamenoid petals (Spe), a natural variant of Capsella bursa-pastoris (Brassicaceae). In the flowers of Spe plants, petals are transformed into stamens, whereas all other floral organs are unaffected. In contrast with most other homeotic mutants, the Spe variant occurs in relatively stable populations in the wild. In order to determine how the profound change in floral architecture influences plant performance in the wild, we performed common garden experiments running over 3 years. Here, we show that Spe and wild-type plants attract the same assemblage of floral visitors: mainly hoverflies, wild bees and thrips. However, floral visitation is about twice as frequent in wild-type plants as in Spe plants. Nevertheless, the numbers of seeds per fruit were about the same in both variants. Wild-type plants produced more flowers, fruits and seeds per plant than Spe plants, whereas the germination capacity of Spe seeds was higher than that of the wild-type. Determination of volatile composition revealed monoterpenes and 3,4-dimethylbenzaldehyde, which were detected only in wild-type flowers, presumably because they are produced only by petals. Our data indicate that the similar fitness of Spe and wild-type C. bursa-pastoris in the field results from complex compensation between plant architecture and germination capacity. In contrast, flower structure and floral visitation are only of minor importance, possibly because C. bursa-pastoris is mainly self-pollinating.     

Integrating floral scent, pollination ecology and population genetics

1 . Floral scent is a key factor in the attraction of pollinators. Despite this, the role of floral scent in angiosperm speciation and evolution remains poorly understood. Modern population genetic approaches when combined with pollination ecology can open new opportunities for studying the evolutionary role of floral scent.
2 . A framework of six hypotheses for the application of population genetic tools to questions about the evolutionary role of floral scent is presented. When floral volatile chemistry is linked to pollinator attraction we can analyse questions such as: Does floral volatile composition reflect plant species boundaries? Can floral scent facilitate or suppress hybridization between taxa? Can the attraction of different pollinators influence plant mating systems and pollen-mediated gene flow? How is population genetic structure indirectly influenced by floral scent variation?
3 . The application of molecular tools in sexually deceptive orchids has confirmed that volatile composition reflects species boundaries, revealed the role of shared floral odour in enabling hybridization, confirmed that the sexual attraction mediated by floral odour has implications for pollen flow and population genetic structure and provided examples of pollinator-mediated selection on floral scent variation. Interdisciplinary studies to explore links between floral volatile variation, ecology and population genetics are rare in other plant groups.
4 . Ideal study systems for future floral scent research that incorporate population genetics will include closely related taxa that are morphologically similar, sympatric and co-flowering as well as groups that display wide variation in pollination mechanisms and floral volatiles.     

Genetic diversity and genetic structure of populations of Ranunculus japonicus Thunb. (Ranunculaceae)

Abstract In order to clarify the genetic diversity and population structure of Ranunculus japonicus , allozymic analysis was conducted on 60 populations in southwestern Japan. Considerable genetic variati ons were detected among the populations of R. japonicus . The genetic diversities within species ( H _es = 0.215) and within populations ( H _ep = 0.172) were slightly higher than those of other perennial herbs with widespread distribution and outcrossing plants. Significantly higher values of fixation index were detected in some populations, which might have arisen from restricted mating partners. The majority of genetic variation (approx. 80%) resided within a population and a moderate level of genetic differentiation ( G _ST = 0.203) was observed among populations. The F _ST value (0.203) suggests the existence of a substantial population structure in this species. The highly significant correlation between geographic distance and F _ST values indicates that isolation by distance has played an important role in the construction of the genetic structure of this species.     

Capsella as a model system to study the evolutionary relevance of floral homeotic mutants

Several lines of evidence suggest that homeotic changes played a considerable role during the evolution of flowers. This, however, is difficult to reconcile with the predominant evolutionary theory which rejects any drastic, saltational change of the phenotype as reasonable mode of evolution due to its assumed negative impact on the fitness of the affected organism. A better understanding of the evolutionary potential of homeotic transitions requires a study of the performance of respective mutant varieties in the wild. Here we introduce ``Stamenoid petals' (Spe), a variety of Capsella bursa-pastoris (shepherd's purse), as a suitable model to study the evolutionary potential of floral homeotic mutants. In the flowers of the Spe variety all petals are transformed into stamens, while all other floral organs are unaffected. In contrast to most other homeotic mutants the Spe variety occurs on several locations in relatively large and stable populations in the wild. Due to its close relationship to the model plant Arabidopsis thaliana, the Spe variety of C. bursa-pastoris can be rigorously studied, from the molecular genetic basis of the phenotype to its consequences on the fitness in wild habitats. Investigations on Spe may thus help to clarify whether homeotic transformations have the potential to contribute to macroevolution.     

The population genetic effects of ancestry and admixture in a subdivided cattle breed

The genetic structure of the Dexter, a minority cattle breed with complex demographic history, was investigated using microsatellite markers and a range of statistical approaches designed to detect both admixture and genetic drift. Modern representatives of two putative ancestral populations, the Devon and Kerry, together with the different populations of the Dexter, which have experienced different demographic histories, were analysed. Breed units showed comparatively high levels of genetic variability ( H _E = 0.63–0.68); however, distinct genetic subgroups were detected within the Dexter, which could be attributed to known demographic events. Much lower diversity was identified in three small, isolated Dexter populations ( H _E = 0.52–0.55) and higher differentiation ( F _ST > 0.13) was found. For one of these populations, where strong selection has taken place, we also found evidence of a demographic bottleneck. Three methods for quantifying breed admixture were applied and substantial method-based variation in estimates for the genetic contribution of the two proposed ancestral populations for each subdivision of the Dexter was found. Results were consistent only in the case of a group consisting of selected Traditional Dexter animals, where the ancestor of the modern Kerry breed was also determined as the greater parental contributor to the Dexter. The inconsistency of estimation of admixture proportions between the methods highlights the potentially confounding role of genetic drift in shaping small population structure, and the consequences of accurately describing population histories from contemporary genetic data.     

Relatedness structure in Rhododendron metternichii var. hondoense revealed by microsatellite analysis

The relatedness structure of Rhododendron metternichii Sieb. et Zucc. var. hondoense Nakai was analysed in a 150 x 70-m quadrat in Hiroshima Prefecture, western Japan. The population of R. metternichii occurred as three subpopulations at the study site (A1-A3). Pairwise relatedness based on microsatellite genotypes at eight loci and Mantel tests revealed a hierarchical structure of relatedness within and among subpopulations: (i) relatedness between individuals within 10 m of one another was significantly positive; (ii) relatedness between individuals in the same subpopulation was significantly positive, but negative between individuals in distant subpopulations; and (iii) relatedness was not significantly different from zero among neighbouring subpopulations. In detail, however, relatedness within each subpopulation was significantly positive in subpopulation A1, relatively weak but significantly positive in subpopulation A2, and not significantly different from zero in subpopulation A3. Relatedness within each subpopulation was inversely related to correlations between interindividual distance and relatedness. The aggregation of related individuals at short distances from one another may lead to decreasing relatedness within subpopulations as a whole. Moreover, negative correlations between interindividual distance and relatedness corresponded to high flowering densities at less than 10-m distance, implying that high flowering densities reduce pollinator foraging distance and lead to stronger genetic structure within subpopulations. Small individuals (< 2.0 m in height) showed stronger genetic structure compared with that of large individuals (> or = 2.0 m in height). The different relatedness structure within and among subpopulations may be caused by various degrees of gene flow affected by distribution patterns of individuals and population density.     

Contrasting patterns of floral and molecular variation across a cline in Mimulus aurantiacus

Abstract Steep clines in ecologically important traits may be caused by divergent natural selection. However, processes that do not necessarily invoke ongoing selection, such as secondary contact or restricted gene flow, can also cause patterns of phenotypic differentiation over short spatial scales. Distinguishing among all possible scenarios is difficult, but an attainable goal is to establish whether scenarios that imply selection need to be invoked. We compared the extent of morphological and genetic differentiation between geographically structured red and yellow floral races of Mimulus aurantiacus (bush monkeyflower; Phrymacea). Flower color was assessed in a common garden as well as in the field to determine whether variation was genetic and to quantify the extent of geographical differentiation. Population genetic differentiation at marker loci was measured for both chloroplast and nuclear genomes, and the degree of population structure within and among the floral races was evaluated. Flower color shows both a strong genetic basis and a sharp geographic transition, with pure red-flowered populations in western San Diego County and pure yellow-flowered populations to the east. In the zone of contact, both pure and intermediate phenotypes occur. Patterns of genetic differentiation at marker loci are far less pronounced, as little of the variation is partitioned according to the differences in flower color. Phenotypic differentiation (Q_ST) between populations with different flower colors is much greater than neutral genetic differentiation (F_ST). When comparisons are made between populations of the same flower color, the opposite trend is evident. Limited neutral genetic structure between the floral races, combined with sharp differentiation in flower color, is consistent with the hypothesis that current or recent natural selection maintains the cline in flower color.     

Among- and within-patch components of genetic diversity respond at different rates to habitat fragmentation: an empirical demonstration

Habitat fragmentation is a ubiquitous by-product of human activities that can alter the genetic structure of natural populations, with potentially deleterious effects on population persistence and evolutionary potential. When habitat fragmentation results in the subdivision of a population, random genetic drift then leads to the erosion of genetic diversity from within the resulting subpopulation, random genetic drift then leads to the erosion of genetic diversity from within the resulting subpopulations and greater genetic divergence among them. Theoretical and simulation analyses predict that these two main genetic effects of fragmentation, greater differentiation among resulting subpopulation and reduced genetic diversity within them, will proceed at very different rates. Despite important implications for the interpretation of genetics data from fragmented populations, empirical evidence for this phenomenon has been lacking. In this analysis, we carry out an empirical study in population of an alpine meadow-dwelling butterfly, which have become fragmented increasing forest cover over five decades. We show that genetic differentiation among subpopulations (G(ST)) is most highly correlated with contemporary forest cover, while genetics diversity within subpopulation (expected heterozygosity) is better correlated with the spatial pattern of forest cover 40 years in the past. Thus, where habitat fragmentation has occurred in recent decades, genetic differentiation among subpopulation can be near equilibrium while contemporary measures of within subpopulation diversity may substantially overestimate the equilibrium values that will eventually be attained.