Bud phenology and growth are subject to divergent selection across a latitudinal gradient in Populus angustifolia and impact adaptation across the distributional range and associated arthropods

Temperate forest tree species that span large geographical areas and climatic gradients often have high levels of genetic variation. Such species are ideal for testing how neutral demographic factors and climate‐driven selection structure genetic variation within species, and how this genetic variation can affect ecological communities. Here, we quantified genetic variation in vegetative phenology and growth traits in narrowleaf cottonwood, Populus angustifolia, using three common gardens planted with genotypes originating from source populations spanning the species' range along the Rocky Mountains of North America (ca. 1700 km). We present three main findings. First, we found strong evidence of divergent selection (Q_ST > F_ST) on fall phenology (bud set) with adaptive consequences for frost avoidance. We also found evidence for selection on bud flush duration, tree height, and basal diameter, resulting in population differentiation. Second, we found strong associations with climate variables that were strongly correlated with latitude of origin. More strongly differentiated traits also showed stronger climate correlations, which emphasizes the role that climate has played in divergent selection throughout the range. We found population × garden interaction effects; for some traits, this accounted for more of the variance than either factor alone. Tree height was influenced by the difference in climate of the source and garden locations and declined with increasing transfer distance. Third, growth traits were correlated with dependent arthropod community diversity metrics. Synthesis. Overall, we conclude that climate has influenced genetic variation and structure in phenology and growth traits and leads to local adaptation in P. angustifolia, which can then impact dependent arthropod species. Importantly, relocation of genotypes far northward or southward often resulted in poor growth, likely due to a phenological mismatch with photoperiod, the proximate cue for fall growth cessation. Genotypes moved too far southward suffer from early growth cessation, whereas those moved too far northward are prone to fall frost and winter dieback. In the face of current and forecasted climate change, habitat restoration, forestry, and tree breeding efforts should utilize these findings to better match latitudinal and climatic source environments with management locations for optimal future outcomes.     

An ecological genetic delineation of local seed‐source provenance for ecological restoration

An increasingly important practical application of the analysis of spatial genetic structure within plant species is to help define the extent of local provenance seed collection zones that minimize negative impacts in ecological restoration programs. Here, we derive seed sourcing guidelines from a novel range‐wide assessment of spatial genetic structure of 24 populations of Banksia menziesii (Proteaceae), a widely distributed Western Australian tree of significance in local ecological restoration programs. An analysis of molecular variance (AMOVA) of 100 amplified fragment length polymorphism (AFLP) markers revealed significant genetic differentiation among populations (Φ_PT = 0.18). Pairwise population genetic dissimilarity was correlated with geographic distance, but not environmental distance derived from 15 climate variables, suggesting overall neutrality of these markers with regard to these climate variables. Nevertheless, Bayesian outlier analysis identified four markers potentially under selection, although these were not correlated with the climate variables. We calculated a global R‐statistic using analysis of similarities (ANOSIM) to test the statistical significance of population differentiation and to infer a threshold seed collection zone distance of ~60 km (all markers) and 100 km (outlier markers) when genetic distance was regressed against geographic distance. Population pairs separated by >60 km were, on average, twice as likely to be significantly genetically differentiated than population pairs separated by <60 km, suggesting that habitat‐matched sites within a 30‐km radius around a restoration site genetically defines a local provenance seed collection zone for B. menziesii. Our approach is a novel probability‐based practical solution for the delineation of a local seed collection zone to minimize negative genetic impacts in ecological restoration.     

High degree of genetic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus)

Populations of widespread marine organisms are typically characterized by a low degree of genetic differentiation in neutral genetic markers, but much less is known about differentiation in genes whose functional roles are associated with specific selection regimes. To uncover possible adaptive population divergence and heterogeneous genomic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus), we used a candidate gene‐based genome‐scan approach to analyse variability in 138 microsatellite loci located within/close to (<6 kb) functionally important genes in samples collected from ten geographic locations. The degree of genetic differentiation in markers classified as neutral or under balancing selection—as determined with several outlier detection methods—was low (F_ST = 0.033 or 0.011, respectively), whereas average F_ST for directionally selected markers was significantly higher (F_ST = 0.097). Clustering analyses provided support for genomic and geographic heterogeneity in selection: six genetic clusters were identified based on allele frequency differences in the directionally selected loci, whereas four were identified with the neutral loci. Allelic variation in several loci exhibited significant associations with environmental variables, supporting the conjecture that temperature and salinity, but not optic conditions, are important drivers of adaptive divergence among populations. In general, these results suggest that in spite of the high degree of physical connectivity and gene flow as inferred from neutral marker genes, marine stickleback populations are strongly genetically structured in loci associated with functionally relevant genes.     

Effect of Yangtze River on population genetic structure of the relict plant Parrotia subaequalis in eastern China

Parrotia subaequalis (Hamamelidaceae) is a Tertiary relic species endemic in eastern China. We used inter‐simple sequence repeat (ISSR) markers to access genetic diversity and population genetic structure in natural five populations of P. subaequalis. The levels of genetic diversity were higher at species level (H = 0.2031) but lower at population level (H = 0.1096). The higher genetic diversity at species levels might be attributed to the accumulation of distinctive genotypes which adapted to the different habitats after Quaternary glaciations. Meanwhile, founder effects on the early stage, and subsequent bottleneck of population regeneration due to its biological characteristics, environmental features, and human activities, seemed to explain the low population levels of genetic diversity. The hierarchical AMOVA revealed high levels (42.60%) of among‐population genetic differentiation, which was in congruence with the high levels of Nei's genetic differentiation index (G_ST = 0.4629) and limited gene flow (N_m = 0.5801) among the studied populations. Mantel test showed a significant isolation‐by‐distance, indicating that geographic isolation has a significant effect on genetic structure in this species. Unweighted pair‐group method with arithmetic average clustering, PCoA, and Bayesian analyses uniformly recovered groups that matched the geographical distribution of this species. In particular, our results suggest that Yangtze River has served as a natural barrier to gene flow between populations occurred on both riversides. Concerning the management of P. subaequalis, the high genetic differentiation among populations indicates that preserving all five natural populations in situ and collecting enough individuals from these populations for ex situ conservation are necessary.     

Environmental gradients shape the genetic structure of two medicinal Salvia species in Jordan

• Environmental gradients, and particularly climatic variables, exert a strong influence on plant distribution and, potentially, population genetic diversity and differentiation. Differences in water availability can cause among‐population variation in ecological processes and can thus interrupt populations’ connectivity and isolate them environmentally. The present study examines the effect of environmental heterogeneity on plant populations due to environmental isolation unrelated to geographic distance.
• Using AFLP markers, we analyzed genetic diversity and differentiation among 12 Salvia spinosa populations and 13 Salvia syriaca populations from three phytogeographical regions (Mediterranean, Irano‐Turanian and Saharo‐Arabian) representing the extent of the species’ geographic range in Jordan. Differences in geographic location and climate were considered in the analyses.
• For both species, flowering phenology varied among populations and regions. Irano‐Turanian and Saharo‐Arabian populations had higher genetic diversity than Mediterranean populations, and genetic diversity increased significantly with increasing temperature. Genetic diversity in Salvia syriaca was affected by population size, while genetic diversity responded to drought in S. spinosa. For both species, high levels of genetic differentiation were found as well as two well‐supported phytogeographical groups of populations, with Mediterranean populations clustering in one group and the Irano‐Turanian and Saharo‐Arabian populations in another. Genetic distance was significantly correlated to environmental distance, but not to geographic distance.
• Our data indicate that populations from moist vs. arid environments are environmentally isolated, where environmental gradients affect their flowering phenology, limit gene flow and shape their genetic structure. We conclude that environmental heterogeneity may act as driver for the observed variation in genetic diversity.

     

Evolutionary dynamics of the leaf phenological cycle in an oak metapopulation along an elevation gradient

It has been predicted that environmental changes will radically alter the selective pressures on phenological traits. Long‐lived species, such as trees, will be particularly affected, as they may need to undergo major adaptive change over only one or a few generations. The traits describing the annual life cycle of trees are generally highly evolvable, but nothing is known about the strength of their genetic correlations. Tight correlations can impose strong evolutionary constraints, potentially hampering the adaptation of multivariate phenological phenotypes. In this study, we investigated the evolutionary, genetic and environmental components of the timing of leaf unfolding and senescence within an oak metapopulation along an elevation gradient. Population divergence, estimated from in situ and common‐garden data, was compared to expectations under neutral evolution, based on microsatellite markers. This approach made it possible (1) to evaluate the influence of genetic correlation on multivariate local adaptation to elevation and (2) to identify traits probably exposed to past selective pressures due to the colder climate at high elevation. The genetic correlation was positive but very weak, indicating that genetic constraints did not shape the local adaptation pattern for leaf phenology. Both spring and fall (leaf unfolding and senescence, respectively) phenology timings were involved in local adaptation, but leaf unfolding was probably the trait most exposed to climate change‐induced selection. Our data indicated that genetic variation makes a much smaller contribution to adaptation than the considerable plastic variation displayed by a tree during its lifetime. The evolutionary potential of leaf phenology is, therefore, probably not the most critical aspect for short‐term population survival in a changing climate.     

Large‐scale adaptive divergence in Boechera fecunda,an endangered wild relative of Arabidopsis

Many biological species are threatened with extinction because of a number of factors such as climate change and habitat loss, and their preservation depends on an accurate understanding of the extent of their genetic variability within and among populations. In this study, we assessed the genetic divergence of five quantitative traits in 10 populations of an endangered cruciferous species, Boechera fecunda, found in only several populations in each of two geographic regions (WEST and EAST) in southwestern Montana. We analyzed variation in quantitative traits, neutral molecular markers, and environmental factors and provided evidence that despite the restricted geographical distribution of this species, it exhibits a high level of genetic variation and regional adaptation. Conservation efforts therefore should be directed to the preservation of populations in each of these two regions without attempting transplantation between regions. Heritabilities and genetic coefficients of variation estimated from nested ANOVAs were generally high for leaf and rosette traits, although lower (and not significantly different from 0) for water‐use efficiency. Measures of quantitative genetic differentiation, Q_ST, were calculated for each trait from each pair of populations. For three of the five traits, these values were significantly higher between regions compared with those within regions (after adjustment for neutral genetic variation, F_ST). This suggested that natural selection has played an important role in producing regional divergence in this species. Our analysis also revealed that the B. fecunda populations appear to be locally adapted due, at least in part, to differences in environmental conditions in the EAST and WEST regions.     

The influence of breeding phenology on the genetic structure of four pond‐breeding salamanders

Understanding metapopulation dynamics requires knowledge about local population dynamics and movement in both space and time. Most genetic metapopulation studies use one or two study species across the same landscape to infer population dynamics; however, using multiple co‐occurring species allows for testing of hypotheses related to different life history strategies. We used genetic data to study dispersal, as measured by gene flow, in three ambystomatid salamanders (Ambystoma annulatum , A. maculatum , and A. opacum ) and the Central Newt (Notophthalmus viridescens louisianensis ) on the same landscape in Missouri, USA . While all four salamander species are forest dependent organisms that require fishless ponds to reproduce, they differ in breeding phenology and spatial distribution on the landscape. We use these differences in life history and distribution to address the following questions: (1) Are there species‐level differences in the observed patterns of genetic diversity and genetic structure? and (2) Is dispersal influenced by landscape resistance? We detected two genetic clusters in A. annulatum and A. opacum on our landscape; both species breed in the fall and larvae overwinter in ponds. In contrast, no structure was evident in A. maculatum and N. v. louisianensis , species that breed during the spring. Tests for isolation by distance were significant for the three ambystomatids but not for N. v. louisianensis . Landscape resistance also contributed to genetic differentiation for all four species. Our results suggest species‐level differences in dispersal ability and breeding phenology are driving observed patterns of genetic differentiation. From an evolutionary standpoint, the observed differences in dispersal distances and genetic structure between fall breeding and spring breeding species may be a result of the trade‐off between larval period length and size at metamorphosis which in turn may influence the long‐term viability of the metapopulation. Thus, it is important to consider life history differences among closely related and ecologically similar species when making management decisions.     

Genetic inference of epiphytic orchid colonization; it may only take one

Colonization of vacant habitat is a fundamental ecological process that affects the ability of species to persist and undergo range modifications in continually shifting landscapes. Thus, understanding factors that affect and limit colonization has important ecological and conservation implications. Epiphytic orchids are increasingly threatened by various factors, including anthropogenic habitat disturbance. As cleared areas (e.g. pastures) are recolonized by suitable host trees, the establishment and genetic composition of epiphytic orchid populations are likely a function of their colonization patterns. We used genetic analyses to infer the prevailing colonization pattern of the epiphytic orchid, Brassavola nodosa. Samples from three populations (i.e. individuals within a tree) from each of five pastures in the dry forest of Costa Rica were genotyped with neutral nuclear and chloroplast markers. Spatial autocorrelation and hierarchical genetic structure analyses were used to assess the relatedness of individuals within populations, among populations within pastures and among populations in different pastures. The results showed significant relatedness within populations (mean r = 0.166) and significant but lower relatedness among populations within a pasture (mean r = 0.058). Our data suggest that colonization of available habitats is by few individuals with subsequent population expansion resulting from in situ reproduction, and that individuals within a tree are not a random sample of the regional seed pool. Furthermore, populations within a pasture were likely colonized by seeds produced by founders of a neighbouring population within that pasture. These results have important ramifications for understanding conservation measures needed for this species and other epiphytic orchids.     

Use of intraspecific variation in thermal responses for estimating an elevational cline in the timing of cold hardening in a sub‐boreal conifer

To avoid winter frost damage, evergreen coniferous species develop cold hardiness with suitable phenology for the local climate regime. Along the elevational gradient, a genetic cline in autumn phenology is often recognised among coniferous populations, but further quantification of evolutionary adaptation related to the local environment and its responsible signals generating the phenological variation are poorly understood. We evaluated the timing of cold hardening among populations of Abies sachalinensis, based on time series freezing tests using trees derived from four seed source populations × three planting sites. Furthermore, we constructed a model to estimate the development of hardening from field temperatures and the intraspecific variations occurring during this process. An elevational cline was detected such that high‐elevation populations developed cold hardiness earlier than low‐elevation populations, representing significant genetic control. Because development occurred earlier at high‐elevation planting sites, the genetic trend across elevation overlapped with the environmental trend. Based on the trade‐off between later hardening to lengthen the active growth period and earlier hardening to avoid frost damage, this genetic cline would be adaptive to the local climate. Our modelling approach estimated intraspecific variation in two model components: the threshold temperature, which was the criterion for determining whether the trees accumulated the thermal value, and the chilling requirement for trees to achieve adequate cold hardiness. A higher threshold temperature and a lower chilling requirement could be responsible for the earlier phenology of the high‐elevation population. These thermal responses may be one of the important factors driving the elevation‐dependent adaptation of A. sachalinensis.     

Toxicity and population structure of the Rough‐Skinned Newt (Taricha granulosa) outside the range of an arms race with resistant predators

Species interactions, and their fitness consequences, vary across the geographic range of a coevolutionary relationship. This spatial heterogeneity in reciprocal selection is predicted to generate a geographic mosaic of local adaptation, wherein coevolutionary traits are phenotypically variable from one location to the next. Under this framework, allopatric populations should lack variation in coevolutionary traits due to the absence of reciprocal selection. We examine phenotypic variation in tetrodotoxin (TTX) toxicity of the Rough‐Skinned Newt (Taricha granulosa) in regions of allopatry with its TTX‐resistant predator, the Common Garter Snake (Thamnophis sirtalis). In sympatry, geographic patterns of phenotypic exaggeration in toxicity and toxin‐resistance are closely correlated in prey and predator, implying that reciprocal selection drives phenotypic variation in coevolutionary traits. Therefore, in allopatry with TTX‐resistant predators, we expect to find uniformly low levels of newt toxicity. We characterized TTX toxicity in northwestern North America, including the Alaskan panhandle where Ta. granulosa occur in allopatry with Th. sirtalis. First, we used microsatellite markers to estimate population genetic structure and determine if any phenotypic variation in toxicity might be explained by historical divergence. We found northern populations of Ta. granulosa generally lacked population structure in a pattern consistent with northern range expansion after the Pleistocene. Next, we chose a cluster of sites in Alaska, which uniformly lacked genetic divergence, to test for phenotypic divergence in toxicity. As predicted, overall levels of newt toxicity were low; however, we also detected unexpected among‐ and within‐population variation in toxicity. Most notably, a small number of individuals contained large doses of TTX that rival means of toxic populations in sympatry with Th. sirtalis. Phenotypic variation in toxicity, despite limited neutral genetic divergence, suggests that factors other than reciprocal selection with Th. sirtalis likely contribute to geographic patterns of toxicity in Ta. granulosa.     

Secondary contact and local adaptation contribute to genome‐wide patterns of clinal variation in Drosophila melanogaster

Populations arrayed along broad latitudinal gradients often show patterns of clinal variation in phenotype and genotype. Such population differentiation can be generated and maintained by both historical demographic events and local adaptation. These evolutionary forces are not mutually exclusive and can in some cases produce nearly identical patterns of genetic differentiation among populations. Here, we investigate the evolutionary forces that generated and maintain clinal variation genome‐wide among populations of Drosophila melanogaster sampled in North America and Australia. We contrast patterns of clinal variation in these continents with patterns of differentiation among ancestral European and African populations. Using established and novel methods we derive here, we show that recently derived North America and Australia populations were likely founded by both European and African lineages and that this hybridization event likely contributed to genome‐wide patterns of parallel clinal variation between continents. The pervasive effects of admixture mean that differentiation at only several hundred loci can be attributed to the operation of spatially varying selection using an F_ST outlier approach. Our results provide novel insight into the well‐studied system of clinal differentiation in D. melanogaster and provide a context for future studies seeking to identify loci contributing to local adaptation in a wide variety of organisms, including other invasive species as well as temperate endemics.     

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.     

QST–FST comparisons with unbalanced half‐sib designs

Q_ST, a measure of quantitative genetic differentiation among populations, is an index that can suggest local adaptation if Q_ST for a trait is sufficiently larger than the mean F_ST of neutral genetic markers. A previous method by Whitlock and Guillaume derived a simulation resampling approach to statistically test for a difference between Q_ST and F_ST, but that method is limited to balanced data sets with offspring related as half‐sibs through shared fathers. We extend this approach (i) to allow for a model more suitable for some plant populations or breeding designs in which offspring are related through mothers (assuming independent fathers for each offspring; half‐sibs by dam); and (ii) by explicitly allowing for unbalanced data sets. The resulting approach is made available through the R package QstFstComp.     

Population genetic structure,genetic diversity,and natural history of the South American species of Nothofagus subgenus Lophozonia (Nothofagaceae) inferred from nuclear microsatellite data

The effect of glaciation on the levels and patterns of genetic variation has been well studied in the Northern Hemisphere. However, although glaciation has undoubtedly shaped the genetic structure of plants in the Southern Hemisphere, fewer studies have characterized the effect, and almost none of them using microsatellites. Particularly, complex patterns of genetic structure might be expected in areas such as the Andes, where both latitudinal and altitudinal glacial advance and retreat have molded modern plant communities. We therefore studied the population genetics of three closely related, hybridizing species of Nothofagus (N. obliqua, N. alpina, and N. glauca, all of subgenus Lophozonia; Nothofagaceae) from Chile. To estimate population genetic parameters and infer the influence of the last ice age on the spatial and genetic distribution of these species, we examined and analyzed genetic variability at seven polymorphic microsatellite DNA loci in 640 individuals from 40 populations covering most of the ranges of these species in Chile. Populations showed no significant inbreeding and exhibited relatively high levels of genetic diversity (H_E = 0.502–0.662) and slight, but significant, genetic structure (R_ST = 8.7–16.0%). However, in N. obliqua, the small amount of genetic structure was spatially organized into three well‐defined latitudinal groups. Our data may also suggest some introgression of N. alpina genes into N. obliqua in the northern populations. These results allowed us to reconstruct the influence of the last ice age on the genetic structure of these species, suggesting several centers of genetic diversity for N. obliqua and N. alpina, in agreement with the multiple refugia hypothesis.     

A trait‐based approach to predict population genetic structure in bees

Understanding population genetic structure is key to developing predictions about species susceptibility to environmental change, such as habitat fragmentation and climate change. It has been theorized that life‐history traits may constrain some species in their dispersal and lead to greater signatures of population genetic structure. In this study, we use a quantitative comparative approach to assess if patterns of population genetic structure in bees are driven by three key species‐level life‐history traits: body size, sociality, and diet breadth. Specifically, we reviewed the current literature on bee population genetic structure, as measured by the differentiation indices Nei's G_ST, Hedrick's G′_ST, and Jost's D. We then used phylogenetic generalised linear models to estimate the correlation between the evolution of these traits and patterns of genetic differentiation. Our analyses revealed a negative and significant effect of body size on genetic structure, regardless of differentiation index utilized. For Hedrick's G′_ST and Jost's D, we also found a significant impact of sociality, where social species exhibited lower levels of differentiation than solitary species. We did not find an effect of diet specialization on population genetic structure. Overall, our results suggest that physical dispersal or other functions related to body size are among the most critical for mediating population structure for bees. We further highlight the importance of standardizing population genetic measures to more easily compare studies and to identify the most susceptible species to landscape and climatic changes.     

Host‐associated genomic differentiation in congeneric butterflies: now you see it,now you do not

Ecotypic variation among populations may become associated with widespread genomic differentiation, but theory predicts that this should happen only under particular conditions of gene flow, selection and population size. In closely related species, we might expect the strength of host‐associated genomic differentiation (HAD) to be correlated with the degree of phenotypic differentiation in host‐adaptive traits. Using microsatellite and Amplified Fragment Length Polymorphism (AFLP) markers, and controlling for isolation by distance between populations, we sought HAD in two congeneric species of butterflies with different degrees of host plant specialization. Prior work on Euphydryas editha had shown strong interpopulation differentiation in host‐adapted traits, resulting in incipient reproductive isolation among host‐associated ecotypes. We show here that Euphydryas aurinia had much weaker host‐associated phenotypic differentiation. Contrary to our expectations, we detected HAD in Euphydryas aurinia, but not in E. editha. Even within an E. aurinia population that fed on both hosts, we found weak but significant sympatric HAD that persisted in samples taken 9 years apart. The finding of significantly stronger HAD in the system with less phenotypic differentiation may seem paradoxical. Our findings can be explained by multiple factors, ranging from differences in dispersal or effective population size, to spatial variation in genomic or phenotypic traits and to structure induced by past histories of host‐adapted populations. Other infrequently measured factors, such as differences in recombination rates, may also play a role. Our result adds to recent work as a further caution against assumptions of simple relationships between genomic and adaptive phenotypic differentiation.     

Comparative phylogeographic study of Hosta sieboldiana and Hosta albomarginata (Asparagaceae) in Japan

We analyzed variations in chloroplast DNA (cpDNA) in the widespread herbaceous species Hosta sieboldiana and Hosta albomarginata across large portions of their geographic ranges in the Japanese archipelago. Our objective was to compare the phylogeographic histories and phylogeographic structures of the two congeneric species in the Japanese archipelago. The location of the study is Japanese archipelago. We sequenced 1380 bp of noncoding cpDNA from 45 populations of H. sieboldiana (n = 362) and 55 populations of H. albomarginata (n = 436) to assess genetic variations within and among populations across almost the entire distributions of the species in Japan. Extant patterns of geographic structure were analyzed using statistical parsimony networks and spatial analysis of molecular variance (SAMOVA). We also used Monmonier's algorithm to detect genetic barriers between regions. Relationships between the populations were examined using a neighbor‐joining (NJ) method. Four haplotypes were found for H. sieboldiana, whereas eight haplotypes were identified for H. albomarginata. Total genetic haplotype diversity (hT) and within‐population haplotype diversity (hS) for H. sieboldiana were 0.352 and 0.040, respectively, while the values for H. albomarginata were 0.529 and 0.085, respectively. The population differentiations (GST) for H. sieboldiana and H. albomarginata were 0.839 and 0.886, respectively. The SAMOVA analysis revealed two clusters in H. sieboldiana and four clusters in H. albomarginata. Differentiations between and among the clusters were supported by the BARRIER analysis and the NJ tree. We detected differences in the population genetic structure between the two species. We found that H. sieboldiana had lower haplotype diversity than H. albomarginata. These results may be partially explained by the difference in ecological habitats and geographic distributions between the species. Hosta albomarginata is more widely distributed than H. sieboldiana in East Asia including Russia, and this large distribution range would enable more chances to intraspecific gene flow.     

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.     

Predicting bird phenology from space: satellite‐derived vegetation green‐up signal uncovers spatial variation in phenological synchrony between birds and their environment

Population‐level studies of how tit species (Parus spp.) track the changing phenology of their caterpillar food source have provided a model system allowing inference into how populations can adjust to changing climates, but are often limited because they implicitly assume all individuals experience similar environments. Ecologists are increasingly using satellite‐derived data to quantify aspects of animals' environments, but so far studies examining phenology have generally done so at large spatial scales. Considering the scale at which individuals experience their environment is likely to be key if we are to understand the ecological and evolutionary processes acting on reproductive phenology within populations. Here, we use time series of satellite images, with a resolution of 240 m, to quantify spatial variation in vegetation green‐up for a 385‐ha mixed‐deciduous woodland. Using data spanning 13 years, we demonstrate that annual population‐level measures of the timing of peak abundance of winter moth larvae (Operophtera brumata) and the timing of egg laying in great tits (Parus major) and blue tits (Cyanistes caeruleus) is related to satellite‐derived spring vegetation phenology. We go on to show that timing of local vegetation green‐up significantly explained individual differences in tit reproductive phenology within the population, and that the degree of synchrony between bird and vegetation phenology showed marked spatial variation across the woodland. Areas of high oak tree (Quercus robur) and hazel (Corylus avellana) density showed the strongest match between remote‐sensed vegetation phenology and reproductive phenology in both species. Marked within‐population variation in the extent to which phenology of different trophic levels match suggests that more attention should be given to small‐scale processes when exploring the causes and consequences of phenological matching. We discuss how use of remotely sensed data to study within‐population variation could broaden the scale and scope of studies exploring phenological synchrony between organisms and their environment.