Global patterns of population genetic differentiation in seed plants

Evaluating the factors that drive patterns of population differentiation in plants is critical for understanding several biological processes such as local adaptation and incipient speciation. Previous studies have given conflicting results regarding the significance of pollination mode, seed dispersal mode, mating system, growth form and latitudinal region in shaping patterns of genetic structure, as estimated by F_ST values, and no study to date has tested their relative importance together across a broad scale. Here, we assembled a 337‐species data set for seed plants from publications with data on F_ST from nuclear markers and species traits, including variables pertaining to the sampling scheme of each study. We used species traits, while accounting for sampling variables, to perform phylogenetic multiple regressions. Results demonstrated that F_ST values were higher for tropical, mixed‐mating, non‐woody species pollinated by small insects, indicating greater population differentiation, and lower for temperate, outcrossing trees pollinated by wind. Among the factors we tested, latitudinal region explained the largest portion of variance, followed by pollination mode, mating system and growth form, while seed dispersal mode did not significantly relate to F_ST. Our analyses provide the most robust and comprehensive evaluation to date of the main ecological factors predicted to drive population differentiation in seed plants, with important implications for understanding the basis of their genetic divergence. Our study supports previous findings showing greater population differentiation in tropical regions and is the first that we are aware of to robustly demonstrate greater population differentiation in species pollinated by small insects.     

Drift happens: Molecular genetic diversity and differentiation among populations of jewelweed (Impatiens capensis Meerb.) reflect fragmentation of floodplain forests

Landscape features often shape patterns of gene flow and genetic differentiation in plant species. Populations that are small and isolated enough also become subject to genetic drift. We examined patterns of gene flow and differentiation among 12 floodplain populations of the selfing annual jewelweed (Impatiens capensis Meerb.) nested within four river systems and two major watersheds in Wisconsin, USA. Floodplain forests and marshes provide a model system for assessing the effects of habitat fragmentation within agricultural/urban landscapes and for testing whether rivers act to genetically connect dispersed populations. We generated a panel of 12,856 single nucleotide polymorphisms and assessed genetic diversity, differentiation, gene flow, and drift. Clustering methods revealed strong population genetic structure with limited admixture and highly differentiated populations (mean multilocus F_ST = 0.32, F_ST’ = 0.33). No signals of isolation by geographic distance or environment emerged, but alleles may flow along rivers given that genetic differentiation increased with river distance. Differentiation also increased in populations with fewer private alleles (R² = 0.51) and higher local inbreeding (R² = 0.22). Populations varied greatly in levels of local inbreeding (F_IS = 0.2–0.9) and F_IS increased in more isolated populations. These results suggest that genetic drift dominates other forces in structuring these Impatiens populations. In rapidly changing environments, species must migrate or genetically adapt. Habitat fragmentation limits both processes, potentially compromising the ability of species to persist in fragmented landscapes.     

Population genetics and breeding system of Tupistra pingbianensis (Liliaceae), a naturally rare plant endemic to SW China

The levels and partitioning of genetic diversity and inbreeding depression were investigated in Tupistra pingbianensis, a narrow endemic of South-east Yunnan, China, characterized by a naturally fragmented distribution due to extreme specialization on a rare habitat type. Here genetic diversity and patterns of genetic variation within and among 11 populations were analyzed using AFLP markers with 97 individuals across its whole geographical range. High levels of genetic variation were revealed both at the species level (P₉₉ = 96.012%; H_t = 0.302) and at the population level (P₉₉ = 51.41%; H_s = 0.224). Strong genetic differentiation among populations was also detected (F_ST = 0.2961; ⍬^嘦= 0.281), which corresponded to results reported for typical animal-pollinated, mixed selfing and outcrossing plant species. This result was consistent with mating patterns detected by our pollination experiments. The indirect estimate of gene flow based on ⍬^嘦 was low (N_m = 0.64). Special habitat and its life history traits may play an important role in shaping the genetic diversity and the genetic structure of this species. A pollination experiment also fail to detect significant inbreeding depression upon F₁ fruit set, seed weight and germinate rate fitness-traits. Since naturally rare species T. pingbianensis is not seriously genetically impoverished and likely to have adapted to tolerating a high level of inbreeding early in its history, we propose this species need only periodic monitoring to ensure their continued persistence but not intervention to remain viable.     

Combining multiple analytical approaches for the identification of population structure and genetic delineation of two subspecies of the endemic Arabian burnet moth Reissita simonyi (Zygaenidae; Lepidoptera)

Habitat fragmentation and landscape topology may influence the genetic structure and connectivity between natural populations. Six microsatellite loci were used to infer the population structure of 35 populations (N = 788) of the alpine Arabian burnet moth Reissita simonyi (Lepidoptera, Zygaenidae) in Yemen and Oman. Due to the patchy distribution of larval food plants, R. simonyi is not continuously distributed throughout the studied area and the two recognized subspecies of this endemic species (Reissita s. simonyi/R. s. yemenicola) are apparently discretely distributed. All microsatellites showed prevalence of null alleles and therefore a thorough investigation of the impact of null alleles on different population genetic parameters (F _ST, inbreeding coefficients, and Population Graph topologies) is given. In general, null alleles reduced genetic covariance and independence of allele frequencies resulting in a more connected genetic topology in Population Graphs and an overestimation of pairwise F _ST values and inbreeding coefficients. Despite the presence of null alleles, Population Graphs also showed a much higher genetic connectivity within subspecies (and lower genetic differentiation (via F _ST)) than between; supporting existing taxonomic distinction. Partial Mantel tests showed that both geographical distance and altitude were highly correlated with the observed distribution of genetic structure within R. simonyi. In conclusion, we identified geographical and altitudinal distances in R. simonyi as well as an intervening desert area to be the main factors for spatial genetic structure in this species and show that the taxonomic division into two subspecies is confirmed by genetic analysis.     

ESTIMATES OF INTRAGAMETOPHYTIC SELFING AND INTERPOPULATIONAL GENE FLOW IN HOMOSPOROUS FERNS

Relatively little information is available on mating systems and interpopulational gene flow in species of homosporous pteridophytes. Because of the proximity of antheridia and archegonia on the same thallus, it has long been maintained that intragametophytic selling is the predominant mode of reproduction in natural populations of homosporous ferns and other homosporous plants. Furthermore, quantitative estimates of interpopulational gene flow via spore dispersal are lacking. In this paper, we examine five species of homosporous ferns (Botrychium virginianum, Polystichum munitum, P. imbricans, Blechnum spicant, and Dryopteris expansa) and present estimates of 1) rates of intragametophytic selling, 2) levels of interpopulational gene flow, and 3) interpopulational genetic differentiation (F_ST). Our data demonstrate that mating systems vary among species of ferns, just as they do among species of seed plants. The data also suggest that levels of interpopulational gene flow are generally high. The F_ST values indicate little genetic divergence among populations for all species except Dryopteris expansa, which exhibits significant levels of interpopulational genetic differentiation. Patterns of genetic diversity in the five species examined are related to the mating system and rate of interpopulational gene flow in each species. The F_ST values for all species except Botrychium virginianum are in close agreement with those predicted for an island model of population structure.     

Emergent patterns of population genetic structure for a coral reef community

What shapes variation in genetic structure within a community of codistributed species is a central but difficult question for the field of population genetics. With a focus on the isolated coral reef ecosystem of the Hawaiian Archipelago, we assessed how life history traits influence population genetic structure for 35 reef animals. Despite the archipelago's stepping stone configuration, isolation by distance was the least common type of genetic structure, detected in four species. Regional structuring (i.e. division of sites into genetically and spatially distinct regions) was most common, detected in 20 species and nearly in all endemics and habitat specialists. Seven species displayed chaotic (spatially unordered) structuring, and all were nonendemic generalist species. Chaotic structure also associated with relatively high global F_ST. Pelagic larval duration (PLD) was not a strong predictor of variation in population structure (R² = 0.22), but accounting for higher F_ST values of chaotic and invertebrate species, compared to regionally structured and fish species, doubled the power of PLD to explain variation in global F_ST (adjusted R² = 0.50). Multivariate correlation of eight species traits to six genetic traits highlighted dispersal ability, taxonomy (i.e. fish vs. invertebrate) and habitat specialization as strongest influences on genetics, but otherwise left much variation in genetic traits unexplained. Considering that the study design controlled for many sampling and geographical factors, the extreme interspecific variation in spatial genetic patterns observed for Hawaìi marine species may be generated by demographic variability due to species‐specific abundance and migration patterns and/or seascape and historical factors.     

Phylogeography of Chinese cherry (Prunus pseudocerasus Lindl.) inferred from chloroplast and nuclear DNA: insights into evolutionary patterns and demographic history

Chinese cherry (Prunus pseudocerasus Lindl.) is a commercially valuable fruit crop in China. In order to obtain new insights into its evolutionary history and provide valuable recommendations for resource conservation, phylogeographic patterns of 26 natural populations (305 total individuals) from six geographic regions were analyzed using chloroplast and nuclear DNA fragments. Low levels of haplotype and nucleotide diversity were found in these populations, especially in landrace populations. It is likely that a combined effect of botanical characteristics impact the effective population size, such as inbreeding mating system, long life span, as well as vegetative reproduction. In addition, strong bottleneck effect caused by domestication, together with founder effect after dispersal and subsequent demographic expansion, might also accelerate the reduction of the genetic variation in landrace populations. Interestingly, populations from Longmen Mountain (LMM) and Daliangshan Mountain (DLSM) exhibited relatively higher levels of genetic diversity, inferring the two historical genetic diversity centers of the species. Moreover, moderate population subdivision was also detected by both chloroplast DNA (G_ST = 0.215; N_ST = 0.256) and nuclear DNA (G_ST = 0.146; N_ST = 0.342), respectively. We inferred that the episodes of efficient gene flow through seed dispersal, together with features of long generation cycle and inbreeding mating system, were likely the main contributors causing the observed phylogeographic patterns. Finally, factors that led to the present demographic patterns of populations from these regions and taxonomic varieties were also discussed.     

Inbreeding variability and population structure in the invasive haplodiploid palm‐seed borer (Coccotrypes dactyliperda)

We investigated the mating system and population genetic structure of the invasive haplodiploid palm‐seed borer Coccotrypes dactyliperda in California. We focused on whether these primarily inbreeding beetles have a ‘mixed‐breeding’ system that includes occasional outbreeding, and whether local inbreeding coefficients (F_IS) varied with dominant environmental factors. We also analysed the genetic structure of C. dactyliperda populations across local and regional scales. Based on the analysis of genetic variation at seven microsatellite loci in 1034 individual beetles from 59 populations, we found both high rates of inbreeding and plentiful evidence of mixed‐breeding. F_IS ranged from ?0.56 to 0.90, the highest variability reported within any animal species. There was a negative correlation between F_IS and latitude, suggesting that some latitude‐associated factor affecting mating decisions influenced inbreeding rates. Multiple regressions suggested that precipitation, but not temperature, may be an important correlate. Finally, we found highly significant genetic differentiation among sites, even over short geographic distances (< 1000 m).     

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

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

Familial social structure and socially driven genetic differentiation in Hawaiian short‐finned pilot whales

Social structure can have a significant impact on divergence and evolution within species, especially in the marine environment, which has few environmental boundaries to dispersal. On the other hand, genetic structure can affect social structure in many species, through an individual preference towards associating with relatives. One social species, the short‐finned pilot whale (Globicephala macrorhynchus), has been shown to live in stable social groups for periods of at least a decade. Using mitochondrial control sequences from 242 individuals and single nucleotide polymorphisms from 106 individuals, we examine population structure among geographic and social groups of short‐finned pilot whales in the Hawaiian Islands, and test for links between social and genetic structure. Our results show that there are at least two geographic populations in the Hawaiian Islands: a Main Hawaiian Islands (MHI) population and a Northwestern Hawaiian Islands/Pelagic population (F_ST and Φ_ST p < .001), as well as an eastern MHI community and a western MHI community (F_ST p = .009). We find genetically driven social structure, or high relatedness among social units and clusters (p < .001), and a positive relationship between relatedness and association between individuals (p < .0001). Further, socially organized clusters are genetically distinct, indicating that social structure drives genetic divergence within the population, likely through restricted mate selection (F_ST p = .05). This genetic divergence among social groups can make the species less resilient to anthropogenic or ecological disturbance. Conservation of this species therefore depends on understanding links among social structure, genetic structure and ecological variability within the species.     

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

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

Genetic diversity in fragmented populations of the critically endangered spider orchid Caladenia huegelii: implications for conservation

The Orchidaceae is characterised by a diverse range of life histories, reproductive strategies and geographic distribution, reflected in a variety of patterns in the population genetic structure of different species. In this study, the genetic diversity and structure was assessed within and among remnant populations of the critically endangered sexually deceptive orchid, Caladenia huegelii. This species has experienced severe recent habitat loss in a landscape marked by ancient patterns of population fragmentation within the Southwest Australian Floristic Region, a global biodiversity hotspot. Using seven polymorphic microsatellite loci, high levels of within-population diversity (mean alleles/locus = 6.73; mean H _E = 0.690), weak genetic structuring among 13 remnant populations (F _ST = 0.047) and a consistent deficit of heterozygotes from Hardy–Weinberg expectation were found across all populations (mean F _IS = 0.22). Positive inbreeding coefficients are most likely due to Wahlund effects and/or inbreeding effects from highly correlated paternity and typically low fruit set. Indirect estimates of gene flow (Nm = 5.09 using F _ST; Nm = 3.12 using the private alleles method) among populations reflects a historical capacity for gene flow through long distance pollen dispersal by sexually deceived wasp pollinators and/or long range dispersal of dust-like orchid seed. However, current levels of gene flow may be impacted by habitat destruction, fragmentation and reduced population size. A genetically divergent population was identified, which should be a high priority for conservation managers. Very weak genetic differentiation indicates that the movement and mixing of seeds from different populations for reintroduction programs should result in minimal negative genetic effects.     

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

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

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

Background and Aims

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

Methods

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

Key Results

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

Conclusions

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

Association between inbreeding depression and floral traits in a generalist‐pollinated plant

Individual variation in the magnitude of inbreeding depression (ID) in plants and its association with phenotypic traits may have important consequences for mating system evolution. This association has been investigated only scarcely, and always considering traits functionally related to autogamy. Here, we explore the association between individual variation in ID and plant traits associated with pollinator attractiveness (related to plant size, corolla size and corolla shape) in two populations of Erysimum mediohispanicum (Brassicaceae). ID was calculated along the entire life cycle of the plants. In addition, we also explored the relationship between phenotypic traits and the individual levels of heterozygosity. We found significant associations between ID and corolla diameter and stalk height, being taller plants with larger corollas those undergoing a lower intensity of ID. Furthermore, we found a negative relationship between corolla diameter and heterozygosity, suggesting that plants with large flowers have purged their genetic load. Finally, we found a significant effect of corolla diameter on the intrapopulation genetic structure. All these findings suggest that plants with large flowers have secularly suffered frequent inbreeding in the study populations. Because corolla diameter is a trait frequently selected by pollinators in E. mediohispanicum, we believe that the observed relationship between this trait and ID could be mediated by pollinators, probably throughout an increasing in biparental inbreeding, geitonogamy or autogamy.     

Genetic diversity of the black mangrove (Avicennia germinans L.) in Colombia

This study analyzed the genetic diversity and patterns of genetic structure in Colombian populations of Avicennia germinans L. using microsatellite loci. A lower genetic diversity was found on both the Caribbean (Ho = 0.439) and the Pacific coasts (Ho = 0.277) than reported for the same species in other locations of Central American Pacific, suggesting the deterioration of genetic diversity. All the populations showed high inbreeding coefficients (0.131–0.462) indicating heterozygotes deficience. The genetic structure between the Colombian coasts separated by Central American Isthmus was high (F_RT = 0.39) and the analyses of the genetic patterns of A. germinans revealed a clear differentiation of populations and no-recent gene flow evidence between coasts. Genetic structure was found within each coast (F_ST = 0.10 for the Caribbean coast and F_ST = 0.22 for the Pacific coast). The genetic patterns along the two coasts appear to reflect a forcing by local geomorphology and marine currents. Both coasts constitute a different Evolutionary Significant Unit, so we suggest for future transplantations plans that propagules or saplings of the populations of the Caribbean coast should not be mixed with those of the Pacific Colombian coast. Besides, we suggest that reforestation efforts should carefully distinguish propagules sources within each coast.     

POPULATION STRUCTURE AND KINSHIP IN POLISTES (HYMENOPTERA,VESPIDAE): AN ANALYSIS USING RIBOSOMAL DNA AND PROTEIN ELECTROPHORESIS

Six variable protein loci and one variable ribosomal DNA restriction site were used for an analysis of population structure in five species of Polistes from Texas. A sample-reuse algorithm was developed that estimated F_ST, F_IS, and ø (the coefficient of kinship) from probabilities of identity. Of the four species analyzed in detail only one, Polistes exclamans, had statistically significant values of F_ST. These values may reflect natural constraints on successful nesting for migrants of this species. Three of the four species had significant values of F_IS and three of the four species had significant values of ø. In many cases ø also differed from the expected value under haplodiploidy and random mating. Values of ø did not differ from expectations under haplodiploidy and local inbreeding. These results emphasize that theories of social behavior and evolution based on coefficients of kinship should include some explicit consideration of population structure.     

Inbreeding shapes the evolution of marine invertebrates

Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (F_IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in F_IS within invertebrates is related to the potential to self-fertilize, disperse, and choose mates. The similarity of F_IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F_IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.     

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.