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Oligoryzomys flavescens (Rodentia, Muridae): gene flow among populations from central-eastern Argentina.

In species acting as hosts of infectious agents, the extent of gene flow between populations is of particular interest because the expansion of different infectious diseases is usually related to the dispersal of the host. We have estimated levels of gene flow among populations of the sigmodontine rodent Oligoryzomys flavescens, in which high titers of antibodies have been detected for a Hantavirus in Argentina that produces a severe pulmonary syndrome. Enzyme polymorphism was studied by means of starch gel electrophoresis in 10 populations from the area where human cases of Hantavirus have occurred. Genetic differentiation between populations was calculated from FST values with the equation Nm = [(1/FST) - 1]/4. To assess the relative importance of current gene flow and historical associations between populations, the relationship of population pairwise log Nm and log geographic distance was examined. Low FST (mean = 0.038) and high Nm (15.27) values suggest high levels of gene flow among populations. The lack of an isolation by distance pattern would indicate that this species has recently colonized the area. The northernmost population, located on the margin of a great river, shows very high levels of gene flow with the downstream populations despite the large geographic distances. Passive transport of animals down the river by floating plants would promote unidirectional gene flow. This fact and the highest mean heterozygosity of that northernmost population suggest it is a center of dispersal within the species' range.

Animals↗

Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking-sticks.

Population differentiation often reflects a balance between divergent natural selection and the opportunity for homogenizing gene flow to erode the effects of selection. However, during ecological speciation, trait divergence results in reproductive isolation and becomes a cause, rather than a consequence, of reductions in gene flow. To assess both the causes and the reproductive consequences of morphological differentiation, we examined morphological divergence and sexual isolation among 17 populations of Timema cristinae walking-sticks. Individuals from populations adapted to using Adenostoma as a host plant tended to exhibit smaller overall body size, wide heads, and short legs relative to individuals using Ceonothus as a host. However, there was also significant variation in morphology among populations within host-plant species. Mean trait values for each single population could be reliably predicted based upon host-plant used and the potential for homogenizing gene flow, inferred from the size of the neighboring population using the alternate host and mitochondrial DNA estimates of gene flow. Morphology did not influence the probability of copulation in between-population mating trials. Thus, morphological divergence is facilitated by reductions in gene flow, but does not cause reductions in gene flow via the evolution of sexual isolation. Combined with rearing data indicating that size and shape have a partial genetic basis, evidence for parallel origins of the host-associated forms, and inferences from functional morphology, these results indicate that morphological divergence in T. cristinae reflects a balance between the effects of host-specific natural selection and gene flow. Our findings illustrate how data on mating preferences can help determine the causal associations between trait divergence and levels of gene flow.

Adaptation, Biological↗

Comparing relative rates of pollen and seed gene flow in the island model using nuclear and organelle measures of population structure.

We describe a method for comparing nuclear and organelle population differentiation (F(ST)) in seed plants to test the hypothesis that pollen and seed gene flow rates are equal. Wright's infinite island model is used, with arbitrary levels of self-fertilization and biparental organelle inheritance. The comparison can also be applied to gene flow in animals. Since effective population sizes are smaller for organelle genomes than for nuclear genomes and organelles are often uniparentally inherited, organelle F(ST) is expected to be higher at equilibrium than nuclear F(ST) even if pollen and seed gene flow rates are equal. To reject the null hypothesis of equal seed and pollen gene flow rates, nuclear and organelle F(ST)'s must differ significantly from their expected values under this hypothesis. Finite island model simulations indicate that infinite island model expectations are not greatly biased by finite numbers of populations (>/=100 subpopulations). The power to distinguish dissimilar rates of pollen and seed gene flow depends on confidence intervals for fixation index estimates, which shrink as more subpopulations and loci are sampled. Using data from the tropical tree Corythophora alta, we rejected the null hypothesis that seed and pollen gene flow rates are equal but cannot reject the alternative hypothesis that pollen gene flow is 200 times greater than seed gene flow.

Genetics, Population↗

Using genetic markers to directly estimate gene flow and reproductive success parameters in plants on the basis of naturally regenerated seedlings.

Estimating seed and pollen gene flow in plants on the basis of samples of naturally regenerated seedlings can provide much needed information about "realized gene flow," but seems to be one of the greatest challenges in plant population biology. Traditional parentage methods, because of their inability to discriminate between male and female parentage of seedlings, unless supported by uniparentally inherited markers, are not capable of precisely describing seed and pollen aspects of gene flow realized in seedlings. Here, we describe a maximum-likelihood method for modeling female and male parentage in a local plant population on the basis of genotypic data from naturally established seedlings and when the location and genotypes of all potential parents within the population are known. The method models female and male reproductive success of individuals as a function of factors likely to influence reproductive success (e.g., distance of seed dispersal, distance between mates, and relative fecundity--i.e., female and male selection gradients). The method is designed to account for levels of seed and pollen gene flow into the local population from unsampled adults; therefore, it is well suited to isolated, but also wide-spread natural populations, where extensive seed and pollen dispersal complicates traditional parentage analyses. Computer simulations were performed to evaluate the utility and robustness of the model and estimation procedure and to assess how the exclusion power of genetic markers (isozymes or microsatellites) affects the accuracy of the parameter estimation. In addition, the method was applied to genotypic data collected in Scots pine (isozymes) and oak (microsatellites) populations to obtain preliminary estimates of long-distance seed and pollen gene flow and the patterns of local seed and pollen dispersal in these species.

Computer Simulation↗

Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis).

The traditional view of the species as the fundamental unit of evolution has been challenged by observations that in heterogeneous environments, gene flow may be too restricted to overcome the effects of local selection. Whether a species evolves as a cohesive unit depends critically on the dynamic balance between homogenizing gene flow among populations and potentially disruptive local adaptation. To examine this evolutionary balance between "global" gene flow and local selection, we studied northern Californian populations of Helianthus exilis, the serpentine sunflower, within a mosaic of contrasting serpentine and nonserpentine areas that differ considerably in soil chemistry and water availability. Local adaptation to riparian and serpentine habitats was studied in Helianthus exilis along with an analysis of gene flow patterns among populations within these habitats. Local adaptation was assessed in H. exilis during 2002 and 2003 using reciprocal transplant experiments at multiple locations within serpentine and riparian habitats. Effects of competition and germination date on the expression of local adaptation were also examined within the reciprocal transplant experiments. Local adaptation was detected in both years at the local site level and at the level of habitat. The analysis of the transplanted populations indicated that the patterns of selection differed considerably between riparian and serpentine sites. Differential survivorship occurred in serpentine habitats, whereas selection on reproductive output predominated in riparian habitats. Local adaptation was expressed only in the absence of competition. Local adaptation in terms of survivorship was most strongly expressed in treatments with delayed seed germination. Microsatellite markers were used to quantify population genetic parameters and examine the patterns of gene flow among sampled populations. Analysis of molecular markers revealed a system of population patches that freely exchange genes with each other. Strong selection seems to maintain ecotypic variation within this endemic sunflower species, while extensive gene flow among populations prevents local speciation between serpentine and riparian ecotypes.

Adaptation, Physiological↗

Phylogeographic breaks without geographic barriers to gene flow.

The spatial distribution of genetic markers can be useful both in estimating patterns of gene flow and in reconstructing biogeographic history, particularly when gene genealogies can be estimated. Genealogies based on nonrecombining genetic units such as mitochondrial and chloroplast DNA often consist of geographically separated clades that come into contact in narrow regions. Such phylogeographic breaks are usually assumed to be the result of long-term barriers to gene flow. Here I show that deep phylogeographic breaks can form within a continuously distributed species even when there are no barriers to gene flow. The likelihood of observing phylogeographic breaks increases as the average individual dispersal distance and population size decrease. Those molecular markers that are most likely to show evidence of real geographic barriers are also most likely to show phylogeographic breaks that formed without any barrier to gene flow. These results might provide an explanation as to why some species, such as the greenish warblers (Phylloscopus trochiloides), have phylogeographic breaks in mitochondrial or chloroplast DNA that do not coincide with sudden changes in other traits.

Animals↗

Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker.

Sampling methods and results of a gene flow study are described that will be of interest to plant scientists, evolutionary biologists, ecologists, and stakeholders assessing the environmental safety of transgenic crops. This study documents gene flow on a landscape level from creeping bentgrass (Agrostis stolonifera L.), one of the first wind-pollinated, perennial, and highly outcrossing transgenic crops being developed for commercial use. Most of the gene flow occurred within 2 km in the direction of prevailing winds. The maximal gene flow distances observed were 21 km and 14 km in sentinel and resident plants, respectively, that were located in primarily nonagronomic habitats. The selectable marker used in these studies was the CP4 EPSPS gene derived from Agrobacterium spp. strain CP4 that encodes 5-enol-pyruvylshikimate-3-phosphate synthase and confers resistance to glyphosate herbicide. Evidence for gene flow to 75 of 138 sentinel plants of A. stolonifera and to 29 of 69 resident Agrostis plants was based on seedling progeny survival after spraying with glyphosate in greenhouse assays and positive TraitChek, PCR, and sequencing results. Additional studies are needed to determine whether introgression will occur and whether it will affect the ecological fitness of progeny or the structure of plant communities in which transgenic progeny may become established.

3-Phosphoshikimate 1-Carboxyvinyltransferase↗

Gene flow among Cydia pomonella (Lepidoptera: Tortricidae) geographic and host populations in South Africa.

Information on gene flow among geographic and host populations of C. pomonella (L.) (Lepidoptera: Tortricidae) in South Africa is lacking, despite the importance of these measures for the success of control practices such as chemical control and sterile insect release, which are affected by the amount of gene flow among populations. Therefore, populations collected from nine geographically distant regions in South Africa from apples, pears, and stone fruit were compared using amplified fragment length polymorphism with five selective primer pairs. Results showed that although populations from different hosts were not genetically differentiated, significant evidence for population substructure was apparent between geographic populations. Over local scales, it was possible to distinguish between populations collected from orchards situated <1 km apart. These results suggest that although extensive gene flow occurs among populations from different hosts, gene flow among local geographic C. pomonella populations may be limited and is explained in terms of limited moth flight, the relative isolation of pome fruit production areas, and the absence of wild hosts.

Animals↗

How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles.

The traditional view that species are held together through gene flow has been challenged by observations that migration is too restricted among populations of many species to prevent local divergence. However, only very low levels of gene flow are necessary to permit the spread of highly advantageous alleles, providing an alternative means by which low-migration species might be held together. We re-evaluate these arguments given the recent and wide availability of indirect estimates of gene flow. Our literature review of F(ST) values for a broad range of taxa suggests that gene flow in many taxa is considerably greater than suspected from earlier studies and often is sufficiently high to homogenize even neutral alleles. However, there are numerous species from essentially all organismal groups that lack sufficient gene flow to prevent divergence. Crude estimates on the strength of selection on phenotypic traits and effect sizes of quantitative trait loci (QTL) suggest that selection coefficients for leading QTL underlying phenotypic traits may be high enough to permit their rapid spread across populations. Thus, species may evolve collectively at major loci through the spread of favourable alleles, while simultaneously differentiating at other loci due to drift and local selection.

Adaptation, Biological↗

Long-distance gene flow in a cooperative breeder detected in genealogies of mitochondrial DNA sequences.

Rates of gene flow among populations of cooperatively breeding birds have been inferred primarily from distributions of observed distances of dispersal from birthplace to place of first breeding. However, for most cooperative breeders, characteristics of geographic population structure and extent of realized gene flow as measured by genetic markers are not known. To estimate rates of gene flow in a cooperatively breeding bird, I conducted a continent-wide survey of DNA sequence diversity in the most variable part of the mitochondrial (mt) genome among 163 grey-crowned babblers (Pomatostomus temporalis) throughout Australia and Papua New Guinea. The variability found among 86 types of mtDNA was used to infer genealogical trees relating sequences within both eastern (P. t. temporalis) and western (P. t. rubeculus) babblers. The genealogies imply low but detectable levels of gene flow between populations separated by over 1000 km. In addition, they suggest that genes from unrelated migrants contribute to genetic diversity in 5 of 50 (10%) social groups, occasionally producing large (> 3%) intragroup sequence differences. However, on average, the fraction of sequence diversity apportioned among populations (Fst) and among social groups within populations (Fgs), was substantial for both P. t. temporalis and P t. rubeculus, implying a large opportunity for the spread of social behaviours in both lineages of babblers.

Animals↗

A role for nonphysical barriers to gene flow in the diversification of a highly vagile seabird, the masked booby (Sula dactylatra).

To test the hypothesis that nonphysical barriers to gene flow play a role in the divergence of low-latitude seabird populations, we applied phylogeographic methods to mitochondrial control region sequence variation in a global sample of masked boobies (Sula dactylatra). In accord with previous studies, we found that Indo-Pacific and Atlantic haplotypes form two divergent lineages, excluding one haplotype previously attributed to secondary contact between the Indian Ocean and the Caribbean Sea. Within the Indo-Pacific and the Atlantic, we found a relatively large number of haplotypes, many of which were unique to a single population. Although haplotypes from most populations were found in more than one higher-level clade, nested clade analysis revealed a significant association between clades and geography for the majority of higher-level clades, most often interpreted as a consequence of isolation by distance. We found low levels of gene flow within Indo-Pacific and Atlantic populations, and a significant correlation between gene flow and geographical distance among Indo-Pacific populations. We estimate that Indo-Pacific masked boobies experienced rapid population growth approximately 180,000 years ago and that the majority of Indo-Pacific and Atlantic populations diverged within the last approximately 115,000 years. These combined data suggest that the predominant pattern between Indo-Pacific and Atlantic populations is long-term isolation by physical barriers to gene flow. In contrast, populations within these regions appear to have diverged despite few obvious physical barriers to gene flow, perhaps as a consequence of limited natal dispersal combined with local adaptation and/or genetic drift.

Animals↗

Patterns and levels of gene flow in Rhododendron metternichii var. hondoense revealed by microsatellite analysis.

Parentage analysis was conducted to elucidate the patterns and levels of gene flow in Rhododendron metternichii Sieb. et Zucc. var. hondoense Nakai in a 150 x 70 m quadrant in Hiroshima Prefecture, western Japan. The population of R. metternichii occurred as three subpopulations at the study site. Seventy seedlings were randomly collected from each of three 10 x 10 m plots (S1, S2, and S3) on the forest floor of each subpopulation (A1, A2, and A3). Almost all parents (93.8%) of the 70 seedlings were unambiguously identified by using 12 pairs of microsatellite markers. Within the quadrant, adult trees less than 5 m from the centre of the seedling bank (plots S1, S2, and S3) produced large numbers of seedlings. The effects of tree height and distance from the seedling bank on the relative fertilities of adult trees were highly variable among subpopulations because of the differences in population structure near the seedling bank: neither distance nor tree height had any significant effect in subpopulation A1; distance from the seedling bank had a significant effect in subpopulation A2; and tree height had a significant effect in subpopulation A3. Although gene flow within each subpopulation was highly restricted to less than 25 m and gene flow among the three subpopulations was extremely small (0-2%), long-distance gene flow from outside the quadrant reached 50%. This long-distance gene flow may be caused by a combination of topographical and vegetational heterogeneity, differences in flowering phenology, and genetic substructuring within subpopulations.

DNA, Plant↗

A study of crop-to-crop gene flow using farm scale sites of fodder maize (Zea mays L.) in the UK.

From 2000 to 2003 a range of Farm Scale Evaluation (FSE) trials were established in the UK to assess the effect of the release and management of herbicide tolerant (HT) crops on arable weeds and invertebrates. The FSE trials for maize were also used to investigate crop-to-crop gene flow and to develop a statistical model for the prediction of gene flow frequency that can be used to evaluate current separation distance guidelines for GM crops. Seed samples were collected from the non-GM half of 55 trial sites and 1,055 were tested for evidence of gene flow from the GM HT halves using a quantitative PCR assay specific to the HT (pat) gene. Rates of gene flow were found to decrease rapidly with increasing distance from the GM source. Gene flow was detected in 30% of the samples (40 out of 135) at 150 m from the GM source and events of GM to non-GM gene flow were detected at distances up to and including 200 m from the GM source. The quantitative data were subjected to statistical analysis and a two-step model was found to provide the best fit for the data. A dynamic whole field model predicted that a square field (150 m x 150 m in size) of grain maize would require a separation distance of 3 m for the adjacent crop to be below a 0.9% threshold (with <2% probability of exceeding the threshold). The data and models presented here are discussed in the context of necessary separation distances to achieve various possible thresholds for adventitious presence of GM in maize.

Agriculture↗

Parentage versus two-generation analyses for estimating pollen-mediated gene flow in plant populations.

Assessment of contemporary pollen-mediated gene flow in plants is important for various aspects of plant population biology, genetic conservation and breeding. Here, through simulations we compare the two alternative approaches for measuring pollen-mediated gene flow: (i) the NEIGHBORHOOD model--a representative of parentage analyses, and (ii) the recently developed TWOGENER analysis of pollen pool structure. We investigate their properties in estimating the effective number of pollen parents (N(ep)) and the mean pollen dispersal distance (delta). We demonstrate that both methods provide very congruent estimates of N(ep) and delta, when the methods' assumptions considering the shape of pollen dispersal curve and the mating system follow those used in data simulations, although the NEIGHBORHOOD model exhibits generally lower variances of the estimates. The violations of the assumptions, especially increased selfing or long-distance pollen dispersal, affect the two methods to a different degree; however, they are still capable to provide comparable estimates of N(ep). The NEIGHBORHOOD model inherently allows to estimate both self-fertilization and outcrossing due to the long-distance pollen dispersal; however, the TWOGENER method is particularly sensitive to inflated selfing levels, which in turn may confound and suppress the effects of distant pollen movement. As a solution we demonstrate that in case of TWOGENER it is possible to extract the fraction of intraclass correlation that results from outcrossing only, which seems to be very relevant for measuring pollen-mediated gene flow. The two approaches differ in estimation precision and experimental efforts but they seem to be complementary depending on the main research focus and type of a population studied.

Computer Simulation↗

Testing for asymmetrical gene flow in a Drosophila melanogaster body-size cline.

Asymmetrical gene flow is an important, but rarely examined genetic parameter. Here, we develop a new method for detecting departures from symmetrical migration between two populations using microsatellite data that are based on the difference in the proportion of private alleles. Application of this approach to data collected from wild-caught Drosophila melanogaster along a latitudinal body-size cline in eastern Australia revealed that asymmetrical gene flow could be detected, but was uncommon, nonlocalized, and occurred in both directions. We also show that, in contrast to the findings of a previous study, there is good evidence to suggest that the cline experiences significant levels of gene flow between populations.

Animals↗

Speciation despite gene flow when developmental pathways evolve.

Evolutionary biologists assume that species formation requires a drastic reduction in gene exchange between populations, but the rate sufficient to prevent speciation is unknown. To study speciation, we use a new class of population genetic models that incorporate simple developmental genetic rules, likely present in all organisms, to construct the phenotype. When we allow replicate populations to evolve in parallel to a new, shared optimal phenotype, often their hybrids acquire poorly regulated phenotypes: Dobzhansky-Muller incompatibilities arise and postzygotic reproductive isolation evolves. Here we show that, although gene exchange does inhibit this process, it is the proportion of migrants exchanged (m) rather than the number of migrants (Nm) that is critical, and rates as high as 16 individuals exchanged per generation still permit the evolution of postzygotic isolation. Stronger directional selection counters the inhibitory effect of gene flow, increasing the speciation probability. We see similar results when populations in a standard two-locus, two-allele Dobzhansky-Muller model are subject to simultaneous directional selection and gene flow. However, in developmental pathway models with more than two loci, gene flow is more able to impede speciation. Genetic incompatibilities arise as frequent by-products of adaptive evolution of traits determined by regulatory pathways, something that does not occur when phenotypes are modeled using the standard, additive genetic framework. Development therefore not only constrains the microevolutionary process, it also facilitates the interactions among genes and gene products that make speciation more likely-even in the face of strong gene flow.

Animals↗

Isozyme allelic frequencies related to selection and gene-flow hypotheses.

Significant correlations between allelic frequencies and environmental variables in a number of insect species have been demonstrated by multivariate techniques. Since many environmental variables show a strong relationship to geographic location and since gene flow between populations can also produce patterns of gene frequencies which are related to the geographic location, both selection and gene-flow hypotheses are consistent with the observed correlations. The genetic variables can be corrected for geographic location and so for linear gene-flow patterns. If, after correction, the genetic variables still show significant correlations with similarly corrected environmental variables, then these correlations are consistent with hypotheses of selection but not of gene flow. The data of Johnson and Schaffer (1973) have been reanalyzed using the method of canonical correlation after correction for geographical location by means of multiple regression. Five of the nine loci studied exhibit significant canonical correlations. These results, under the assumption of linear gene flow, support hypotheses of selective action of environmental variables in the genotype-environment relationships observed.

Alleles↗

Genetic Differentiation is Constrained to Chromosomal Inversions and Putative Centromeres in Locally Adapted Populations With Higher Gene Flow.

The impact of genome structure on adaptation is a growing focus in evolutionary biology, revealing an important role for structural variation and recombination landscapes in shaping genetic diversity across genomes and among populations. This is particularly relevant when local adaptation occurs despite gene flow, where clustering of differentiated loci can maintain locally adapted variants by reducing recombination between them. However, the limited genomic resources for nonmodel species, including reference genomes and recombination maps, have constrained our understanding of these patterns. In this study, we leverage the Atlantic silverside-a nonmodel fish with extensive local adaptation across a steep latitudinal gradient-as an ideal system to explore how genome structure influences adaptation under varying levels of gene flow, using a newly available reference genome and multiple recombination maps. Analyzing 168 genomes from four populations, we found a continuum of genome-wide differentiation increasing from south to north, reflecting higher connectivity among southern populations and reduced gene flow at northern latitudes. With increasing gene flow, the number and clustering of FST outlier loci also increased, with differentiated loci found exclusively within large haploblocks harboring inversions and smaller peaks overlapping putative centromeric regions. Notably, sequence divergence was only evident in inversions, supporting their role in adaptive divergence with gene flow, whereas centromeric regions appeared differentiated because of low recombination and diversity, with no indication of elevated divergence. Our results support the hypothesis that clustered genomic architectures evolve with high gene flow and enhance our understanding of how inversions and centromeres are linked to different evolutionary processes.

Gene Flow↗