Ecological genetics of range size variation in Boechera spp. (Brassicaceae).
ABSTRACT: 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.
Project description:<h4>Background</h4>Genomic variation is widespread, and both neutral and selective processes can generate similar patterns in the genome. These processes are not mutually exclusive, so it is difficult to infer the evolutionary mechanisms that govern population and species divergence. Boechera stricta is a perennial relative of Arabidopsis thaliana native to largely undisturbed habitats with two geographic and ecologically divergent subspecies. Here, we delineate the evolutionary processes driving the genetic diversity and population differentiation in this species.<h4>Results</h4>Using whole-genome re-sequencing data from 517 B. stricta accessions, we identify four genetic groups that diverged around 30-180 thousand years ago, with long-term small effective population sizes and recent population expansion after the Last Glacial Maximum. We find three genomic regions with elevated nucleotide diversity, totaling about 10% of the genome. These three regions of elevated nucleotide diversity show excess of intermediate-frequency alleles, higher absolute divergence (d<sub>XY</sub>), and lower relative divergence (F<sub>ST</sub>) than genomic background, and significant enrichment in immune-related genes, reflecting long-term balancing selection. Scattered across the genome, we also find regions with both high F<sub>ST</sub> and d<sub>XY</sub> among the groups, termed F<sub>ST</sub>-islands. Population genetic signatures indicate that F<sub>ST</sub>-islands with elevated divergence, which have experienced directional selection, are derived from divergent sorting of ancient polymorphisms.<h4>Conclusions</h4>Our results suggest that long-term balancing selection on disease resistance genes may have maintained ancestral haplotypes across different geographical lineages, and unequal sorting of balanced polymorphisms may have generated genomic regions with elevated divergence. This study highlights the importance of ancestral balanced polymorphisms as crucial components of genome-wide variation.
Project description:The ability to respond to natural selection under novel conditions is critical for the establishment and persistence of introduced alien species and their ability to become invasive. Here we correlated neutral and quantitative genetic diversity of the weed Pennisetum setaceum Forsk. Chiov. (Poaceae) with differing global (North American and African) patterns of invasiveness and compared this diversity to native range populations. Numerous molecular markers indicate complete monoclonality within and among all of these areas (F(ST) = 0.0) and is supported by extreme low quantitative trait variance (Q(ST) = 0.00065-0.00952). The results support the general-purpose-genotype hypothesis that can tolerate all environmental variation. However, a single global genotype and widespread invasiveness under numerous environmental conditions suggests a super-genotype. The super-genotype described here likely evolved high levels of plasticity in response to fluctuating environmental conditions during the Early to Mid Holocene. During the Late Holocene, when environmental conditions were predominantly constant but extremely inclement, strong selection resulted in only a few surviving genotypes.
Project description:Widespread plant species are expected to maintain genetic diversity and gene flow via pollen and seed dispersal. Stature is a key life history trait that affects seed and potentially pollen dispersal, with limited stature associated with limited dispersal and greater genetic differentiation. We sampled Hill's tabletop wattle (<i>Acacia hilliana</i>) and curry wattle (<i>Acacia spondylophylla</i>), two co-distributed, widespread, <i>Acacia</i> shrubs of low stature, across the arid Pilbara region of north-western Australia. Using chloroplast sequence and nuclear microsatellite data we evaluated patterns of population genetic and phylogeographic diversity and structure, demographic signals, ratios of pollen to seed dispersal, evidence for historical refugia, and association between elevation and diversity. Results showed strong phylogeographic (chloroplast, <i>G</i> <sub>ST</sub> = 0.831 and 0.898 for <i>A. hilliana</i> and <i>A. spondylophylla</i>, respectively) and contemporary (nuclear, <i>F</i> <sub>ST</sub> = 0.260 and 0.349 for <i>A. hilliana</i> and <i>A. spondylophylla</i>, respectively) genetic structure in both species. This indicates limited genetic connectivity via seed and pollen dispersal associated with <i>Acacia</i> species of small stature compared to taller tree and shrub acacias across the Pilbara bioregion. This effect of stature on genetic structure is superimposed on moderate levels of genetic diversity that were expected based on widespread ranges (haplotype diversity <i>h</i> = 25 and 12; nuclear diversity <i>H</i>e = 0.60 and 0.47 for <i>A. hilliana</i> and <i>A. spondylophylla</i>, respectively). Contemporary genetic structure was congruent at the greater landscape scale, especially in terms of strong genetic differentiation among geographically disjunct populations in less elevated areas. Measures of diversity and connectivity were associated with traits of greater geographic population proximity, population density, population size, and greater individual longevity, and some evidence for range expansion in <i>A. hilliana</i>. Results illustrate that low stature is associated with limited dispersal and greater patterns of genetic differentiation for congenerics in a common landscape and highlight the complex influence of taxon-specific life history and ecological traits to seed and pollen dispersal.
Project description:Freshwater biodiversity has declined dramatically in Europe in recent decades. Because of massive habitat pollution and morphological degradation of water bodies, many once widespread species persist in small fractions of their original range. These range contractions are generally believed to be accompanied by loss of intraspecific genetic diversity, due to the reduction of effective population sizes and the extinction of regional genetic lineages. We aimed to assess the loss of genetic diversity and its significance for future potential reintroduction of the long-tailed mayfly Palingenia longicauda (Olivier), which experienced approximately 98% range loss during the past century. Analysis of 936 bp of mitochondrial DNA of 245 extant specimens across the current range revealed a surprisingly large number of haplotypes (87), and a high level of haplotype diversity (Hd = 0.875). In contrast, historic specimens (6) from the lost range (Rhine catchment) were not differentiated from the extant Rába population (F(ST) = 0.02, p = 0.61), despite considerable geographic distance separating the two rivers. These observations can be explained by an overlap of the current with the historic (Pleistocene) refugia of the species. Most likely, the massive recent range loss mainly affected the range which was occupied by rapid post-glacial dispersal. We conclude that massive range losses do not necessarily coincide with genetic impoverishment and that a species' history must be considered when estimating loss of genetic diversity. The assessment of spatial genetic structures and prior phylogeographic information seems essential to conserve once widespread species.
Project description:North American tree species, subspecies and genetic varieties have primarily evolved in a landscape of extensive continental ice and restricted temperate climate environments. Here, we reconstruct the refugial history of western North American trees since the last glacial maximum using species distribution models, validated against 3571 palaeoecological records. We investigate how modern subspecies structure and genetic diversity corresponds to modelled glacial refugia, based on a meta-analysis of allelic richness and expected heterozygosity for 473 populations of 22 tree species. We find that species with strong genetic differentiation into subspecies had widespread and large glacial refugia, whereas species with restricted refugia show no differentiation among populations and little genetic diversity, despite being common over a wide range of environments today. In addition, a strong relationship between allelic richness and the size of modelled glacial refugia (r(2) = 0.55) suggest that population bottlenecks during glacial periods had a pronounced effect on the presence of rare alleles.
Project description:A changing global climate can threaten the diversity of species and ecosystems. We explore the consequences of catastrophic disturbances in determining the evolutionary and demographic histories of secluded marble trout populations in Slovenian streams subjected to weather extremes, in particular recurrent flash floods and debris flows causing massive mortalities. Using microsatellite data, a pattern of extreme genetic differentiation was found among populations (global F(ST) of 0.716), which exceeds the highest values reported in freshwater fish. All locations showed low levels of genetic diversity as evidenced by low heterozygosities and a mean of only 2 alleles per locus, with few or no rare alleles. Many loci showed a discontinuous allele distribution, with missing alleles across the allele size range, suggestive of a population contraction. Accordingly, bottleneck episodes were inferred for all samples with a reduction in population size of 3-4 orders of magnitude. The reduced level of genetic diversity observed in all populations implies a strong impact of genetic drift, and suggests that along with limited gene flow, genetic differentiation might have been exacerbated by recurrent mortalities likely caused by flash flood and debris flows. Due to its low evolutionary potential the species might fail to cope with an intensification and altered frequency of flash flood events predicted to occur with climate change.
Project description:Boechera is a model genus that is of particular interest for understanding apomixis due to the presence of numerous apomictic diploid lineages that are tightly correlated with hybridisation events. Boechera includes many narrowly distributed endemics and apomictic hybrid lineages that obscure morphological boundaries amongst taxa. In this study, we focus on the Boechera suffrutescens complex, a phylogenetically well-supported but taxonomically complex north-western United States clade whose diploid species currently include the widespread B. suffrutescens and two narrowly distributed serpentine endemics, B. constancei and B. rollei. Using a 15-locus microsatellite dataset, we infer ploidy and sexual vs. apomictic reproduction for all individuals and then assess species limits for all sexual diploid samples. Our results support the recognition of B. rollei and B. constancei as distinct species and reveal three divergent sexual diploid lineages within B. suffrutescens sensu lato. The latter three lineages exhibit geographic, genetic and morphological coherence and consequently warrant recognition at the species rank. These include Boechera suffrutescens s.s., which is restricted to Idaho and eastern Oregon, Boechera botulifructa, a newly described species distributed along the Cascade Mountain Province from Lassen County, California north to Deschutes County, Oregon and the heretofore dismissed species Boechera duriuscula (basionym ? Arabis duriuscula), which occurs along the Sierra Nevada Province from Plumas County southwards to Fresno County, California. Our data also reveal substructure in B. constancei that is likely attributable to the highly fragmented distribution of its serpentine habitat. This refined taxonomic framework for the B. suffrutescens complex enhances Boechera as a model system, adds to our knowledge of speciation in edaphically extreme environments and provides information on ongoing conservation efforts for these taxa.
Project description:Populations in previously glaciated regions are often genetically depauperate in comparison with populations at lower latitudes, due either to bottlenecks experienced in post-glacial colonization or to contemporary genetic drift in small, peripheral populations. Populations of the rare self-fertilizing North American orchid Isotria medeoloides are largest in the previously glaciated region near the northern range limit, allowing us to examine the role of historical versus contemporary processes in determining population genetic diversity and structure. If contemporary processes predominate, genetic diversity should increase with increasing census size. In contrast, if sequential bottlenecks associated with colonization are paramount, diversity should decrease with latitude and be relatively insensitive to census size. We genotyped 299 individuals from 20 populations at four variable microsatellite loci to contrast genetic diversity and structure for populations in previously glaciated regions versus previously unglaciated regions. Populations were highly inbred (F=0.95) and highly differentiated (R(ST)=0.485). Across all sampled populations, genetic diversity decreased and genetic differentiation increased with declining population size. Small southern populations were especially differentiated and genetically depauperate. In the glaciated part of the range, genetic diversity increased as populations approached the northern range limit, demonstrating the centrality of contemporary processes for this post-glacial colonist.
Project description:The analysis of genetic structure and variability of isolated species is of critical importance in evaluating whether stochastic or human-caused factors are affecting rare species. Low genetic diversity compromises the ability of populations to evolve and reduces their chances of survival under environmental changes. Petunia secreta, a rare and endemic species, is an annual and heliophilous herb that is bee-pollinated and easily recognizable by its purple and salverform corolla. It was described as a new species of the Petunia genus in 2005. Few individuals of P. secreta have been observed in nature and little is known about this species. All the natural populations of P. secreta that were found were studied using 15 microsatellite loci, two intergenic plastid sequences and morphological traits. Statistical analysis was performed to describe the genetic diversity of this rare species and the results compared with those of more widespread and frequent Petunia species from the same geographic area to understand whether factors associated with population size could affect rare species of this genus. The results showed that despite its rarity, P. secreta presented high genetic diversity that was equivalent to or even higher than that of widespread Petunia species. It was shown that this species is divided into two evolutionary lineages, and the genetic differentiation indices between them and other congeneric species presented different patterns. The major risk to P. secreta maintenance is its rarity, suggesting the necessity of a preservation programme and more biological and evolutionary studies that handle the two evolutionary lineages independently.
Project description:Asexual reproduction is expected to reduce the adaptive potential to novel or changing environmental conditions, restricting or altering the ecological niche of asexual lineages. Asexual lineages of plants and animals are typically polyploid, an attribute that may influence their genetic variation, plasticity, adaptive potential, and niche breadth. The genus Boechera (Brassicaceae) represents an ideal model to test the relative ecological and biogeographic impacts of reproductive mode and ploidy because it is composed of diploid sexual and both diploid and polyploid asexual (i.e., apomictic) lineages. Here, we demonstrate a strong association between a transcriptionally conserved allele and apomictic seed formation. We then use this allele as a proxy apomixis marker in 1,649 accessions to demonstrate that apomixis is likely to be a common feature across the Boechera phylogeny. Phylogeographic analyses of these data demonstrate (i) species-specific niche differentiation in sexuals, (ii) extensive niche conservation between differing reproductive modes of the same species, (iii) ploidy-specific niche differentiation within and among species, and (iv) occasional niche drift between apomicts and their sexual ancestors. We conclude that ploidy is a substantially stronger and more common driver of niche divergence within and across Boechera species although variation in both traits may not necessarily lead to niche evolution on the species scale.