James B. Beck

Native range genetic variation in Arabidopsis thaliana is strongly geographically structured and reflects Pleistocene glacial dynamics

Despite Arabidopsis thalianas pre‐eminence as a model organism, major questions remain regarding the geographic structure of its genetic variation due to the geographically incomplete sample set available for previous studies. Many of these questions are addressed here with an analysis of genome‐wide variation at 10 loci in 475 individuals from 167 globally distributed populations, including many from critical but previously un‐sampled regions. Rooted haplotype networks at three loci suggest that A. thaliana arose in the Caucasus region. Identification of large‐scale metapopulations indicates clear east–west genetic structure, both within proposed Pleistocene refugia and post‐Pleistocene colonized regions. The refugia themselves are genetically differentiated from one another and display elevated levels of within‐population genetic diversity relative to recolonized areas. The timing of an inferred demographic expansion coincides with the Eemian interglacial (approximately 120 000 years ago). Taken together, these patterns are strongly suggestive of Pleistocene range dynamics. Spatial autocorrelation analyses indicate that isolation by distance is pervasive at all hierarchical levels, but that it is reduced in portions of Europe.

A Diploids-First Approach to Species Delimitation and Interpreting Polyploid Evolution in the Fern Genus Astrolepis (Pteridaceae)

Abstract Polyploidy presents a challenge to those wishing to delimit the species within a group and reconstruct the phylogenetic relationships among these taxa. A clear understanding of the tree-like relationships among the diploid species can provide a framework upon which to reconstruct the reticulate events that gave rise to the polyploid lineages. In this study we apply this “diploids-first” strategy to the fern genus Astrolepis (Pteridaceae). Diploids are identified using the number of spores per sporangium and spore size. Analyses of plastid and low-copy nuclear sequence data provide well-supported estimates of phylogenetic relationships, including strong evidence for two morphologically distinctive diploid lineages not recognized in recent treatments. One of these corresponds to the type of Notholaena deltoidea, a species that has not been recognized in any modern treatment of Astrolepis. This species is resurrected here as the new combination Astrolepis deltoidea . The second novel lineage is that of a diploid initially hypothesized to exist by molecular and morphological characteristics of several established Astrolepis allopolyploids. This previously missing diploid species is described here as Astrolepis obscura.

DOES HYBRIDIZATION DRIVE THE TRANSITION TO ASEXUALITY IN DIPLOID BOECHERA

Gametophytic apomixis is a common form of asexual reproduction in plants. Virtually all gametophytic apomicts are polyploids, and some view polyploidy as a prerequisite for the transition to apomixis. However, any causal link between apomixis and polyploidy is complicated by the fact that most apomictic polyploids are allopolyploids, leading some to speculate that hybridization, rather than polyploidy, enables apomixis. Diploid apomixis presents a rare opportunity to isolate the role of hybridization, and a number of diploid apomicts have been documented in the genus Boechera (Brassicaceae). Here, we present the results of a microsatellite study of 1393 morphologically and geographically diverse diploid individuals, evaluating the hypothesis that diploid Boechera apomicts are hybrids. This genus‐wide dataset was made possible by the applicability of a core set of microsatellite loci in 69 of the 70 diploid Boechera species and by our ability to successfully genotype herbarium specimens of widely varying ages. With few exceptions, diploid apomicts exhibited markedly high levels of heterozygosity resulting from the combination of disparate genomes. This strongly suggests that most apomictic diploid Boechera lineages are of hybrid origin, and that the genomic consequences of hybridization allow for the transition to gametophytic apomixis in this genus.

DO ASEXUAL POLYPLOID LINEAGES LEAD SHORT EVOLUTIONARY LIVES? A CASE STUDY FROM THE FERN GENUS ASTROLEPIS

A life‐history transition to asexuality is typically viewed as leading to a heightened extinction risk, and a number of studies have evaluated this claim by examining the relative ages of asexual versus closely related sexual lineages. Surprisingly, a rigorous assessment of the age of an asexual plant lineage has never been published, although asexuality is extraordinarily common among plants. Here, we estimate the ages of sexual diploids and asexual polyploids in the fern genus Astrolepis using a well‐supported plastid phylogeny and a relaxed‐clock dating approach. The 50 asexual polyploid samples we included were conservatively estimated to comprise 19 distinct lineages, including a variety of auto‐ and allopolyploid genomic combinations. All were either the same age or younger than the crown group comprising their maternal sexual‐diploid parents based simply on their phylogenetic position. Node ages estimated with the relaxed‐clock approach indicated that the average maximum age of asexual lineages was 0.4 My, and individual lineages were on average 7 to 47 times younger than the crown‐ and total‐ages of their sexual parents. Although the confounding association between asexuality and polyploidy precludes definite conclusions regarding the effect of asexuality, our results suggest that asexuality limits evolutionary potential in Astrolepis.

Leavenworthia (Brassicaceae) Revisited: Testing Classic Systematic and Mating System Hypotheses

Abstract The genus Leavenworthia (Brassicaceae) has long been a focus of research on mating system evolution, due to the presence of both self-incompatible and self-compatible species within the genus. A phylogenetic hypothesis invoking multiple transitions between mating systems has been proposed for Leavenworthia, but this hypothesis has not been subject to molecular phylogenetic analysis. DNA sequence variation from four non-coding chloroplast regions (the trnL intron; and the trnT-trnL, trnL-trnF, and psbA-trnH intergenic spacers) was used to reconstruct the generic phylogeny, to test the validity of several proposed species, and to assess the number of mating system transitions within the genus. The strict consensus tree largely reflected the long-standing phylogenetic hypothesis for Leavenworthia, although additional data are needed to fully validate the recognition of L. crassa and L. alabamica. Unexpected results included the placement of L. uniflora as sister to the rest of the genus, and the apparent hybridization between L. exigua and L. torulosa. Finally, our data strongly supported a minimum of three mating system transitions within Leavenworthia.

Molecular Phylogenetics and Taxonomy of the Genus Boechera and Related Genera (Brassicaceae: Boechereae)

Abstract Boechera (Brassicaceae) is a diverse genus of ±70 sexual diploid species and numerous apomictic hybrids concentrated in western North America. It is the largest genus in tribe Boechereae, which also includes seven other small genera. Boechera is closely related to Arabidopsis and is becoming a model genus for diverse studies, focusing particularly on apomixis and hybrid speciation. As part of an ongoing effort to clarify the taxonomy of the group, we present phylogenetic analyses of Boechereae, including all genera of the tribe and most of the sexual diploid species of Boechera. Ten loci are used, including two plastid loci, nrDNA ITS, and seven low-copy nuclear loci. These analyses indicate that Boechera, as currently circumscribed, is polyphyletic, comprising three main clades. Eastern North American species previously assigned to Boechera form a distinct clade with the Asian taxon Borodinia macrophylla and are herein transferred to the genus Borodinia, resulting in seven new combinations (Borodinia burkii, Borodinia canadensis, Borodinia dentata, Borodinia laevigata, Borodinia missouriensis, Borodinia perstellata, and Borodinia serotina). Boechera repanda, a morphologically aberrant species endemic to the Sierra Nevada, is recognized in the new genus Yosemitea (as Yosemitea repanda). A primarily western North American clade comprising all remaining species is strongly supported and retains the name Boechera. Although resolution within Boechera sensu stricto is limited, a number of well-supported clades are identified.

Adaptation to warmer climates by parallel functional evolution of CBF genes in Arabidopsis thaliana

The evolutionary processes and genetics underlying local adaptation at a specieswide level are largely unknown. Recent work has indicated that a frameshift mutation in a member of a family of transcription factors, C‐repeat binding factors or CBFs, underlies local adaptation and freezing tolerance divergence between two European populations of Arabidopsis thaliana. To ask whether the specieswide evolution of CBF genes in Arabidopsis is consistent with local adaptation, we surveyed CBF variation from 477 wild accessions collected across the species’ range. We found that CBF sequence variation is strongly associated with winter temperature variables. Looking specifically at the minimum temperature experienced during the coldest month, we found that Arabidopsis from warmer climates exhibit a significant excess of nonsynonymous polymorphisms in CBF genes and revealed a CBF haplotype network whose structure points to multiple independent transitions to warmer climates. We also identified a number of newly described mutations of significant functional effect in CBF genes, similar to the frameshift mutation previously indicated to be locally adaptive in Italy, and find that they are significantly associated with warm winters. Lastly, we uncover relationships between climate and the position of significant functional effect mutations between and within CBF paralogs, suggesting variation in adaptive function of different mutations. Cumulatively, these findings support the hypothesis that disruption of CBF gene function is adaptive in warmer climates, and illustrate how parallel evolution in a transcription factor can underlie adaptation to climate.

Is subtribe Solidagininae (Asteraceae) monophyletic

As currently delimited, Solidagininae are a large (approximately 190 species) subtribe of tribe Astereae. Recent molecular and morphological studies have prompted a new definition of the subtribe, but the lack of absolutemorphological synapomorphies raises the possibility that this assemblage may not be monophyletic. Cladistic and likelihood-based analyses were conducted on a nuclear rDNA ITS sequence dataset derived from 23 of the 24 genera included in recent Solidagininae circumscriptions. Cladistic analyses identified two clades entirely composed of proposed Solidagininae genera. The data were not able to support deeper relationships, and these two clades might or might not form one monophyletic lineage. Topology testing indicated compatibility between the taxonomic definition of Solidagininae and molecular data.

Identifying multiple origins of polyploid taxa: A multilocus study of the hybrid cloak fern (Astrolepis integerrima; Pteridaceae)

PREMISE OF THE STUDY Molecular studies have shown that multiple origins of polyploid taxa are the rule rather than the exception. To understand the distribution and ecology of polyploid species and the evolutionary significance of polyploidy in general, it is important to delineate these independently derived lineages as accurately as possible. Although gene flow among polyploid lineages and backcrossing to their diploid parents often confound this process, such post origin gene flow is very infrequent in asexual polyploids. In this study, we estimate the number of independent origins of the apomictic allopolyploid fern Astrolepis integerrima, a morphologically heterogeneous species most common in the southwestern United States and Mexico, with outlying populations in the southeastern United States and the Caribbean. METHODS Plastid DNA sequence and AFLP data were obtained from 33 A. integerrima individuals. Phylogenetic analysis of the sequence data and multidimensional clustering of the AFLP data were used to identify independently derived lineages. KEY RESULTS Analysis of the two datasets identified 10 genetic groups within the 33 analyzed samples. These groups suggest a minimum of 10 origins of A. integerrima in the northern portion of its range, with both putative parents functioning as maternal donors, both supplying unreduced gametes, and both contributing a significant portion of their genetic diversity to the hybrids. CONCLUSIONS Our results highlight the extreme cryptic genetic diversity and systematic complexity that can underlie a single polyploid taxon.

Weaving a Tangled Web: Divergent and Reticulate Speciation in Boechera fendleri Sensu Lato (Brassicaceae: Boechereae)

Abstract Hybrid speciation is relatively common in plants compared to other well-studied groups. Polyploidy and apomixis are strongly associated with hybrid speciation, presumably due to the opportunities they provide for both reestablishing reproductive function in hybrids with incomplete chromosomal homology and creating rapid reproductive isolation in sympatry. Boechera, a species-rich genus closely related to Arabidopsis, is a particularly fertile ground for the study of hybrid speciation. Thirty-eight apomictic triploid hybrid species are currently recognized in Boechera. Recent research has shown that apomictic diploid hybrids, although very rare in angiosperms, are common in Boechera. Given this complexity, focused studies of individual species complexes are critical to understanding speciation and diagnosing biodiversity in Boechera. Here we analyze DNA sequences from seven nuclear loci and multilocus genotypes from 15 microsatellite markers in a group of closely related taxa formerly included in B. fendleri. Our results support the recognition of four species previously segregated from B. fendleri s. l., including three genetically distinct, sexual diploids (B. fendleri, B. spatifolia, and B. texana) and one apomictic triploid hybrid (B. porphyrea). We also identify four novel apomictic diploid hybrid species (B. carrizozoensis, B. centrifendleri, B. sanluisensis, and B. zephyra) and additional apomictic triploid hybrids. Our results reveal a complex network of relationships. Sexual diploid species can hybridize to form apomictic diploids, and members of these two groups can hybridize to form trigenomic, apomictic triploids.