Hybrid enrichment of adaptive variation revealed by genotype-environment associations in montane sedges.

The role of hybridization in diversification is complex and may result in many possible outcomes. Not only can hybridization produce new lineages, but those lineages may contain unique combinations of adaptive genetic variation derived from parental taxa that allow hybrid-origin lineages to occupy unique environmental space relative to one (or both) parent(s). We document such a case of hybridization between two sedge species, Carex nova and Carex nelsonii (Cyperaceae), that occupy partially overlapping environmental space in the southern Rocky Mountains, USA. In the region hypothesized to be the origin of the hybrid lineage, one parental taxon (C. nelsonii) is at the edge of its environmental tolerance. Hybrid-origin individuals display mixed ancestry between the parental taxa-of nearly 7000 unlinked loci sampled, almost 30% showed evidence of excess ancestry from one parental lineage-approximately half displayed a genomic background skewed towards one parent, and half skewed towards the other. To test whether excess ancestry loci may have conferred an adaptive advantage to the hybrid-origin lineage, we conducted genotype-environment association analyses on different combinations of loci-with and without excess ancestry-and with multiple contrasts between the hybrids and parental taxa. Loci with skewed ancestry showed significant environmental associations distinguishing the hybrid lineage from one parent (C. nelsonii), whereas loci with relatively equal representation of parental ancestries showed no such environmental associations. Moreover, the overwhelming majority of candidate adaptive loci with respect to environmental gradients also had excess ancestry from a parental lineage, implying these loci have facilitated the persistence of the hybrid lineage in an environment unsuitable to at least one parent.

Testing which axes of species differentiation underlie covariance of phylogeographic similarity among montane sedge species.

Co-distributed species may exhibit similar phylogeographic patterns due to shared environmental factors or discordant patterns attributed to the influence of species-specific traits. Although either concordant or discordant patterns could occur due to chance, stark differences in key traits (e.g., dispersal ability) may readily explain differences between species. Multiple species' attributes may affect genetic patterns, and it is difficult to isolate the contribution of each. Here we compare the relative importance of two attributes, range size, and niche breadth, in shaping the spatial structure of genetic variation in four sedge species (genus Carex) from the Rocky Mountains. Within two pairs of co-distributed species, one species exhibits narrow niche breadth, while the other species has broad niche breadth. Furthermore, one pair of co-distributed species has a large geographical distribution, while the other has a small distribution. The four species represent a natural experiment to tease apart how these attributes (i.e., range size and niche breadth) affect phylogeographic patterns. Investigations of genetic variation and structure revealed that range size, but not niche breadth, is related to spatial genetic covariation across species of montane sedges. Our study highlights how isolating key attributes across multiple species can inform their impact on processes driving intraspecific differentiation.

Population history provides foundational knowledge for utilizing and developing native plant restoration materials.

A species' population structure and history are critical pieces of information that can help guide the use of available native plant materials in restoration treatments and decide what new native plant materials should be developed to meet future restoration needs. In the western United States, Pseudoroegneria spicata (bluebunch wheatgrass; Poaceae) is an important component of grassland and shrubland plant communities and commonly used for restoration due to its drought resistance and competitiveness with exotic weeds. We used next-generation sequencing data to investigate the processes that shaped P. spicata's geographic pattern of genetic variation across the Intermountain West. Pseudoroegneria spicata's genetic diversity is partitioned into populations that likely differentiated since the Last Glacial Maximum. Adjacent populations display varying magnitudes of historical gene flow, with migration rates ranging from multiple migrants per generation to multiple generations per migrant. When considering the commercial germplasm sources available for restoration, genetic identities remain representative of the wildland localities from which germplasm sources were originally developed, and they maintain high levels of heterozygosity and nucleotide diversity. However, the commercial germplasm sources represent a small fraction of the overall genetic diversity of P. spicata in the Intermountain West. Given the low migration rates and long divergence times between some pairs of P. spicata populations, using commercial germplasm sources could facilitate undesirable restoration outcomes when used in certain geographic areas, even if the environment in which the commercial materials thrive is similar to that of the restoration site. As such, population structure and history can be used to provide guidance on what geographic areas may need additional native plant materials so that restoration efforts support species and community resilience and improve outcomes.

Genetic analyses of Astragalus sect. Humillimi (Fabaceae) resolve taxonomy and enable effective conservation.

PREMISE OF THE STUDY: Astragalus sect. Humillimi is distributed across the southwestern United States and contains two endangered taxa, A. cremnophylax var. cremnophylax and A. humillimus. The former was originally described from the South Rim of the Grand Canyon. Analysis of individuals discovered on the North Rim of the Grand Canyon yielded some evidence that the population represented a distinct species. To enable effective conservation, we clarify the group's taxonomy and characterize the genetic diversity of A. cremnophylax and A. humillimus. METHODS: We used AFLPs to genotype most species in sect. Humillimi, focusing on the two endangered forms. We examined patterns of genetic diversity using complementary analytical approaches. KEY RESULTS: Our results demonstrate that North Rim populations group with A. c. var. cremnophylax. We found low levels of genetic diversity at certain localities and strong differentiation among populations. Astragalus humillimus, which has suffered recent and severe population declines, exhibits weak differentiation among and low diversity within populations. CONCLUSIONS: Our results clarify the taxonomy of sect. Humillimi and define the boundaries of A. c. var. cremnophylax, which is shown to inhabit both rims of the Grand Canyon. This clarification, and detailed analysis of genetic variation within both endangered taxa, may advance ongoing efforts to conserve these taxa. Our results suggest that range-wide genetic analysis of A. humillimus may inform recovery strategies for this taxon.

Contrasting support for alternative models of genomic variation based on microhabitat preference: species-specific effects of climate change in alpine sedges.

Deterministic processes may uniquely affect codistributed species' phylogeographic patterns such that discordant genetic variation among taxa is predicted. Yet, explicitly testing expectations of genomic discordance in a statistical framework remains challenging. Here, we construct spatially and temporally dynamic models to investigate the hypothesized effect of microhabitat preferences on the permeability of glaciated regions to gene flow in two closely related montane species. Utilizing environmental niche models from the Last Glacial Maximum and the present to inform demographic models of changes in habitat suitability over time, we evaluate the relative probabilities of two alternative models using approximate Bayesian computation (ABC) in which glaciated regions are either (i) permeable or (ii) a barrier to gene flow. Results based on the fit of the empirical data to data sets simulated using a spatially explicit coalescent under alternative models indicate that genomic data are consistent with predictions about the hypothesized role of microhabitat in generating discordant patterns of genetic variation among the taxa. Specifically, a model in which glaciated areas acted as a barrier was much more probable based on patterns of genomic variation in Carex nova, a wet-adapted species. However, in the dry-adapted Carex chalciolepis, the permeable model was more probable, although the difference in the support of the models was small. This work highlights how statistical inferences can be used to distinguish deterministic processes that are expected to result in discordant genomic patterns among species, including species-specific responses to climate change.

Utilizing RADseq data for phylogenetic analysis of challenging taxonomic groups: A case study in Carex sect. Racemosae.

PREMISE OF THE STUDY: Relationships among closely related and recently diverged taxa can be especially difficult to resolve. Here we use both Sanger sequencing and next-generation RADseq data sets to estimate phylogenetic relationships among species of Carex section Racemosae (Cyperaceae), a clade largely restricted to high latitudes and elevations. Interest in relationships among these taxa derives from questions about the species' biogeographic histories and possible links between diversification and Pleistocene glaciations. METHODS: A combination of approaches and molecular markers were used to estimate relationships among Carex species within sect. Racemosae and taxa from closely related sections. Nuclear and chloroplast loci generated by Sanger sequencing were analyzed with *BEAST, and SNP data from RADseq loci were analyzed as a concatenated data set using maximum likelihood and as independent loci using SVDquartets. KEY RESULTS: Sanger sequencing data sets resolved relationships among taxa at intermediate phylogenetic depths (albeit with low levels of support). Only the RADseq data resolved relationships with strong support at all phylogenetic depths. Moreover, different methods and data partitions of the RADseq data resulted in nearly identical topologies. Carex sect. Racemosae is a strongly supported clade, although a handful of species were found to group with closely related sections. Herbarium specimens up to 35 yr old successfully produced informative RADseq data. CONCLUSIONS: Despite the short read lengths of RADseq data, they nevertheless resolved relationships that Sanger sequencing data did not. Resolution of the phylogenetic relationships among recently and rapidly diversifying taxa within sect. Racemosae clades suggest a role for the Pleistocene glaciations in clade diversification.

Colonization from divergent ancestors: glaciation signatures on contemporary patterns of genomic variation in Collared Pikas (Ochotona collaris).

Identifying the genetic structure of a species and the factors that drive it is an important first step in modern population management, in part because populations evolving from separate ancestral sources may possess potentially different characteristics. This is especially true for climate-sensitive species such as pikas, where the delimitation of distinct genetic units and the characterization of population responses to contemporary and historical environmental pressures are of particular interest. We combined a restriction site-associated DNA sequencing (RADSeq) data set containing 4156 single nucleotide polymorphisms with ecological niche models (ENMs) of present and past habitat suitability to characterize population composition and evaluate the effects of historical range shifts, contemporary climates and landscape factors on gene flow in Collared Pikas, which are found in Alaska and adjacent regions of northwestern Canada and are the lesser-studied of North America's two pika species. The results suggest that contemporary environmental factors contribute little to current population connectivity. Instead, genetic diversity is strongly shaped by the presence of three ancestral lineages isolated during the Pleistocene (~148 and 52 kya). Based on ENMs and genetic data, populations originating from a northern refugium experienced longer-term stability, whereas both southern lineages underwent population expansion - contradicting the southern stability and northern expansion patterns seen in many other taxa. Current populations are comparable with respect to generally low diversity within populations and little-to-no recent admixture. The predominance of divergent histories structuring populations implies that if we are to understand and manage pika populations, we must specifically assess and accurately account for the forces underlying genetic similarity.

Microhabitat differences impact phylogeographic concordance of codistributed species: genomic evidence in montane sedges (Carex L.) from the Rocky Mountains.

By selecting codistributed, closely related montane sedges from the Rocky Mountains that are similar in virtually all respects but one-their microhabitat affinities-we test predictions about how patterns of genetic variation are expected to differ between Carex nova, an inhabitant of wetlands, and Carex chalciolepis, an inhabitant of drier meadows, slopes, and ridges. Although contemporary populations of the taxa are similarly isolated, the distribution of glacial moraines suggests that their past population connectedness would have differed. Sampling of codistributed population pairs from different mountain ranges combined with the resolution provided by over 24,000 single nucleotide polymorphism loci supports microhabitat-mediated differences in the sedges' patterns of genetic variation that are consistent with their predicted differences in the degree of isolation of ancestral source populations. Our results highlight how microhabitat preferences may interact with glaciations to produce fundamental differences in the past distributions of presently codistributed species. We discuss the implications of these findings for generalizing the impacts of climate-induced distributional shifts for communities, as well as for the prospects of gaining insights about species-specific deterministic processes, not just deterministic community-level responses, from comparative phylogeographic study.