Scots pine - panmixia and the elusive signal of genetic adaptation.

Scots pine is the foundation species of diverse forested ecosystems across Eurasia and displays remarkable ecological breadth, occurring in environments ranging from temperate rainforests to arid tundra margins. Such expansive distributions can be favored by various demographic and adaptive processes and the interactions between them. To understand the impact of neutral and selective forces on genetic structure in Scots pine, we conducted range-wide population genetic analyses on 2321 trees from 202 populations using genotyping-by-sequencing, reconstructed the recent demography of the species and examined signals of genetic adaptation. We found a high and uniform genetic diversity across the entire range (global FST 0.048), no increased genetic load in expanding populations and minor impact of the last glacial maximum on historical population sizes. Genetic-environmental associations identified only a handful of single-nucleotide polymorphisms significantly linked to environmental gradients. The results suggest that extensive gene flow is predominantly responsible for the observed genetic patterns in Scots pine. The apparent missing signal of genetic adaptation is likely attributed to the intricate genetic architecture controlling adaptation to multi-dimensional environments. The panmixia metapopulation of Scots pine offers a good study system for further exploration into how genetic adaptation and plasticity evolve under gene flow and changing environment.

Effects of landscapes and range expansion on population structure and local adaptation.

Understanding the origin and distribution of genetic diversity across landscapes is critical for predicting the future of organisms in changing climates. This study investigated how adaptive and demographic forces have shaped diversity and population structure in Pinus densata, a keystone species on Qinghai-Tibetan Plateau (QTP). We examined the distribution of genomic diversity across the range of P. densata using exome capture sequencing. We applied spatially explicit tests to dissect the impacts of allele surfing, geographic isolation and environmental gradients on population differentiation and forecasted how this genetic legacy may limit the persistence of P. densata in future climates. We found that allele surfing from range expansion could explain the distribution of 39% of the c. 48 000 genotyped single nucleotide polymorphisms (SNPs). Uncorrected, these allele frequency clines severely confounded inferences of selection. After controlling for demographic processes, isolation-by-environment explained 9.2-19.5% of the genetic structure, with c. 4.0% of loci being affected by selection. Allele surfing and genotype-environment associations resulted in genomic mismatch under projected climate scenarios. We illustrate that significant local adaptation, when coupled with reduced diversity as a result of demographic history, constrains potential evolutionary response to climate change. The strong signal of genomic vulnerability in P. densata may be representative for other QTP endemics.

The Mitogenome of Norway Spruce and a Reappraisal of Mitochondrial Recombination in Plants.

Plant mitogenomes can be difficult to assemble because they are structurally dynamic and prone to intergenomic DNA transfers, leading to the unusual situation where an organelle genome is far outnumbered by its nuclear counterparts. As a result, comparative mitogenome studies are in their infancy and some key aspects of genome evolution are still known mainly from pregenomic, qualitative methods. To help address these limitations, we combined machine learning and in silico enrichment of mitochondrial-like long reads to assemble the bacterial-sized mitogenome of Norway spruce (Pinaceae: Picea abies). We conducted comparative analyses of repeat abundance, intergenomic transfers, substitution and rearrangement rates, and estimated repeat-by-repeat homologous recombination rates. Prompted by our discovery of highly recombinogenic small repeats in P. abies, we assessed the genomic support for the prevailing hypothesis that intramolecular recombination is predominantly driven by repeat length, with larger repeats facilitating DNA exchange more readily. Overall, we found mixed support for this view: Recombination dynamics were heterogeneous across vascular plants and highly active small repeats (ca. 200 bp) were present in about one-third of studied mitogenomes. As in previous studies, we did not observe any robust relationships among commonly studied genome attributes, but we identify variation in recombination rates as a underinvestigated source of plant mitogenome diversity.

Interspecific Plastome Recombination Reflects Ancient Reticulate Evolution in Picea (Pinaceae).

Plastid sequences are a cornerstone in plant systematic studies and key aspects of their evolution, such as uniparental inheritance and absent recombination, are often treated as axioms. While exceptions to these assumptions can profoundly influence evolutionary inference, detecting them can require extensive sampling, abundant sequence data, and detailed testing. Using advancements in high-throughput sequencing, we analyzed the whole plastomes of 65 accessions of Picea, a genus of ∼35 coniferous forest tree species, to test for deviations from canonical plastome evolution. Using complementary hypothesis and data-driven tests, we found evidence for chimeric plastomes generated by interspecific hybridization and recombination in the clade comprising Norway spruce (P. abies) and 10 other species. Support for interspecific recombination remained after controlling for sequence saturation, positive selection, and potential alignment artifacts. These results reconcile previous conflicting plastid-based phylogenies and strengthen the mounting evidence of reticulate evolution in Picea. Given the relatively high frequency of hybridization and biparental plastid inheritance in plants, we suggest interspecific plastome recombination may be more widespread than currently appreciated and could underlie reported cases of discordant plastid phylogenies.

Evidence for selection on a CONSTANS-like gene between two red oak species.

BACKGROUND AND AIMS: Hybridizing species such as oaks may provide a model to study the role of selection in speciation with gene flow. Discrete species' identities and different adaptations are maintained among closely related oak species despite recurrent gene flow. This is probably due to ecologically mediated selection at a few key genes or genomic regions. Neutrality tests can be applied to identify so-called outlier loci, which demonstrate locus-specific signatures of divergent selection and are candidate genes for further study. METHODS: Thirty-six genic microsatellite markers, some with putative functions in flowering time and drought tolerance, and eight non-genic microsatellite markers were screened in two population pairs (n = 160) of the interfertile species Quercus rubra and Q. ellipsoidalis, which are characterized by contrasting adaptations to drought. Putative outliers were then tested in additional population pairs from two different geographic regions (n = 159) to support further their potential role in adaptive divergence. KEY RESULTS: A marker located in the coding sequence of a putative CONSTANS-like (COL) gene was repeatedly identified as under strong divergent selection across all three geographically disjunct population pairs. COL genes are involved in the photoperiodic control of growth and development and are implicated in the regulation of flowering time. CONCLUSIONS: The location of the polymorphism in the Quercus COL gene and given the potential role of COL genes in adaptive divergence and reproductive isolation makes this a promising candidate speciation gene. Further investigation of the phenological characteristics of both species and flowering time pathway genes is suggested in order to elucidate the importance of phenology genes for the maintenance of species integrity. Next-generation sequencing in multiple population pairs in combination with high-density genetic linkage maps could reveal the genome-wide distribution of outlier genes and their potential role in reproductive isolation between these species.

Bat-cave catchment areas: using stable isotopes (deltaD) to determine the probable origins of hibernating bats.

The application of stable hydrogen isotope (deltaD) techniques has swiftly advanced our understanding of animal movements, but this progression is dominated by studies of birds and relatively long-distance, north-south migrants. This dominance reflects the challenge of incorporating multiple sources of error into geographic assignments and the nature of spatially explicit deltaD models, which possess greater latitudinal than longitudinal resolution. However, recent progress in likelihood-based assignments that incorporate multiple sources of isotopic error and Bayesian approaches that include additional sources of information may advance finer-scale understanding of animal movements. We develop a stable-isotope method for determining probable origins of bats within hibernacula and show that this method produces spatially explicit, continuous assignments with regional resolution. We outline how these assignments can be used to infer hibernacula connectivity, an application that could inform spatial modeling of white-nose syndrome. Additionally, estimates of seasonal and annual flight distances for many cave-dwelling bat species can be derived from this approach. We also discuss how this application can be used in general to provide insights into variable migratory and foraging strategies within bat populations.