Population genomics and climate adaptation of a C4 perennial grass, Panicum hallii (Poaceae).

BACKGROUND: Understanding how and why genetic variation is partitioned across geographic space is of fundamental importance to understanding the nature of biological species. How geographical isolation and local adaptation contribute to the formation of ecotypically differentiated groups of plants is just beginning to be understood through population genomic studies. We used whole genome sequencing combined with association study of climate to discover the drivers of differentiation in the perennial C4 grass Panicum hallii. RESULTS: Sequencing of 89 natural accessions of P.hallii revealed complex population structure across the species range. Major population genomic separation was found between subspecies P.hallii var. hallii and var. filipes as well as between at least four major unrecognized subgroups within var. hallii. At least 139 genomic SNPs were significantly associated with temperature or precipitation across the range and these SNPs were enriched for non-synonymous substitutions. SNPs associated with temperature and aridity were more often found in or near genes than expected by chance and enriched for putative involvement in dormancy processes, seed maturation, response to hyperosmosis and salinity, abscisic acid metabolism, hormone metabolism, and drought recovery. CONCLUSIONS: Both geography and climate adaptation contribute significantly to patterns of genome-wide variation in P.hallii. Population subgroups within P.hallii may represent early stages in the formation of ecotypes. Climate associated loci identified here represent promising targets for future research in this and other perennial grasses.

Gene regulatory divergence between locally adapted ecotypes in their native habitats.

Local adaptation is a key driver of ecological specialization and the formation of new species. Despite its importance, the evolution of gene regulatory divergence among locally adapted populations is poorly understood, especially how that divergence manifests in nature. Here, we evaluate gene expression divergence and allele-specific gene expression responses for locally adapted coastal perennial and inland annual accessions of the yellow monkeyflower, Mimulus guttatus, in a field reciprocal transplant experiment. Overall, 6765 (73%) of surveyed genes were differentially expressed between coastal and inland habitats, while 7213 (77%) were differentially expressed between the coastal perennial and inland annual accessions. Cis-regulatory variation was pervasive, affecting 79% (5532) of differentially expressed genes. We detected trans effects for 52% (3611) of differentially expressed genes. Expression plasticity of alleles across habitats (G × E interactions) appears to be relatively common (affecting 18% of transcripts) and could minimize fitness trade-offs at loci that contribute to local adaptation. We also found evidence that at least one chromosomal inversion may act as supergene by holding together haplotypes of differentially expressed genes, but this pattern depends on habitat context. Our results highlight multiple key patterns regarding the relationship between gene expression and the evolution of locally adapted populations.

Population genomic scans suggest novel genes underlie convergent flowering time evolution in the introduced range of Arabidopsis thaliana.

A long-standing question in evolutionary biology is whether the evolution of convergent phenotypes results from selection on the same heritable genetic components. Using whole-genome sequencing and genome scans, we tested whether the evolution of parallel longitudinal flowering time clines in the native and introduced ranges of Arabidopsis thaliana has a similar genetic basis. We found that common variants of large effect on flowering time in the native range do not appear to have been under recent strong selection in the introduced range. We identified a set of 38 new candidate genes that are putatively linked to the evolution of flowering time. A high degree of conditional neutrality of flowering time variants between the native and introduced range may preclude parallel evolution at the level of genes. Overall, neither gene pleiotropy nor available standing genetic variation appears to have restricted the evolution of flowering time to high-frequency variants from the native range or to known flowering time pathway genes.

Pooled ecotype sequencing reveals candidate genetic mechanisms for adaptive differentiation and reproductive isolation.

The early stages of speciation are often characterized by the formation of partially reproductively isolated ecotypes, which evolve as a by-product of divergent selective forces that are endemic to different habitats. Identifying the genomic regions, genes and ultimately functional polymorphisms that are involved in the processes of ecotype formation is inherently challenging, as there are likely to be many different loci involved in the process. To localize candidate regions of the genome contributing to ecotype formation, we conducted whole-genome pooled sequencing (pool-seq) with 47 coastal perennial and 50 inland annual populations of the yellow monkeyflower, Mimulus guttatus. Coastal perennial and inland annual ecotypes of M. guttatus have previously been shown to be ecologically reproductively isolated and highly locally adapted to their respective habitats. Our pool-seq results found allelic differentiation between the ecotypes for two chromosomal inversions, suggesting that frequencies of inversion heterokaryotypes are strongly differentiated between the ecotypes. Further, there were elevated levels of nonsynonymous change across chromosomal inversions. Across the genome, we identified multiple strong candidate genes potentially driving the morphological, life history and salt tolerance differences between the ecotypes. Several candidate genes coincide with previously identified quantitative trait locus regions and also show a signature of recent natural selection. Overall, the results of our study add to growing support for a major role of chromosomal inversions in adaptation and speciation and provide new insights into the genetic mechanisms underlying classic plant ecotype adaptations to wet and dry habitats.

Factors influencing the effect size distribution of adaptive substitutions.

The distribution of effect sizes of adaptive substitutions has been central to evolutionary biology since the modern synthesis. Early theory proposed that because large-effect mutations have negative pleiotropic consequences, only small-effect mutations contribute to adaptation. More recent theory suggested instead that large-effect mutations could be favoured when populations are far from their adaptive peak. Here we suggest that the distributions of effect sizes are expected to differ among study systems, reflecting the wide variation in evolutionary forces and ecological conditions experienced in nature. These include selection, mutation, genetic drift, gene flow, and other factors such as the degree of pleiotropy, the distance to the phenotypic optimum, whether the optimum is stable or moving, and whether new mutation or standing genetic variation provides the source of adaptive alleles. Our goal is to review how these factors might affect the distribution of effect sizes and to identify new research directions. Until more theory and empirical work is available, we feel that it is premature to make broad generalizations about the effect size distribution of adaptive substitutions important in nature.

The genomic landscape of molecular responses to natural drought stress in Panicum hallii.

Environmental stress is a major driver of ecological community dynamics and agricultural productivity. This is especially true for soil water availability, because drought is the greatest abiotic inhibitor of worldwide crop yields. Here, we test the genetic basis of drought responses in the genetic model for C4 perennial grasses, Panicum hallii, through population genomics, field-scale gene-expression (eQTL) analysis, and comparison of two complete genomes. While gene expression networks are dominated by local cis-regulatory elements, we observe three genomic hotspots of unlinked trans-regulatory loci. These regulatory hubs are four times more drought responsive than the genome-wide average. Additionally, cis- and trans-regulatory networks are more likely to have opposing effects than expected under neutral evolution, supporting a strong influence of compensatory evolution and stabilizing selection. These results implicate trans-regulatory evolution as a driver of drought responses and demonstrate the potential for crop improvement in drought-prone regions through modification of gene regulatory networks.

Temporal patterns of damage and decay kinetics of DNA retrieved from plant herbarium specimens.

Herbaria archive a record of changes of worldwide plant biodiversity harbouring millions of specimens that contain DNA suitable for genome sequencing. To profit from this resource, it is fundamental to understand in detail the process of DNA degradation in herbarium specimens. We investigated patterns of DNA fragmentation and nucleotide misincorporation by analysing 86 herbarium samples spanning the last 300 years using Illumina shotgun sequencing. We found an exponential decay relationship between DNA fragmentation and time, and estimated a per nucleotide fragmentation rate of 1.66 × 10(-4) per year, which is six times faster than the rate estimated for ancient bones. Additionally, we found that strand breaks occur specially before purines, and that depurination-driven DNA breakage occurs constantly through time and can to a great extent explain decreasing fragment length over time. Similar to what has been found analysing ancient DNA from bones, we found a strong correlation between the deamination-driven accumulation of cytosine to thymine substitutions and time, which reinforces the importance of substitution patterns to authenticate the ancient/historical nature of DNA fragments. Accurate estimations of DNA degradation through time will allow informed decisions about laboratory and computational procedures to take advantage of the vast collection of worldwide herbarium specimens.

Identifying the genes underlying quantitative traits: a rationale for the QTN programme.

The goal of identifying the genes or even nucleotides underlying quantitative and adaptive traits has been characterized as the 'QTN programme' and has recently come under severe criticism. Part of the reason for this criticism is that much of the QTN programme has asserted that finding the genes and nucleotides for adaptive and quantitative traits is a fundamental goal, without explaining why it is such a hallowed goal. Here we outline motivations for the QTN programme that offer general insight, regardless of whether QTNs are of large or small effect, and that aid our understanding of the mechanistic dynamics of adaptive evolution. We focus on five areas: (i) vertical integration of insight across different levels of biological organization, (ii) genetic parallelism and the role of pleiotropy in shaping evolutionary dynamics, (iii) understanding the forces maintaining genetic variation in populations, (iv) distinguishing between adaptation from standing variation and new mutation, and (v) the role of genomic architecture in facilitating adaptation. We argue that rather than abandoning the QTN programme, we should refocus our efforts on topics where molecular data will be the most effective for testing hypotheses about phenotypic evolution.

Evidence of a high-Andean, mid-Holocene plant community: An ancient DNA analysis of glacially preserved remains.

PREMISE OF THE STUDY: Around the world, tropical glaciers and ice caps are retreating at unprecedented rates because of climate change. In at least one location, along the margin of the Quelccaya Ice Cap in southeastern Peru, ancient plant remains have been continually uncovered since 2002. We used genetic analysis to identify plants that existed at these sites during the mid-Holocene. • METHODS: We examined remains between 4576 and 5222 yr old, using PCR amplification, cloning, and sequencing of a fragment of the chloroplast trnL intron. We then matched these sequences to sequences in GenBank. • KEY RESULTS: We found evidence of at least five taxa characteristic of wetlands, which occur primarily at lower elevations in the region today. • CONCLUSIONS: A diverse community most likely existed at these locations the last time they were ice-free and thus has the potential to reestablish with time. This is the first genetic analysis of vegetation uncovered by receding glacial ice, and it may become one of many as ancient plant materials are newly uncovered in a changing climate.