John K. McKay

Adaptive population divergence: markers, QTL and traits

Abstract Molecular markers appear to be poor indicators of heritable variation in adaptive traits. Direct comparison of population structure in markers with that in traits is made possible by the measure Q st , which partitions quantitative genetic variation in a manner analogous to F st for single gene markers. A survey of the literature reveals that mean Q st is typically larger than and poorly correlated with mean F st across 29 species. Within species, Q st varies widely among traits; traits experiencing the strongest local selection pressures are expected to be the most divergent from molecular F st . Thus, Q st will be particularly relevant to conservation efforts where preserving extant adaptation to local environments is an important goal. Recent theoretical and simulation studies suggest however that F st is a better predictor of the pattern of allelic differentiation at quantitative trait loci (QTLs) than is Q st in random mating populations, in which case allelic variation at QTLs might be better assessed by molecular markers than will extant variation in the traits themselves.

Harnessing genomics for delineating conservation units

Genomic data have the potential to revolutionize the delineation of conservation units (CUs) by allowing the detection of adaptive genetic variation, which is otherwise difficult for rare, endangered species. In contrast to previous recommendations, we propose that the use of neutral versus adaptive markers should not be viewed as alternatives. Rather, neutral and adaptive markers provide different types of information that should be combined to make optimal management decisions. Genetic patterns at neutral markers reflect the interaction of gene flow and genetic drift that affects genome-wide variation within and among populations. This population genetic structure is what natural selection operates on to cause adaptive divergence. Here, we provide a new framework to integrate data on neutral and adaptive markers to protect biodiversity.

Genetics of drought adaptation in Arabidopsis thaliana : I. Pleiotropy contributes to genetic correlations among ecological traits

We examined patterns of genetic variance and covariance in two traits (i) carbon stable isotope ratio δ13C (dehydration avoidance) and (ii) time to flowering (drought escape), both of which are putative adaptations to local water availability. Greenhouse screening of 39 genotypes of Arabidopsis thaliana native to habitats spanning a wide range of climatic conditions, revealed a highly significant positive genetic correlation between δ13C and flowering time. Studies in a range of C3 annuals have also reported large positive correlations, suggesting the presence of a genetically based trade‐off between mechanisms of dehydration avoidance (δ13C) and drought escape (early flowering). We examined the contribution of pleiotropy by using a combination of mutant and near‐isogenic lines to test for positive mutational covariance between δ13C and flowering time. Ecophysiological mutants generally showed variation in δ13C but not flowering time. However, flowering time mutants generally demonstrated pleiotropic effects consistent with natural variation. Mutations that caused later flowering also typically resulted in less negative δ13C and thus probably higher water use efficiency. We found strong evidence for pleiotropy using near‐isogenic lines of FRIGIDA and FLOWERING LOCUS C, cloned loci known to be responsible for natural variation in flowering time. These data suggest the correlated evolution of δ13C and flowering time is explained in part by the fixation of pleiotropic alleles that alter both δ13C and time to flowering.

2b-RAD: a simple and flexible method for genome-wide genotyping

We describe 2b-RAD, a streamlined restriction site–associated DNA (RAD) genotyping method based on sequencing the uniform fragments produced by type IIB restriction endonucleases. Well-studied accessions of Arabidopsis thaliana were genotyped to validate the methods accuracy and to demonstrate fine-tuning of marker density as needed. The simplicity of the 2b-RAD protocol makes it particularly suitable for high-throughput genotyping as required for linkage mapping and profiling genetic variation in natural populations.

LATITUDINAL VARIATION IN GENETIC DIVERGENCE OF POPULATIONS AND THE POTENTIAL FOR FUTURE SPECIATION

Abstract —The increase in biological diversity with decreasing latitude is widely appreciated but the cause of the pattern is unknown. This pattern reflects latitudinal variation in both the origin of new species (cladogenesis) and the number of species that coexist. Here we address latitudinal variation in species origination, by examining population genetic processes that influence speciation. Previous data suggest a greater number of speciation events at lower latitudes. If speciation events occur more frequently at lower latitudes, we predicted that genetic divergence among populations within species, an important component of cladogenesis, should be greater among lower latitude populations. We tested this prediction using within‐species patterns of mtDNA variation across 60 vertebrate species that collectively spanned six continents, two oceans, and 119 degrees latitude. We found greater genetic divergence of populations, controlling for geographic distance, at lower latitudes within species. This pattern remained statistically significant after removing populations that occur in localities previously covered by continental glaciers during the last glaciation. Results suggest that lower latitude populations within species exhibit greater evolutionary independence, increasing the likelihood that mutation, recombination, selection, and/or drift will lead to divergence of traits important for reproductive isolation and speciation. Results are consistent with a greater influence of seasonality, reduced energy, and/or glacial (Milankovitch) cycles acting on higher latitude populations, and represent one of the few tests of predictions of latitudinal variation in speciation rates using population genetic data.

Genomics and the challenging translation into conservation practice

The global loss of biodiversity continues at an alarming rate. Genomic approaches have been suggested as a promising tool for conservation practice as scaling up to genome-wide data can improve traditional conservation genetic inferences and provide qualitatively novel insights. However, the generation of genomic data and subsequent analyses and interpretations remain challenging and largely confined to academic research in ecology and evolution. This generates a gap between basic research and applicable solutions for conservation managers faced with multifaceted problems. Before the real-world conservation potential of genomic research can be realized, we suggest that current infrastructures need to be modified, methods must mature, analytical pipelines need to be developed, and successful case studies must be disseminated to practitioners.

Local adaptation across a climatic gradient despite small effective population size in the rare sapphire rockcress

When assigning conservation priorities in endangered species, two common management strategies seek to protect remnant populations that (i) are the most genetically divergent or (ii) possess the highest diversity at neutral genetic markers. These two approaches assume that variation in molecular markers reflects variation in ecologically important traits and ignore the possibility of local adaptation among populations that show little divergence or variation at marker loci. Using common garden experiments, we demonstrate that populations of the rare endemic plant Arabis fecunda are physiologically adapted to the local microclimate. Local adaptation occurs despite (i) the absence of divergence at almost all marker loci and (ii) very small effective population sizes, as evidenced by extremely low levels of allozyme and DNA sequence polymorphism. Our results provide empirical evidence that setting conservation priorities based exclusively on molecular marker diversity may lead to the loss of locally adapted populations.

Genetics of Drought Adaptation in Arabidopsis thaliana II. Qtl Analysis of a New Mapping Population, Kas-1 × Tsu-1

Abstract Despite compelling evidence that adaptation to local climate is common in plant populations, little is known about the evolutionary genetics of traits that contribute to climatic adaptation. A screen of natural accessions of Arabidopsis thaliana revealed Tsu-1 and Kas-1 to be opposite extremes for water-use efficiency and climate at collection sites for these accessions differs greatly. To provide a tool to understand the genetic basis of this putative adaptation, Kas-1 and Tsu-1 were reciprocally crossed to create a new mapping population. Analysis of F3 families showed segregating variation in both δ13C and transpiration rate, and as expected these traits had a negative genetic correlation (rg=− 0.3). 346 RILs, 148 with Kas-1 cytoplasm and 198 with Tsu-1 cytoplasm, were advanced to the F9 and genotyped using 48 microsatellites and 55 SNPs for a total of 103 markers. This mapping population was used for QTL analysis of δ13C using F9 RIL means. Analysis of this reciprocal cross showed a large effect of cytoplasmic background, as well as two QTL for δ13C. The Kas-1 × Tsu-1 mapping population provides a powerful new resource for mapping QTL underlying natural variation and for dissecting the genetic basis of water-use efficiency differences.

Physiological Genomics of Response to Soil Drying in Diverse Arabidopsis Accessions

This work examines the physiological and transcriptomic responses to soil drying in 17 diverse accessions of Arabidopsis thaliana, finding that acclimation to drought stress involved increased investment in photosynthesis, carbohydrate turnover, and root growth, as well as activation of abscisic acid signaling pathways and identifying functional variants of key stress response genes. Arabidopsis thaliana, like many species, is characterized by abundant genetic variation. This variation is rapidly being cataloged at the sequence level, but careful dissection of genetic variation in whole-organism responses to stresses encountered in the natural environment are lacking; this functional variation can be exploited as a natural mutant screen to determine gene function. Here, we document physiological and transcriptomic response to soil drying in 17 natural accessions of Arabidopsis. By imposing ecologically realistic stress conditions, we found that acclimation in Arabidopsis involved a strong signature of increased investment in photosynthesis, carbohydrate turnover, and root growth. Our results extend previous work in the Columbia accession suggesting that abscisic acid signaling pathways play an important role in drought stress response. We also identified several mechanisms, including an increase in leaf nitrogen concentration and upregulation of two-component signaling relays, that were common to most natural accessions but had not been identified in studies using only the Columbia accession. Principal component analysis reveals strong correlations between suites of genes and specific physiological responses to stress. The functional variants we identified may represent adaptive mutations in natural habitats and useful variants for agronomic improvement of crop species.

Characterizing genomic variation of Arabidopsis thaliana: the roles of geography and climate

Arabidopsis thaliana inhabits diverse climates and exhibits varied phenology across its range. Although A. thaliana is an extremely well‐studied model species, the relationship between geography, growing season climate and its genetic variation is poorly characterized. We used redundancy analysis (RDA) to quantify the association of genomic variation [214 051 single nucleotide polymorphisms (SNPs)] with geography and climate among 1003 accessions collected from 447 locations in Eurasia. We identified climate variables most correlated with genomic variation, which may be important selective gradients related to local adaptation across the species range. Climate variation among sites of origin explained slightly more genomic variation than geographical distance. Large‐scale spatial gradients and early spring temperatures explained the most genomic variation, while growing season and summer conditions explained the most after controlling for spatial structure. SNP variation in Scandinavia showed the greatest climate structure among regions, possibly because of relatively consistent phenology and life history of populations in this region. Climate variation explained more variation among nonsynonymous SNPs than expected by chance, suggesting that much of the climatic structure of SNP correlations is due to changes in coding sequence that may underlie local adaptation.