bioRxiv Science⌕ Search

Biology subjects

Aitken, S. N.

Publications and source records attributed to Aitken, S. N..

7 recordsLinked to original sources

Polygenic and redundant architectures of climate-adaptive traits may complicate genomic predictions of maladaptation

SignificanceUnderstanding the genetic basis of local adaptation is an important step to predict species responses to climate change. Current predictions of maladaptation to climate in trees, however, rely mostly on genotype-environment associations, which overlooks the complexity of genetic architectures underpinning climate-adaptive traits. Based on genotype-phenotype associations, we unveil key aspects of the polygenic architecture of drought tolerance and cold hardiness in two lineages of a widespread conifer. Our results suggest that predictions based solely on climate-associated alleles may mischaracterize maladaptation to future climates due to mismatches between the distribution of climate-associated alleles and alleles contributing to adaptive traits. We also show that cold hardiness and drought tolerance evolved largely independently in the two lineages, and with little pleiotropy between traits. Understanding the genetic architecture of climate-adaptive traits can help predict responses to climate change and inform management strategies that mitigate the effects of future climates. By characterizing the genetic basis of adaptation to spatially varying climate conditions, models can predict response to temporal change in climate by extrapolating from spatial patterns of variation. However, such methods are predicated upon a simple genetic basis, with a linear relationship between allele frequency, phenotype, and environment. Here, we explore the nature of the mapping between genotype, phenotype, and climate adaptation in Douglas-fir, an important North American conifer. Using two large common garden experiments combined with exome sequencing and case-control genome-wide association tests, we found that drought tolerance and cold hardiness in two Douglas-fir varieties (Pseudotsuga menziesii var. menziesii and var. glauca) are highly polygenic with little pleiotropy between the two traits. The two varieties showed little repeated evolution in the genetic basis of drought tolerance and none for cold hardiness. Allelic clines were observed along geographic and climatic gradients across 74 natural populations, but their direction of effect was often inconsistent with phenotypic clines. Our findings reveal that the genomic variation underlying climate-adaptive traits is remarkably complex, with redundancy likely playing a key role in the evolution of the divergent polygenetic architectures of abiotic stress tolerance. This suggests that predicting maladaptation to climate based solely on climate-associated alleles may misrepresent future adaptive responses. Genomic predictions and management practices should focus on individual lineages and consider the particularities of the genetic architecture of climate-adaptive traits.

evolutionary biology↗

Genetic architecture underlying response to the fungal pathogen Dothistroma septosporum in lodgepole pine, jack pine, and their hybrids

In recent decades, Dothistroma needle blight (DNB), a pine tree disease caused by the fungal pathogen Dothistroma septosporum, has severely damaged lodgepole pine (Pinus contorta Dougl. ex. Loud.) in British Columbia, Canada, and raised health concerns for jack pine (Pinus banksiana Lamb.). The pathogen has already shown signs of host shift eastward to the hybrid populations between lodgepole pine and jack pine (Pinus contorta x P. banksiana), and possibly into pure jack pine. However, we have little knowledge about mechanisms of resistance to D. septosporum, especially the underlying genetic basis of variation in pines. In this study, we conducted controlled inoculations to induce infection by D. septosporum and performed a genome-wide case-control association study with pooled sequencing (pool-seq) data to dissect the genetic architecture underlying response in lodgepole pine, jack pine, and their hybrids. We identified candidate genes associated with D. septosporum response in lodgepole pine and in hybrid samples. We also assessed genetic structure in hybrid populations and inferred how introgression may affect the distribution of genetic variation involved in D. septosporum response in the studied samples. These results can be used to develop genomic tools to evaluate DNB risk, guide forest management strategies, and potentially select for resistant genotypes.

plant biology↗

Weak local adaptation to drought in seedlings of a widespread conifer

There is an urgent need for better understanding how populations of trees will respond to predictable changes in climate and the intensification of extreme weather events such as droughts. The distribution of adaptive traits in seedlings is a crucial component of population adaptive potential and its characterization is important for development of management approaches mitigating the effects of climate change on forests. In this study, we used a large-scale common garden drought experiment to characterize the variation in drought tolerance, growth, and plastic responses to extreme summer drought in seedlings of 73 natural provenances of the two main varieties of Douglas-fir (Pseudotsuga menziesii var. menziesii and var. glauca), sampled across most of their extensive natural ranges. We detected large differences between the two Douglas-fir varieties for all traits assessed, with var. glauca showing higher tolerance to drought but slower height growth and less plasticity than var. menziesii. Surprisingly, signals of local adaptation to drought within varieties were weak within var. glauca and nearly absent within var. menziesii. Temperature-related variables were identified as the main climatic drivers of clinal variation in drought tolerance and height growth species-wide, and in height growth within var. menziesii. Furthermore, our data indicate that higher plasticity under extreme droughts could be maladaptive in var. menziesii. Overall, our study suggests that genetic variation for drought tolerance in seedlings is maintained primarily within rather than among provenances within varieties and does not compromise growth at early stages of plant development. Given these results, assisted gene flow is unlikely to help facilitate adaptation to drought within Douglas-fir varieties, but selective breeding within provenances could accelerate adaptation.

evolutionary biology↗

How useful is genomic data for predicting maladaptation to future climate?

Methods using genomic information to forecast potential population maladaptation to climate change are becoming increasingly common, yet the lack of model validation poses serious hurdles toward their incorporation into management and policy. Here, we compare the validation of maladaptation estimates derived from two methods - Gradient Forests (GFoffset) and the Risk Of Non-Adaptedness (RONA) - using exome capture pool-seq data from 35 to 39 populations across three conifer taxa: two Douglas-fir varieties and jack pine. We evaluate sensitivity of these algorithms to the source of input loci (markers selected from genotype-environment associations [GEA] or those selected at random). We validate these methods against two-year and 52-year growth and mortality measured in independent transplant experiments. Overall, we find that both methods often better predict transplant performance than climatic or geographic distances. We also find that GFoffset and RONA models are surprisingly not improved using GEA candidates. Even with promising validation results, variation in model projections to future climates makes it difficult to identify the most maladapted populations using either method. Our work advances understanding of the sensitivity and applicability of these approaches, and we discuss recommendations for their future use.

evolutionary biology↗

Evaluating genomic data for management of local adaptation in a changing climate: A lodgepole pine case study

The need for tools to cost-effectively identify adaptive variation within ecologically and economically important plant species is mounting as the detrimental effects of climate change become increasingly apparent. For crop and wild populations alike, mismatches between adaptive variation and climatic optima will reduce health, growth, survival, reproduction, and continued establishment. The ease with which land managers can quantify the relative importance of different climate factors or the spatial scale of local adaptation to climate will have direct implications for the potential of mitigating or resolving such risks. Using seed collected from 281 provenances of lodgepole pine (Pinus contorta) from across western Canada, we compare genomic data to phenotypic and climatic data to assess their effectiveness in characterizing the climatic drivers and spatial scale of local adaptation in this species. We find that genomic and climate data are nearly equivalent for describing local adaptation in seedling traits. We also find strong agreement between the climate variables associated with genomic variation and with 20-year heights from a long-term provenance trial, suggesting that genomic data may be a viable option for identifying climatic drivers of local adaptation where phenotypic data are unavailable. Genetic clines associated with cold injury occur at broad spatial scales, suggesting that standing variation of adaptive alleles for this and similar species does not require management at scales finer than are indicated by phenotypic data. This study demonstrates that genomic data are most useful when paired with phenotypic data, but can also fill some of the traditional roles of phenotypic data in management of species for which phenotypic trials are not feasible.

evolutionary biology↗

The interplay between demography and neutral evolution at the expansion front of a widespread conifer, Picea sitchensis

Tree species in the northern hemisphere have advanced and retreated with interglacial and glacial periods, and are currently subject to rapid anthropogenic climate change. These observations prompt questions about the mechanisms allowing tree populations to respond quickly to selection pressures when establishing into new areas. Focusing on the northern expanding range edge of Picea sitchensis, a widespread conifer of western North America, we ask how genetic structure and diversity develop during colonization, and assess the role of demographic history in shaping the evolutionary trajectory of a colonizing population. By combining nearly 500 years of tree-ring and genetic data at the expansion front on the Kodiak Archipelago, we show that allelic richness - but not expected heterozygosity - increased rapidly during early stages of establishment in the 1600s, while genetic differentiation from populations further from the front decreased. This trend ended in the 1700s, after an increase in population growth rate. These findings highlight the major role of long-distance pollen dispersal in the recovery of genetic diversity during initial stages of colonization, and suggest that demographic dynamics including an initial lag in population growth are likely limiting factors in the adaptation of tree populations tracking their niche in a changing climate.

evolutionary biology↗

Exploring Approximate Bayesian Computation for inferring recent demographic history with genomicmarkers in non-model species

Approximate Bayesian computation (ABC) is widely used to infer demographic history of populations and species using DNA markers. Genomic markers can now be developed for non-model species using reduced representation library (RRL) sequencing methods that select a fraction of the genome using targeted sequence capture or restriction enzymes (genotyping-by-sequencing, GBS). We explored the influence of marker number and length, knowledge of gametic phase, and tradeoffs between sample size and sequencing depth on the quality of demographic inferences performed with ABC. We focused on 2-population models of recent spatial expansion with varying numbers of unknown parameters. Performing ABC on simulated datasets with known parameter values, we found that the timing of a recent spatial expansion event could be precisely estimated in a 3-parameter model. Taking into account uncertainty in parameters such as initial population size and migration rate collectively decreased the precision of inferences dramatically. Phasing haplotypes did not improve results, regardless of sequence length. Numerous short sequences were as valuable as fewer, longer sequences, and performed best when a large sample size was sequenced at low individual depth, even when sequencing errors were added. ABC results were similar to results obtained with an alternative method based on the site frequency spectrum (SFS) when performed with unphased GBS-type markers. We conclude that unphased GBS-type datasets can be sufficient to precisely infer simple demographic models, and discuss possible improvements for the use of ABC with genomic data.

evolutionary biology↗