Search for: All records

ABSTRACT Chromosomal inversion polymorphisms are ubiquitous across the diversity of diploid organisms and play a significant role in the evolution of adaptations in those species. Inversions are thought to operate as supergenes by trapping adaptive alleles at multiple linked loci through the suppression of recombination. While there is now considerable support for the supergene mechanism of inversion evolution, the extent to which inversions trap pre‐existing adaptive genetic variation versus accumulate new adaptive variants over time remains unclear. In this study, we report new insights into the evolution of a locally adaptive chromosomal inversion polymorphism (inv_chr8A), which contributes to the adaptive divergence between coastal perennial and inland annual ecotypes of the yellow monkeyflower,Mimulus guttatus. This research was enabled by the sequencing, assembly and annotation of new annual and perennial genomes ofM. guttatususing Oxford Nanopore long‐read sequencing technology. In addition to the adaptive inv_chr8A inversion, we identified three other large inversion polymorphisms, including a previously unknown large inversion (inv_chr8B) nested within inv_chr8A. Through population genomic analyses, we determined that the nested inv_chr8B inversion is significantly older than the larger chromosomal inversion in which it resides. We also evaluated the potential role of key candidate genes underlying the phenotypic effects of inv_chr8A. These genes are involved in gibberellin biosynthesis and anthocyanin regulation. Although little evidence was found to suggest that inversion breakpoint mutations drive adaptive phenotypic effects, our findings do support the supergene mechanism of adaptation and suggest it may sometimes involve nested inversions that evolve at different times. 

Abstract PremiseA key goal of evolutionary biologists is to understand how and why genetic variation is partitioned within species. In the yellow monkeyflower,Mimulus guttatus(syn.Erythranthe guttata), coastal perennial populations constitute a single genetically and morphologically differentiated ecotype compared to inlandM. guttatuspopulations. While the coastal ecotype's distinctiveness has now been well documented, there is also environmental variation across the ecotype's range that could drive more continuous differentiation among its component populations. MethodsBased on previous observations of a potential cline within this ecotype, we quantified plant height, among other traits, across coastal perennial accessions from 74 populations in a greenhouse common garden experiment. To evaluate potential drivers of the relationship between trait variation and latitude, we regressed height against multiple climatic factors, including temperature, precipitation, and coastal wind speeds. We also accounted for exposure to the open ocean in all analyses. ResultsMultiple traits were correlated with latitude of origin, but none more than plant height. Height was negatively correlated with latitude, and plants directly exposed to the open ocean were shorter than those protected from coastal winds. Further analyses revealed that height was correlated with climatic factors (precipitation, temperature, and wind speeds) that were autocorrelated with latitude. We hypothesize that one or more of these climatic factors drove the evolution of latitudinal clinal variation within the coastal ecotype. ConclusionsOverall, our study illustrates the complexity of how the distribution of environmental variation can simultaneously drive the evolution of both distinct ecotypesandcontinuous clines within those ecotypes. 

Summary In coevolving species, parasites locally adapt to host populations as hosts locally adapt to resist parasites. Parasites often outpace host local adaptation since they have rapid life cycles, but host diversity, the strength of selection, and external environmental influence can result in complex outcomes.To better understand local adaptation in host–parasite systems, we examined locally adapted switchgrass (Panicum virgatum), and its leaf rust pathogen (Puccinia novopanici) across a latitudinal range in North America. We grew switchgrass genotypes in 10 replicated multiyear common gardens, measuring rust severity from natural infection in a ‘host reciprocal transplant’ framework for testing local adaptation. We conducted genome‐wide association mapping to identify genetic loci associated with rust severity.Genetically differentiated rust populations were locally adapted to northern and southern switchgrass, despite host local adaptation to environmental conditions in the same regions. Rust resistance was polygenic, and distinct loci were associated with rust severity in the north and south. We narrowed a previously identified large‐effect quantitative trait locus for rust severity to a candidate YELLOW STRIPE‐LIKE gene and linked numerous other loci to defense‐related genes.Overall, our results suggest that both hosts and parasites can be simultaneously locally adapted, especially when parasites impose less selection than other environmental factors. 

Abstract Despite multiple ecological and evolutionary hypotheses that predict patterns of phenotypic relationships between plant growth, reproduction and constitutive and/or induced resistance to herbivores, these hypotheses do not make any predictions about the underlying molecular genetic mechanisms that mediate these relationships.We investigated how divergent plant life‐history strategies in the yellow monkeyflower and a life‐history altering locus,DIV1, influence plasticity of phytochemical herbivory resistance traits in response to attack by two herbivore species with different diet breadth.Life‐history strategy (annual vs. perennial) and theDIV1locus significantly influenced levels of constitutive herbivory resistance, as well as resistance induction following both generalist and specialist herbivory. Perennial plants had higher total levels of univariate constitutive and induced defence than annuals, regardless of herbivore type. Annuals induced less in response to generalist herbivory than did perennials, while induction response was equivalent across the ecotypes for specialist herbivory.The effects of theDIV1locus on levels of constitutive and induced defence were dependent on genetic background, the annual versus perennial haplotype ofDIV1and herbivore identity. The patterns of univariate induction due toDIV1were non‐additive and did not always match expectations based on patterns of divergence for annual/perennial parents. For example, perennial plants had higher levels of constitutive and induced defence than did annuals, but when the annualDIV1was present in the perennial genetic background induction response to herbivory was higher than for the perennial parent lines.Patterns for multivariate defence arsenals generally echoed those of univariate, with annual and perennial monkeyflowers and those with alternative versions ofDIV1differing significantly in constitutive and induced resistance. Like univariate resistance, induced multivariate defence arsenals were affected by herbivore identity.Our results highlight the complexity of the genetic mechanisms underlying plastic response to herbivory. While a genetic locus underlying substantial phenotypic variation in life‐history strategy and constitutive defence also influences defence plasticity, the induction response also depends on genetic background. This result demonstrates the potential for some degree of evolutionary independence between constitutive and induced defence, or induced defence and life‐history strategy, in monkeyflowers. Read the freePlain Language Summaryfor this article on the Journal blog. 

Abstract In a rapidly changing environment, predicting changes in the growth and survival of local populations can inform conservation and management. Plastic responses vary as a result of genetic differentiation within and among species, so accurate rangewide predictions require characterization of genotype-specific reaction norms across the continuum of historic and future climate conditions comprising a species’ range. Natural hybrid zones can give rise to novel recombinant genotypes associated with high phenotypic variability, further increasing the variance of plastic responses within the ranges of the hybridizing species. Experiments that plant replicated genotypes across a range of environments can characterize genotype-specific reaction norms; identify genetic, geographic, and climatic factors affecting variation in climate responses; and make predictions of climate responses across complex genetic and geographic landscapes. The North American hybrid zone ofPopulus trichocarpaandP. balsamiferarepresents a natural system in which reaction norms are likely to vary with underlying genetic variation that has been shaped by climate, geography, and introgression. Here, we leverage a dataset containing 45 clonal genotypes of varying ancestry from this natural hybrid zone, planted across 17 replicated common garden experiments spanning a broad climatic range, including sites warmer than the natural species ranges. Growth and mortality were measured over two years, enabling us to model reaction norms for each genotype across these tested environments. Genomic variation associated with species ancestry and northern/southern regions significantly influenced growth across environments, with genotypic variation in reaction norms reflecting a trade-off between cold tolerance and growth. Using modeled reaction norms for each genotype, we predicted that genotypes with moreP. trichocarpaancestry may gain an advantage under warmer climates. Spatial shifts of the hybrid zone could facilitate the spread of beneficial alleles into novel climates. These results highlight that genotypic variation in responses to temperature will have landscape-level effects. 

Abstract PremiseIncreased aridity and drought associated with climate change are exerting unprecedented selection pressures on plant populations. Whether populations can rapidly adapt, and which life history traits might confer increased fitness under drought, remain outstanding questions. MethodsWe utilized a resurrection ecology approach, leveraging dormant seeds from herbarium collections to assess whether populations ofPlantago patagonicafrom the semi‐arid Colorado Plateau have rapidly evolved in response to approximately ten years of intense drought in the region. We quantified multiple traits associated with drought escape and drought resistance and assessed the survival of ancestors and descendants under simulated drought. ResultsDescendant populations displayed a significant shift in resource allocation, in which they invested less in reproductive tissues and relatively more in both above‐ and below‐ground vegetative tissues. Plants with greater leaf biomass survived longer under terminal drought; moreover, even after accounting for the effect of increased leaf biomass, descendant seedlings survived drought longer than their ancestors. ConclusionsOur results document rapid adaptive evolution in response to climate change in a selfing annual and suggest that shifts in tissue allocation strategies may underlie adaptive responses to drought in arid or semi‐arid environments. This work also illustrates a novel approach, documenting that under specific circumstances, seeds from herbarium specimens may provide an untapped source of dormant propagules for future resurrection experiments.