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Lowry, D. B.

Publications and source records attributed to Lowry, D. B..

12 recordsLinked to original sources

Heat stress reveals divergent pollen viability responses across species and populations of monkeyflower

Premise Rising temperatures can reduce plant reproductive success by disrupting pollen development, yet little is known about how reproductive heat sensitivity varies among natural populations. We evaluated pollen viability responses to elevated temperature in two closely related taxa of yellow monkeyflowers across multiple geographic scales to determine whether heat sensitivity varies among species, between populations and across elevations. Methods We conducted three common garden growth chamber experiments. First, we compared pollen viability responses to heat stress between Mimulus guttatus and members of the M. tilingii species complex. Second, we tested whether broad elevational categories explained variation in heat responses. Third, we evaluated heat sensitivity among nine eastern Sierra Nevada populations of M. guttatus spanning an elevational gradient. Pollen viability was assessed following exposure to control and heat treatments. Key results Heat exposure reduced pollen viability in all experiments. In the species comparison experiment, pollen viability decreased more strongly in the high-elevation restricted M. tilingii species complex than the widespread M. guttatus. We found substantial population-level variation in pollen viability within M. guttatus but not members of the M. tilingii complex. Broad elevational categories did not explain this variation in pollen viability responses. However, within eastern Sierra Nevada populations, reductions in pollen viability became stronger with increasing source elevation. Several populations deviated from this trend, indicating reproductive responses to heat cannot be explained by elevation alone. Conclusions Pollen heat sensitivity varies substantially among species and populations of yellow monkeyflowers. Elevation alone is insufficient to predict pollen viability responses to elevated temperatures, suggesting that local adaptation or genetic variation may contribute to reproductive heat tolerance. Some populations of M. guttatus may contain greater capacity to maintain reproductive function under future warming, highlighting the importance of considering intraspecific variation when predicting plant responses to climate change.

plant biology↗

Phenotypic plasticity evolved for climate variability constrains performance under climate warming

Phenotypic plasticity allows plants to rapidly respond to changing environments without the need for evolutionary change or migration. While selection can create variation in plasticity across natural populations, these responses are not adaptive in all environments. To predict whether plasticity will be adaptive requires evaluation of its fitness effects across a range of environments, including novel ones. Here, we test how traits and their plasticity vary for genotypes collected across a natural hybrid zone between two tree species with contrasting climatic niches. Fast-growing Populus trichocarpa inhabits maritime environments with relatively warm and stable temperatures, while P. balsamifera inhabits continental environments with cold winters and large temperature variance throughout the year. We planted 44 clonally replicated genotypes into thirteen common gardens and measured vegetative phenology, leaf morphology, stomata morphology and conductance, and photochemistry. Overall, genotypes from colder, more continental environments exhibited higher plasticity. P. balsamifera ancestry was associated with increased plasticity in timing of fall phenology, stomatal conductance, and leaf mass per unit area. We assessed the effects of trait plasticity on fitness estimated as yearly growth across common gardens and found that the plasticity-fitness relationship was often garden-specific, indicating that the planting environment did not consistently mediate plasticity-fitness relationships. When the effects of trait plasticity on growth varied by garden temperature, higher plasticity generally had neutral or negative associations with growth in warmer environments. These results suggest that elevated plasticity evolved in a P. balsamifera genomic background as part of a climate generalist strategy to seasonal temperature variability, but that there is a trade-off between plasticity and growth in warmer environments. Consequently, less-plastic but warm-adapted P. trichocarpa genotypes are likely to have a fitness advantage under warming climates. These results demonstrate that plasticity may sometimes be maladaptive and will not be universally beneficial in a warming world.

evolutionary biology↗

Variation in responses to temperature across admixed genotypes of Populus trichocarpa x P. balsamifera predict geographic shifts in regions where hybrids are favored

O_LIPlastic responses of plants to their environment vary as a result of genetic differentiation within and among species. To accurately predict rangewide responses to climate change, it is necessary to characterize genotype-specific reaction norms across the continuum of historic and future climate conditions comprising a species range. C_LIO_LIThe North American hybrid zone of Populus trichocarpa and P. balsamifera represents a natural system that has been shaped by climate, geography, and introgression. We leverage a dataset containing 45 clonal genotypes from this natural hybrid zone, planted across 17 replicated common garden experiments spanning a broad climatic range. Growth and mortality were measured over two years, enabling us to model reaction norms for each genotype across these tested environments. C_LIO_LISpecies ancestry and intraspecific genomic variation 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 more P. trichocarpa ancestry may gain an advantage under warmer climates. C_LIO_LISpatial 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. C_LI

evolutionary biology↗

Gene expression divergence between locally adapted inland annual and coastal perennial ecotypes of Mimulus guttatus across developmental stages

The action of natural selection across heterogeneous natural landscapes drives local adaptation and the formation of plant ecotypes, the precursors to new species. Plant ecotypes typically differ significantly in morphology, physiology, and development, yet our understanding of their underlying genetic basis remains limited. Despite their importance, studies of the molecular underpinnings of ecotypic divergence through developmental stages are rare. Here, we compared gene expression at different developmental time points between ecologically reproductively isolated coastal perennial and inland annual ecotypes of the yellow monkeyflower, Mimulus guttatus. We took two major approaches to understand differences in gene regulation between the ecotypes at the level of gene networks. First, we evaluated expression variation between the ecotypes in candidate molecular pathways. Next, we conducted gene co-expression network analyses to identify new candidate mechanisms driving ecotypic divergence. Overall, we found significant differences in global expression between the ecotypes and across developmental stages. Among the candidate pathways we evaluated, genes in the jasmonic acid pathway were the most significantly enriched for divergent gene expression. This includes the most differentially expressed gene in our analyses, which is a key gene (cytochrome P450 CYP94B1) involved in the degradation of bioactive jasmonic acid. Our gene co-expression network analysis revealed different but complementary insights into the differential regulation of genes between the ecotypes, especially at a more microscopic level of these organisms. Overall, our research further supports the hypothesis that plant hormone pathways play a crucial role in the evolution of plant ecotypes and, consequently, the emergence of new species.

evolutionary biology↗

Local adaptation of both plant and pathogen: an arms-race compromise in switchgrass rust

O_LIIn widespread species, parasites can locally adapt to host populations, or hosts can locally adapt to resist parasites. Parasites with rapid life cycles locally adapt more quickly, but host diversity, selective pressure, and climatic factors impact coevolution. C_LIO_LITo better understand local adaptation in co-evolved host-parasite systems, we examined switchgrass (Panicum virgatum), and its leaf rust pathogen (Puccinia novopanici) across a latitudinal range in North America. We grew diverse switchgrass genotypes in ten replicated common gardens spanning 16.78{degrees} latitude for three years, measuring rust severity from natural infection. We conducted genome wide association mapping to identify genetic loci associated with rust severity. C_LIO_LIGenetically differentiated rust populations were locally adapted to northern and southern switchgrass, despite host local adaptation in the same regions. Rust resistance was highly polygenic, and distinct loci were associated with rust severity in the north and south. We narrowed a previously identified large-effect QTL for rust severity to a candidate YSL3-like gene, and linked numerous other loci to immunity-related genes. C_LIO_LIBoth hosts and parasites can be locally adapted when parasites have a lower impact on fitness than other local selection pressures. In switchgrass, our results suggest variation in fungal resistance mechanisms between locally adapted regions. C_LI

evolutionary biology↗

A cline within an ecotype of the yellow monkeyflower, Mimulus guttatus

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 collectively constitute a single genetically and morphologically differentiated ecotype compared to inland populations of M. guttatus. While the distinctiveness of the coastal ecotype has now been well documented, there is also variation in environmental factors across the range of the coastal ecotype that could drive differentiation among its component populations in a more continuous way. MethodsBased on previous observations of a potential cline within this ecotype, we quantified plant height across coastal perennial accessions from 74 total populations in a greenhouse common garden experiment. To evaluate possible environmental factors driving the relationship between trait variation and latitude, we regressed height against multiple climatic factors, including temperature, precipitation, and coastal wind speeds. ResultsMultiple traits were correlated with latitude of origin, but none more than plant height. Plant height was negatively correlated with latitude and plants directly exposed to the open ocean were shorter than those that were more protected from onshore coastal winds. Further analyses revealed that height was correlated with climatic factors (precipitation, temperature, and windspeeds) 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. ConclusionOverall, our study illustrates the complexity of how the distribution of environmental variation can simultaneously drive the evolution of distinct ecotypes as well as continuous clines within those ecotypes.

evolutionary biology↗

Heritability and host genomic determinants of switchgrass root-associated microbiota in field sites spanning its natural range.

A fundamental goal in plant microbiome research is to determine the relative impacts of host and environmental effects on root microbiota composition, particularly how host genotype impacts bacterial community composition. Most studies characterizing the effect of plant genotype on root microbiota undersample host genetic diversity and grow plants outside of their native ranges, making the associations between host and microbes difficult to interpret. Here we characterized the root microbiota of a large population of switchgrass, a North American native C4 bioenergy crop, in three field locations spanning its native range. Our data, composed of >2000 samples, suggest field location is the primary determinant of microbiome composition; however, substantial heritable variation is widespread across bacterial taxa, especially those in the Sphingomonadaceae family. Despite diverse compositions, we find that relatively few highly prevalent bacterial taxa make up the majority of the switchgrass root microbiota, a large fraction of which is shared across sites. Local genotypes preferentially recruit / filter for local microbes, supporting the idea of affinity between local plants and their microbiota. Using genome-wide association, we identified loci impacting the abundance of >400 microbial strains and found an enrichment of genes involved in immune responses, signaling pathways, and secondary metabolism. We found loci associated with over half of the core microbiota (i.e. microbes in >80% of samples) regardless of field location. Finally, we show a genetic relationship between a basal plant immunity pathway and relative abundances of root microbiota. This study brings us closer to harnessing and manipulating beneficial microbial associations via host genetics.

plant biology↗

Mapping of genotype-by-environment interactions in phenology identifies two cues for flowering in switchgrass (Panicum virgatum)

The timing of vegetative and reproductive growth in plants ("phenological timings") depend on genetic effects (G), environmental (e.g., weather) cues, and their interaction. Here, we measure phenological timings in two highly divergent switchgrass (Panicum virgatum) subpopulations using repeated plantings of cloned individuals at eight sites across the central United States. The timing of vegetative growth for the two subpopulations reversed between their two natural ranges and had strong negative correlations between these regions; in contrast, the timing of flowering was positively correlated between gardens. We expect that these phenotypic correlations consist of polygenic effects on phenology which have distinct patterns of GxE segregating at different mapped loci. Thus, we infer the mixture of ways genetic effects impact phenological timings, such as across common gardens (GxE) or with weather cues (GxWeather). We demonstrate that we can identify genetic variation with GxWeather and assign genetic loci to specific weather-based cues or other patterns. For example, in the Gulf subpopulation, 65% of genetic effects on the timing of vegetative growth covary with daylength 14 days prior to green-up date, and 33% of genetic effects on the timing of flowering covary with cumulative rainfall in the week prior to flowering. However, most variation in genetic effects cannot be attributed to variation in weather variables. Selective breeding for particular alleles at GxWeather loci could alter flowering responsiveness in a photoperiod or rainfall-specific way. More broadly, our approach refines the characterization of genotype-by-environment interactions and can be implemented in any species phenotyped in multiple environments.

genetics↗

Locally-adapted Mimulus ecotypes differentially impact rhizosphere bacterial and archaeal communities in an environment-dependent manner

Plant root-microbe interactions influence plant productivity, health, and resistance to stress. Although there is evidence that plant species and even genotypes can alter soil microbial community structure, environmental conditions can potentially outweigh plant genetic effects. Here, we used a reciprocal transplant experiment to understand the contributions of the environment and the host plant to rhizosphere microbiome composition in locally-adapted ecotypes of Mimulus guttatus (syn. Erythranthe guttata (Fisch. ex DC.) G.L. Nesom). Two genotypes of a coastal ecotype and two genotypes of an inland ecotype were planted at coastal and inland sites. After three months, we collected rhizosphere and bulk soil and assessed microbial communities by 16S rRNA gene sequencing. We found that local environment (coastal versus inland site) strongly influenced rhizosphere communities, at least in part due to distinct local microbial species pools. Host identity played a smaller role: at each site, the ecotypes exhibited remarkably similar composition of microbial communities at the class level, indicating that divergent M. guttatus ecotypes recruit phylogenetically similar rhizosphere communities, even in environments to which they are maladapted. Nevertheless, the two ecotypes significantly differed in community composition at the inland site due to an exclusive set of rare taxa associated with each ecotype. Although our results indicate that locally-adapted M. guttatus ecotypes are genetically diverged in factors shaping rhizosphere communities, environmental factors can trump genetic factors in shaping the M. guttatus microbiome. Overall, our findings demonstrate that wild plants strongly impact root-associated microbial communities, but hierarchical drivers interact to shape microbial community assembly outcomes.

plant biology↗

Geographic variation in the genetic basis of resistance to leaf rust in locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)

O_LILocal adaptation is an important process in plant evolution, which can be impacted by differential pathogen pressures along environmental gradients. However, the degree to which pathogen resistance loci vary in effect across space and time is incompletely described. C_LIO_LITo understand how the genetic architecture of resistance varies across time and geographic space, we quantified rust (Puccinia spp.) severity in switchgrass (Panicum virgatum) plantings at eight locations across the central United States for three years and conducted quantitative trait locus (QTL) mapping for rust progression. C_LIO_LIWe mapped several variable QTLs, but two large-effect QTLs which we have named Prr1 and Prr2 were consistently associated with rust severity in multiple sites and years, particularly in northern sites. In contrast, there were numerous small-effect QTLs at southern sites, indicating a genotype-by-environment interaction in rust resistance loci. Interestingly, Prr1 and Prr2 had a strong epistatic interaction, which also varied in strength and direction of effect across space. C_LIO_LIOur results suggest that abiotic factors covarying with latitude interact with the genetic loci underlying plant resistance to control rust infection severity. Further, our results indicate that segregating genetic variation in epistatically interacting loci may play a key role in determining response to infection across geographic space. C_LI

genomics↗

Oceanic salt spray and herbivore pressure contribute to local adaptation of coastal perennial and inland annual ecotypes of the Seep Monkeyflower (Mimulus guttatus)

Identifying the environmental factors responsible for natural selection across different habitats is crucial for understanding the process of local adaptation. Despite its importance, only a few studies have successfully isolated the environmental factors driving local adaptation in nature. In this study, we evaluated the agents of selection responsible local adaptation of the monkeyflower Mimulus guttatus to coastal and inland habitats in California. We implemented a manipulative field reciprocal transplant experiment at coastal and inland sites, where we excluded aboveground stressors in an effort to elucidate their role in the evolution of local adaptation. We found that excluding these stressors, most likely a combination of salt spray and herbivory, completely rescued inland plant fitness when transplanted to coastal habitat. In contrast, the exclosures in inland habitat provided limited fitness benefit for either coastal or inland plants. We have previously established that low soil water availability belowground is the most important agent of selection in inland habitat. Therefore, our study demonstrates that a distinct set of selective agents are responsible for local adaptation at opposite ends of an environmental gradient.

evolutionary biology↗

The Gene Regulatory Landscape of Local Adaptation

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. Further, 18% of transcripts had significant genotype x site (GxE) effects. Habitat-specific differential expression was found for 62% of the GxE transcripts (differential expression in one habitat, but not the other), while only 94 ([~]5%) GxE transcripts had crossing reaction norms. Cis-regulatory variation was pervasive, affecting 79% (5532) of differentially expressed genes. We detected trans effects for 52% (3611) of differentially expressed genes. Consistent with the supergene hypothesis of chromosome inversion evolution, a locally adaptive inversion was enriched for cis-regulatory divergence. These results provide multiple new insights into the evolution of transcriptome-wide gene regulatory divergence and plasticity among locally adapted populations.

evolutionary biology↗