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Gene expression can be highly plastic in response to environmental variation. However, we know little about how expression plasticity is shaped by natural selection and evolves in wild and domesticated species. We used genotypic selection analysis to characterize selection on drought-induced plasticity of over 7,500 leaf transcripts of 118 rice accessions (genotypes) from different environmental conditions grown in a field experiment. Gene expression plasticity was neutral for most gradually plastic transcripts, but transcripts with discrete patterns of expression showed stronger selection on expression plasticity. Whether plasticity was adaptive and co-gradient or maladaptive and counter-gradient varied among varietal groups. No transcripts that experienced selection for plasticity across environments showed selection against plasticity within environments, indicating a lack of evidence for costs of adaptive plasticity that may constrain its evolution. Selection on expression plasticity was influenced by degree of plasticity, transcript length and gene body methylation. We observed positive selection on plasticity of co-expression modules containing transcripts involved in photosynthesis, translation and responsiveness to abiotic stress. Taken together, these results indicate that patterns of selection on expression plasticity were context-dependent and likely associated with environmental conditions of varietal groups, but that the evolution of adaptive plasticity would likely not be constrained by opposing patterns of selection on plasticity within compared to across environments. These results offer a genome-wide view of patterns of selection and ecological constraints on gene expression plasticity and provide insights into the interplay between plastic and evolutionary responses to drought at the molecular level.

Accurately predicting responses to selection is a major goal in biology and important for successful crop breeding in changing environments. However, evolutionary responses to selection can be constrained by such factors as genetic and cross-environment correlations, linkage, and pleiotropy, and our understanding of the extent and impact of such constraints is still developing. Here, we conducted a field experiment to investigate potential constraints to selection for drought resistance in rice (Oryza sativa) using phenotypic selection analysis and quantitative genetics. We found that traits related to drought response were heritable, and some were under selection, including selection for earlier flowering, which could allow drought escape. However, patterns of selection generally were not opposite under wet and dry conditions, and we did not find individual or closely linked genes that influenced multiple traits, indicating a lack of evidence that antagonistic pleiotropy, linkage, or cross-environment correlations would constrain selection for drought resistance. In most cases, genetic correlations had little influence on responses to selection, with direct and indirect selection largely congruent. The exception to this was seed mass under drought, which was predicted to evolve in the opposite direction of direct selection due to correlations. Because of this indirect effect on selection on seed mass, selection for drought resistance was not accompanied by a decrease in seed mass, and yield increased with fecundity. Furthermore, breeding lines with high fitness and yield under drought also had high fitness and yield under wet conditions, indicating that there was no evidence for a yield penalty on drought resistance. We found multiple genes in which expression influenced both water use efficiency (WUE) and days to first flowering, supporting a genetic basis for the trade-off between drought escape and avoidance strategies. Together, these results can provide helpful guidance for understanding and managing evolutionary constraints and breeding stress-resistant crops.

There is now abundant evidence of rapid evolution in natural populations, but the genetic mechanisms of these changes remain unclear. One possible route to rapid evolution is through changes in the expression of genes that influence traits under selection. We examined contemporary evolutionary gene expression changes in plant populations responding to environmental fluctuations. We compared genome-wide gene expression, using RNA-seq, in two populations of Brassica rapa collected over four time points between 1997 and 2014, during which precipitation in southern California fluctuated dramatically and phenotypic and genotypic changes occurred. By combining transcriptome profiling with the resurrection approach, we directly examined evolutionary changes in gene expression over time. For both populations, we found a substantial number of differentially expressed genes between generations, indicating rapid evolution in the expression of many genes. Using existing gene annotations, we found that many changes occurred in genes involved in regulating stress responses and flowering time. These appeared related to the fluctuations in precipitation and were potentially adaptive. However, the evolutionary changes in gene expression differed across generations within and between populations, indicating largely independent evolutionary trajectories across populations and over time. Our study provides strong evidence for rapid evolution in gene expression, and indicates that changes in gene expression can be one mechanism of rapid evolutionary responses to selection episodes. This study also illustrates that combining resurrection studies with transcriptomics is a powerful approach for investigating evolutionary changes at the gene regulatory level, and will provide new insights into the genetic basis of contemporary evolution.

Levels of gene expression underpin organismal phenotypes1,2, but the nature of selection that acts on gene expression and its role in adaptive evolution remain unknown1,2. Here we assayed gene expression in rice (Oryza sativa)3, and used phenotypic selection analysis to estimate the type and strength of selection on the levels of more than 15,000 transcripts4,5. Variation in most transcripts appears (nearly) neutral or under very weak stabilizing selection in wet paddy conditions (with median standardized selection differentials near zero), but selection is stronger under drought conditions. Overall, more transcripts are conditionally neutral (2.83%) than are antagonistically pleiotropic6 (0.04%), and transcripts that display lower levels of expression and stochastic noise7-9 and higher levels of plasticity9 are under stronger selection. Selection strength was further weakly negatively associated with levels of cis-regulation and network connectivity9. Our multivariate analysis suggests that selection acts on the expression of photosynthesis genes4,5, but that the efficacy of selection is genetically constrained under drought conditions10. Drought selected for earlier flowering11,12 and a higher expression of OsMADS18 (Os07g0605200), which encodes a MADS-box transcription factor and is a known regulator of early flowering13-marking this gene as a drought-escape gene11,12. The ability to estimate selection strengths provides insights into how selection can shape molecular traits at the core of gene action.

As climatic conditions change, species will be forced to move or adapt to avoid extinction. Exacerbated by ongoing climate change, California recently experienced a severe and exceptional drought from 2011 to 2017. To investigate whether an adaptive response occurred during this event, we conducted a "resurrection" study of the cutleaf monkeyflower (Mimulus laciniatus), an annual plant, by comparing trait means and variances of ancestral seed collections ("pre-drought") with contemporary descendant collections ("drought"). Plants were grown under common conditions to test whether this geographically restricted species has the capacity to respond evolutionarily to climate stress across its range. We examined if traits shifted in response to the recent, severe drought and included populations across an elevation gradient, including populations at the low- and high-elevation edges of the species range. We found that time to seedling emergence in the drought generation was significantly earlier than in the pre-drought generation, a response consistent with drought adaptation. Additionally, trait variation in days to emergence was reduced in the drought generation, which suggests selection or bottleneck events. Days to first flower increased significantly by elevation, consistent with climate adaptation across the species range. Drought generation plants were larger and had greater reproduction, which was likely a carryover effect of earlier germination. These results demonstrate that rapid shifts in trait means and variances consistent with climate adaptation are occurring within populations, including peripheral populations at warm and cold climate limits, of a plant species with a relatively restricted range that has so far not shifted its elevation distribution during contemporary climate change. Thus, rapid evolution may mitigate, at least temporarily, range shifts under global climate change. This study highlights the need for better understanding rapid adaptation as a means for plant communities to cope with extraordinary climate events.

The resurrection approach of reviving ancestors from stored propagules and comparing them with descendants under common conditions has emerged as a powerful method of detecting and characterizing contemporary evolution. As climatic and other environmental conditions continue to change at a rapid pace, this approach is becoming particularly useful for predicting and monitoring evolutionary responses. We evaluate this approach, explain the advantages and limitations, suggest best practices for implementation, review studies in which this approach has been used, and explore how it can be incorporated into conservation and management efforts. We find that although the approach has thus far been used in a limited number of cases, these studies have provided strong evidence for rapid contemporary adaptive evolution in a variety of systems, particularly in response to anthropogenic environmental change, although it is far from clear that evolution will be able to rescue many populations from extinction given current rates of global changes. We also highlight one effort, known as Project Baseline, to create a collection of stored seeds that can take advantage of the resurrection approach to examine evolutionary responses to environmental change over the coming decades. We conclude that the resurrection approach is a useful tool that could be more widely employed to examine basic questions about evolution in natural populations and to assist in the conservation and management of these populations as they face continued environmental change.

Premise of the studyProject Baseline is a seed bank that offers an unprecedented opportunity to examine spatial and temporal dimensions of microevolution during an era of rapid environmental change. Over the upcoming 50 years, biologists will withdraw genetically representative samples of past populations from this time capsule of seeds and grow them contemporaneously with modern samples to detect any phenotypic and molecular evolution that has occurred during the intervening time.MethodsWe carefully developed this living genome bank using protocols to enhance its experimental value by collecting from multiple populations and species across a broad geographical range in sites that are likely to be preserved into the future. Seeds are accessioned with site and population data and are stored by maternal line under conditions that maximize seed longevity. This open-access resource will be available to researchers at regular intervals to evaluate contemporary evolution.Key resultsTo date, the Project Baseline collection includes 100-200 maternal lines of each of 61 species collected from over 831 populations on sites that are likely to be preserved into the future across the United States (∼78,000 maternal lines). Our strategically designed collection circumvents some problems that can cloud the results of "resurrection" studies involving naturally preserved or existing seed collections that are available fortuitously.ConclusionsThe resurrection approach can be coupled with long-established and newer techniques over the next five decades to elucidate genetic change and thereby vastly improve our understanding of temporal and spatial changes in phenotype and the evolutionary processes underlying it.

Understanding the genetic basis of natural phenotypic variation is of great importance, particularly since selection can act on this variation to cause evolution. We examined expression and allelic variation in candidate flowering time loci in Brassica rapa plants derived from a natural population and showing a broad range in the timing of first flowering. The loci of interest were orthologs of the Arabidopsis genes FLC and SOC1 (BrFLC and BrSOC1, respectively), which in Arabidopsis play a central role in the flowering time regulatory network, with FLC repressing and SOC1 promoting flowering. In B. rapa, there are four copies of FLC and three of SOC1. Plants were grown in controlled conditions in the lab. Comparisons were made between plants that flowered the earliest and latest, with the difference in average flowering time between these groups ∼30 days. As expected, we found that total expression of BrSOC1 paralogs was significantly greater in early than in late flowering plants. Paralog-specific primers showed that expression was greater in early flowering plants in the BrSOC1 paralogs Br004928, Br00393 and Br009324, although the difference was not significant in Br009324. Thus expression of at least 2 of the 3 BrSOC1 orthologs is consistent with their predicted role in flowering time in this natural population. Sequences of the promoter regions of the BrSOC1 orthologs were variable, but there was no association between allelic variation at these loci and flowering time variation. For the BrFLC orthologs, expression varied over time, but did not differ between the early and late flowering plants. The coding regions, promoter regions and introns of these genes were generally invariant. Thus the BrFLC orthologs do not appear to influence flowering time in this population. Overall, the results suggest that even for a trait like flowering time that is controlled by a very well described genetic regulatory network, understanding the underlying genetic basis of natural variation in such a quantitative trait is challenging.

The maintenance of outcrossing in cleistogamous plants that produce both open, facultatively outcrossing chasmogamous (CH), and closed, obligate selfing cleistogamous (CL) flowers is puzzling because CL reproduction is thought to be more reliable and less costly. A possible explanation for the maintenance of CH flowers is the avoidance of inbreeding depression. However, inbreeding depression for cleistogamous species has rarely been quantified. In this study, we estimate levels of inbreeding depression in plants from three populations of Triodanis perfoliata (L.) Nieuwl., a dimorphic cleistogamous annual, under greenhouse conditions. Estimates of inbreeding depression at multiple life stages in all three populations were low and often not different from zero. Inbreeding depression at specific life stages varied, with two populations showing later-acting inbreeding depression, which is also found in other selfing species. In two of the study populations, selfed CL progeny outperformed selfed CH progeny, indicating a flower-type effect. The low levels of inbreeding depression and the superior fitness of CL compared with selfed CH flowers that weobserved make the maintenanceof CH flowersin this system surprising, and suggest that other advantages of outcrossing CH flowers are likely responsible for maintaining mixed mating in this species. Key words: breeding system, Campanulaceae, cleistogamy, inbreeding depression, mixed mating system, plasticity, reproductive ecology. Resume : Le maintien du croisement eloigne chez les vegetaux cleistogames qui produit tant des fleurs ouvertes, a croisement eloigne chasmogame (CH) facultatif que des fleurs fermees, a autofecondation cleistogame (CL) obligee, est intrigant car la reproduction CL est presumee plus fiable et moins couteuse. Une explication possible pour le maintien de fleurs CH consiste en l'evitement de la depression endogamique. Toutefois, la depression endogamique des especes cleistogames a rarement ete quantifiee. Dans cette etude, les auteurs ont estime les niveaux de depression endogamique chez les plants de trois populations de Triodanis perfoliata (L.) Nieuwl., une plante annuelle dimorphique cleistogame, en conditions de serre. Les estimes de la depression endogamique a differents stades de vie chez les trois populations etaient faibles et souvent non differents de zero. La depression endogamique a un stade de vie specifique variait, avec deux populations montrant une depression endogamique plus tardive, qui etait aussi trouvee chez d'autres especes endogames. Chez deux des populations etudiees, la descendance CL issue de l'autofecondation etait plus performante que la descendance CH issue de l'autofecondation, indiquant un effet du type de fleur. Les faibles niveaux de depression endogamique et la valeur d'adaptation superieure des fleurs CL comparativement aux fleurs CH issues de l'autofecondation, comme observes par les auteurs, rendent le maintien des fleurs CH dans ce systeme surprenant, et suggerent que d'autres avantages du croisement eloigne des fleurs CH sont probablement responsables du maintien du croisement mixte chez cette espece. [Traduit par la Redaction] Mots-cles : systeme de croisement, Campanulaceae, cleistogamie, depression endogamique, systeme de croisement mixte, plasticite, ecologie de la reproduction., Introduction Plant reproductive systems are remarkably diverse, but the major selective pressures affecting the evolution of plant mating strategies can be distilled into a few key ecological and genetic factors. [...]