An official website of the United States government
Populations often vary in their evolutionary responses to a shared environmental perturbation. A key hurdle in building more predictive models of rapid evolution is understanding this variation—why do some populations and traits evolve while others do not? We combined long-term demographic and environmental data, estimates of quantitative genetic variance components, a resurrection experiment and individual-based evolutionary simulations to gain mechanistic insights into contrasting evolutionary responses to a severe multi-year drought. We examined five traits in two populations of a native California plant, Clarkia xantiana , at three time points over 7 years. Earlier flowering phenology evolved in only one of the two populations, though both populations experienced similar drought severity and demographic declines and were estimated to have considerable additive genetic variance for flowering phenology. Pairing demographic and experimental data with evolutionary simulations suggested that while seed banks in both populations likely constrained evolutionary responses, a stronger seed bank in the non-evolving population resulted in evolutionary stasis. Gene flow through time via germ banks may be an important, underappreciated control on rapid evolution in response to extreme environmental perturbations.
more »
« less
Evolution and seed dormancy shape plant genotypic structure through a successional cycle
Dormancy has repeatedly evolved in plants, animals, and microbes and is hypothesized to facilitate persistence in the face of environmental change. Yet previous experiments have not tracked demography and trait evolution spanning a full successional cycle to ask whether early bouts of natural selection are later reinforced or erased during periods of population dormancy. In addition, it is unclear how well short-term measures of fitness predict long-term genotypic success for species with dormancy. Here, we address these issues using experimental field populations of the plant Oenothera biennis , which evolved over five generations in plots exposed to or protected from insect herbivory. While populations existed above ground, there was rapid evolution of defensive and life-history traits, but populations lost genetic diversity and crashed as succession proceeded. After >5 y of seed dormancy, we triggered germination from the seedbank and genotyped >3,000 colonizers. Resurrected populations showed restored genetic diversity that reduced earlier responses to selection and pushed population phenotypes toward the starting conditions of a decade earlier. Nonetheless, four defense and life-history traits remained differentiated in populations with insect suppression compared with controls. These findings capture key missing elements of evolution during ecological cycles and demonstrate the impact of dormancy on future evolutionary responses to environmental change.
more »
« less
- Award ID(s):
- 1907491
- PAR ID:
- 10324656
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 34
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Evolutionary change begins at the population scale. Therefore, understanding adaptive variation requires the identification of the factors maintaining and shaping standing genetic variation at the within‐population level. Spatial and temporal environmental heterogeneity represent ecological drivers of within‐population genetic variation, determining the evolutionary trajectory of populations along with random processes. Here, we focused on the effects of spatiotemporal heterogeneity on quantitative and molecular variation in a natural population of the annual plant Arabidopsis thaliana . We sampled 1093 individuals from a Spanish A. thaliana population across an area of 7.4 ha for 10 years (2012–2021). Based on a sample of 279 maternal lines, we estimated spatiotemporal variation in life‐history traits and fitness from a common garden experiment. We genotyped 884 individuals with nuclear microsatellites to estimate spatiotemporal variation in genetic diversity. We assessed spatial patterns by estimating spatial autocorrelation of traits and fine‐scale genetic structure. We analysed the relationships between phenotypic variation, geographical location and genetic relatedness, as well as the effects of environmental suitability and genetic rarity on phenotypic variation. The common garden experiment indicated that there was more temporal than spatial variation in life‐history traits and fitness. Despite the differences among years, genetic distance in ecologically relevant traits (e.g. flowering time) tended to be positively correlated to genetic distance among maternal lines, while isolation by distance was less important. Genetic diversity exhibited significant spatial structure at short distances, which were consistent among years. Finally, genetic rarity, and not environmental suitability, accounted for genetic variation in life‐history traits. Synthesis . Our study highlighted the importance of repeated sampling to detect the large amount of genetic diversity at the quantitative and molecular levels that a single A. thaliana population can harbour. Overall, population genetic attributes estimated from our long‐term monitoring scheme (genetic relatedness and genetic rarity), rather than biological (dispersal) or ecological (vegetation types and environmental suitability) factors, emerged as the most important drivers of within‐population structure of phenotypic variation in A. thaliana .more » « less
-
ABSTRACT Invasive species with native ranges spanning strong environmental gradients are well suited for examining the roles of selection and population history in rapid adaptation to new habitats, providing insight into potential evolutionary responses to climate change. The Atlantic oyster drill (Urosalpinx cinerea) is a marine snail whose native range spans the strongest coastal latitudinal temperature gradient in the world, with invasive populations established on the US Pacific coast. Here, we leverage this system using genome‐wide SNPs and environmental data to examine invasion history and identify genotype–environment associations indicative of local adaptation across the native range, and then assess evidence for allelic frequency shifts that would signal rapid adaptation within invasive populations. We demonstrate strong genetic structuring among native regions which aligns with life history expectations, identifying southern New England as the source of invasive populations. Then, we identify putatively thermally adaptive loci across the native range but find no evidence of allele frequency shifts in invasive populations that suggest rapid adaptation to new environments. Our results indicate that while these loci may underpin local thermal adaptation in their native range, selection is relaxed in invasive populations, perhaps due to complex polygenic architecture underlying thermal traits and/or standing capacity for phenotypic plasticity. Given the prolific invasion ofUrosalpinx, our study suggests population success in new environments is influenced by factors other than selection on standing genetic variation that underlies local adaptation in the native range and highlights the importance of considering population history and environmental selection pressures when evaluating adaptive capacity.more » « less
-
Abstract Global change has profoundly altered the eco-evolutionary trajectories of plant species. Longitudinal studies often document phenotypic shifts in response to climate change, such as earlier flowering in the spring, but it remains challenging to disentangle the contributions of phenotypic plasticity and adaptive evolution to shifted phenotypic distributions. The resurrection approach has emerged as a powerful method to study genetic and plastic responses to novel selection imposed by global change by contrasting ancestral and descendant lineages from the same population under common conditions. Here, we compiled a database of 52 resurrection studies to examine key hypotheses about plant evolutionary responses to global change using a meta-analysis (40 of the studies) and quantitative review (all 52 studies). We found evidence for rapid, contemporary evolution, which often appeared adaptive, in over half of the cases, including some of the fastest cases of evolution in natural populations ever observed. Annual plants evolved earlier reproduction, and leaf economic traits associated with stress escape strategies. We also found evolution of increased plasticity for annual plants in phenology and physiology traits, and a reduction of plasticity in traits related to the leaf economic spectrum. We found less evidence for evolution in perennial species. Overall, our findings demonstrate the key role of drought escape in plant responses to a warming world. However, the lack of evolution in other traits and species indicates that constraints may dampen evolutionary responses in some scenarios. Our review also suggests promising avenues of future research for resurrection studies.more » « less
-
Despite most angiosperms being perennial, once-flowering annuals have evolved multiple times independently, making life history traits among the most labile trait syndromes in flowering plants. Much research has focused on discerning the adaptive forces driving the evolution of annual species, and in pinpointing traits that distinguish them from perennials. By contrast, little is known about how ‘annual traits’ evolve, and whether the same traits and genes have evolved in parallel to affect independent origins of the annual syndrome. Here, we review what is known about the distribution of annuals in both phylogenetic and environmental space and assess the evidence for parallel evolution of annuality through similar physiological, developmental, and/or genetic mechanisms. We then use temperate grasses as a case study for modeling the evolution of annuality and suggest future directions for understanding annual-perennial transitions in other groups of plants. Understanding how convergent life history traits evolve can help predict species responses to climate change and allows transfer of knowledge between model and agriculturally important species.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1073/pnas.2026212118
