skip to main content


Title: 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 plantOenothera 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
NSF-PAR ID:
10287589
Author(s) / Creator(s):
; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
118
Issue:
34
ISSN:
0027-8424
Page Range / eLocation ID:
Article No. e2026212118
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Adaptation to novel environments can result in unanticipated genomic responses to selection. Here, we illustrate how multifarious, correlational selection helps explain a counterintuitive pattern of genetic divergence between the recently derived apple‐ and ancestral hawthorn‐infesting host races ofRhagoletis pomonella(Diptera: Tephritidae). The apple host race terminates diapause and emerges as adults earlier in the season than the hawthorn host race, to coincide with the earlier fruiting phenology of their apple hosts. However, alleles at many loci associated with later emergence paradoxically occur at higher frequencies in sympatric populations of the apple compared to the hawthorn race. We present genomic evidence that historical selection over geographically varying environmental gradients across North America generated genetic correlations between two life history traits, diapause intensity and diapause termination, in the hawthorn host race. Moreover, the loci associated with these life history traits are concentrated in genomic regions in high linkage disequilibrium (LD). These genetic correlations are antagonistic to contemporary selection on local apple host race populations that favours increased initial diapause depth and earlier, not later, diapause termination. Thus, the paradox of apple flies appears due, in part, to pleiotropy or linkage of alleles associated with later adult emergence and increased initial diapause intensity, the latter trait strongly selected for by the earlier phenology of apples. Our results demonstrate how understanding of multivariate trait combinations and the correlative nature of selective forces acting on them can improve predictions concerning adaptive evolution and help explain seemingly counterintuitive patterns of genetic diversity in nature.

     
    more » « less
  2. Abstract

    Despite extensive research on agricultural pests, our knowledge about their evolutionary history is often limited. A mechanistic understanding of the demographic changes and modes of adaptation remains an important goal, as it improves our understanding of organismal responses to environmental change and our ability to sustainably manage pest populations. Emerging genomic datasets now allow for characterization of demographic and adaptive processes, but face limits when they are drawn from contemporary samples, especially in the context of strong demographic change, repeated selection, or adaptation involving modest shifts in allele frequency at many loci. Temporal sampling, however, can improve our ability to reconstruct evolutionary events. Here, we leverage museum samples to examine whether population genomic diversity and structure has changed over time, and to identify genomic regions that appear to be under selection. We focus on the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say 1824; Coleoptera: Chrysomelidae), which is widely regarded as a super-pest due to its rapid, and repeated, evolution to insecticides. By combining whole genome resequencing data from 78 museum samples with modern sampling, we demonstrate that CPB expanded rapidly in the 19th century, leading to a reduction in diversity and limited genetic structure from the Midwest to Northeast United States. Temporal genome scans provide extensive evidence for selection acting in resistant field populations in Wisconsin and New York, including numerous known insecticide resistance genes. We also validate these results by showing that known selective sweeps in modern populations are identified by our genome scan. Perhaps most importantly, temporal analysis indicates selection on standing genetic variation, as we find evidence for parallel evolution in the two geographical regions. Parallel evolution involves a range of phenotypic traits not previously identified as under selection in CPB, such as reproductive and morphological functional pathways that might be important for adaptation to agricultural habitats.

     
    more » « less
  3. Abstract

    Because foundation species create structure in a community, understanding their ecological and evolutionary responses to global change is critical for predicting the ecological and economic management of species and communities that rely on them. Giant kelp (Macrocystis pyrifera) is a globally distributed foundation species with seasonal fluctuations in abundance in response to local nutrient levels, storm intensity, and ocean temperatures. Here we examine genetic variation in individual and population‐level responses of early life history stages (zoospore settlement, survival, and gametogenesis) to increased temperatures to determine the potential for natural selection on temperature‐tolerant individuals that would allow adaptation to a changing climate. We collected fertileM. pyriferasporophyll blades from three sites along the California coast (Los Angeles, Santa Barbara, Monterey Bay) and induced zoospore release in the lab. Spores settled on microscope slides at three treatment temperatures (16, 20, and 22°C), matured for 21 days, and were imaged weekly to determine settlement, survival, and maturation success. On average, individuals from all sites showed lower rates of settlement and maturation in response to increasing temperature. However, the magnitude of the responses to temperature varied among populations. Survival tended to increase with temperature in Los Angeles and Santa Barbara populations but decreased with increasing temperature for the Monterey Bay population. We observed little genetic variation in temperature responses among individuals within sites, suggesting little scope for evolution within populations to increase the resilience ofM. pyriferapopulations to warming ocean temperatures and predicted declines in kelp abundance. Yet sufficient dispersal among populations could allow for adaptation of early life history traits among populations via evolutionary rescue of declining populations.

     
    more » « less
  4. Abstract

    To establish and spread in a new location, an invasive species must be able to carry out its life cycle in novel environmental conditions. A key trait underlying fitness is the shift from vegetative to reproductive growth through floral development. In this study, we used a common garden experiment and genotyping‐by‐sequencing to test whether the latitudinal flowering cline of the North American invasive plantMedicago polymorphawas translocated from its European native range through multiple introductions, or whether the cline rapidly established due to evolution following a genetic bottleneck. Analysis of flowering time in 736 common garden plants showed a latitudinal flowering time cline in both the native and invaded ranges where genotypes from lower latitudes flowered earlier. Genotyping‐by‐sequencing of 9,658SNPs in 446 individuals revealed two major subpopulations ofM. polymorphain the native range, only one of which is present in the invaded range. Additionally, native range populations have higher genetic diversity than invaded range populations, suggesting that a genetic bottleneck occurred during invasion. All invaded range individuals are closely related to plants collected from native range populations in Portugal and southern Spain, and population assignment tests assigned invaded range individuals to this same narrow source region. Taken together, our results suggest that latitudinal clinal variation in flowering time has rapidly evolved across the invaded range despite a genetic bottleneck following introduction.

     
    more » « less
  5. The role of phenotypic plasticity in adaptive evolution has been debated for decades. This is because the strength of natural selection is dependent on the direction and magnitude of phenotypic responses to environmental signals. Therefore, the connection between plasticity and adaptation will depend on the patterns of plasticity harbored by ancestral populations before a change in the environment. Yet few studies have directly assessed ancestral variation in plasticity and tracked phenotypic changes over time. Here we resurrected historic propagules ofDaphniaspanning multiple species and lakes in Wisconsin following the invasion and proliferation of a novel predator (spiny waterflea,Bythotrephes longimanus). This approach revealed extensive genetic variation in predator-induced plasticity in ancestral populations ofDaphnia. It is unlikely that the standing patterns of plasticity shieldedDaphniafrom selection to permit long-term coexistence with a novel predator. Instead, this variation in plasticity provided the raw materials forBythotrephes-mediated selection to drive rapid shifts inDaphniabehavior and life history. Surprisingly, there was little evidence for the evolution of trait plasticity as genetic variation in plasticity was maintained in the face of a novel predator. Such results provide insight into the link between plasticity and adaptation and highlight the importance of quantifying genetic variation in plasticity when evaluating the drivers of evolutionary change in the wild.

     
    more » « less