Steven J. Franks

Rapid evolution of flowering time by an annual plant in response to a climate fluctuation

Ongoing climate change has affected the ecological dynamics of many species and is expected to impose natural selection on ecologically important traits. Droughts and other anticipated changes in precipitation may be particularly potent selective factors, especially in arid regions. Here we demonstrate the evolutionary response of an annual plant, Brassica rapa, to a recent climate fluctuation resulting in a multiyear drought. Ancestral (predrought) genotypes were recovered from stored seed and raised under a set of common environments with descendant (postdrought) genotypes and with ancestor×descendant hybrids. As predicted, the abbreviated growing seasons caused by drought led to the evolution of earlier onset of flowering. Descendants bloomed earlier than ancestors, advancing first flowering by 1.9 days in one study population and 8.6 days in another. The intermediate flowering time of ancestor×descendant hybrids supports an additive genetic basis for divergence. Experiments confirmed that summer drought selected for early flowering, that flowering time was heritable, and that selection intensities in the field were more than sufficient to account for the observed evolutionary change. Natural selection for drought escape thus appears to have caused adaptive evolution in just a few generations. A systematic effort to collect and store propagules from suitable species would provide biologists with materials to detect and elucidate the genetic basis of further evolutionary shifts driven by climate change.

Evolutionary and plastic responses to climate change in terrestrial plant populations

As climate change progresses, we are observing widespread changes in phenotypes in many plant populations. Whether these phenotypic changes are directly caused by climate change, and whether they result from phenotypic plasticity or evolution, are active areas of investigation. Here, we review terrestrial plant studies addressing these questions. Plastic and evolutionary responses to climate change are clearly occurring. Of the 38 studies that met our criteria for inclusion, all found plastic or evolutionary responses, with 26 studies showing both. These responses, however, may be insufficient to keep pace with climate change, as indicated by eight of 12 studies that examined this directly. There is also mixed evidence for whether evolutionary responses are adaptive, and whether they are directly caused by contemporary climatic changes. We discuss factors that will likely influence the extent of plastic and evolutionary responses, including patterns of environmental changes, species’ life history characteristics including generation time and breeding system, and degree and direction of gene flow. Future studies with standardized methodologies, especially those that use direct approaches assessing responses to climate change over time, and sharing of data through public databases, will facilitate better predictions of the capacity for plant populations to respond to rapid climate change.

Genetics of Climate Change Adaptation

The rapid rate of current global climate change is having strong effects on many species and, at least in some cases, is driving evolution, particularly when changes in conditions alter patterns of selection. Climate change thus provides an opportunity for the study of the genetic basis of adaptation. Such studies include a variety of observational and experimental approaches, such as sampling across clines, artificial evolution experiments, and resurrection studies. These approaches can be combined with a number of techniques in genetics and genomics, including association and mapping analyses, genome scans, and transcription profiling. Recent research has revealed a number of candidate genes potentially involved in climate change adaptation and has also illustrated that genetic regulatory networks and epigenetic effects may be particularly relevant for evolution driven by climate change. Although genetic and genomic data are rapidly accumulating, we still have much to learn about the genetic architecture of climate change adaptation.

Plasticity and evolution in drought avoidance and escape in the annual plant Brassica rapa.

A key question in ecological genetics is to what extent do plants adapt to changes in climatic conditions, such as drought, through plasticity or evolution. To address this question, seeds of 140 maternal families of Brassica rapa were generated from collections made before (1997) and after (2004) a natural drought. These seeds were planted in the glasshouse and grown under low-water and high-water conditions. Post-drought lines flowered earlier than pre-drought lines, showing an evolutionary shift to earlier flowering. There was significant genetic variation and genotype by environment (G × E) interactions in flowering time, indicating genetic variation in plasticity in this trait. Plants that flowered earlier had fewer leaf nodes and lower instantaneous (A/g) and integrated (δ(13)C) water use efficiency than late-flowering plants. These results suggest that B. rapa plants escape drought through early flowering rather than avoid drought through increased water use efficiency. The mechanism of this response appears to be high transpiration and inefficient water use, leading to rapid development. These findings demonstrate a trade-off between drought avoidance and escape, and indicate that, in this system, where drought acts to shorten the growing season, selection for drought escape through earlier flowering is more important than phenotypic plasticity.

A change in climate causes rapid evolution of multiple life-history traits and their interactions in an annual plant.

Climate change is likely to spur rapid evolution, potentially altering integrated suites of life‐history traits. We examined evolutionary change in multiple life‐history traits of the annual plant Brassica rapa collected before and after a recent 5‐year drought in southern California. We used a direct approach to examining evolutionary change by comparing ancestors and descendants. Collections were made from two populations varying in average soil moisture levels, and lines propagated from the collected seeds were grown in a greenhouse and experimentally subjected to conditions simulating either drought (short growing season) or high precipitation (long growing season) years. Comparing ancestors and descendants, we found that the drought caused many changes in life‐history traits, including a shift to earlier flowering, longer duration of flowering, reduced peak flowering and greater skew of the flowering schedule. Descendants had thinner stems and fewer leaf nodes at the time of flowering than ancestors, indicating that the drought selected for plants that flowered at a smaller size and earlier ontogenetic stage rather than selecting for plants to develop more rapidly. Thus, there was not evidence for absolute developmental constraints to flowering time evolution. Common principal component analyses showed substantial differences in the matrix of trait covariances both between short and long growing season treatments and between populations. Although the covariances matrices were generally similar between ancestors and descendants, there was evidence for complex evolutionary changes in the relationships among the traits, and these changes depended on the population and treatment. These results show that a full appreciation of the impacts of global change on phenotypic evolution will entail an understanding of how changes in climatic conditions affect trait values and the structure of relationships among traits.

Facilitation in multiple life-history stages: evidence for nucleated succession in coastal dunes

Understanding plant interactions during succession is a central goal of plant ecology. The nucleation model of succession proposes that facilitative interactions lead to outward radiations of colonization from established plants. I tested the nucleation hypothesis for early successional plants on the primary dunes of barrier islands in the southeastern United States. On the coast of Florida and Georgia, I sampled the above-ground vegetation and the seed bank, and conducted a seedling emergence experiment in the field. Vegetation sampling at both field sites showed more positive correlations in percent cover of adult species than expected by chance. At both sites, there were significantly more seeds under plants than in open microsites. Seeds of the same species as the adult plants in the vegetated microsites were removed from the analysis, so the accumulation of seeds under adults is not due simply to a seed shadow effect. Seeds of six species were added to plots under plants and in open microsites, and seedling emergence was significantly higher under plants than in the open. The findings support the predictions of the nucleation hypothesis for the early life-history stages of seed dispersal and germination, and help to explain the clumped distribution of dune plants seen in the field. The results add further support for the contention that facilitation is an important mode of plant interaction in stressful and disturbed habitats.

Burial disturbance leads to facilitation among coastal dune plants

There is growing evidence that interactions among plants can be facilitative as well as competitive, but knowledge of how disturbances influence these interactions and how they vary with species diversity is lacking. We manipulated plant density, species diversity (richness), and a burial disturbance in a controlled, complete factorial experiment to test theories about the relationships among species interactions, disturbance, and richness. The hypotheses tested were 1) burial disturbance reduces plant performance at all levels of density and richness, 2) burial disturbance can cause net plant interactions to become more facilitative, and 3) facilitation increases with species richness. Burial decreased plant survival by 60% and biomass by 50%, supporting the hypothesis that burial reduces plant performance. In the control (unburied) treatment, there was no difference in proportion survival or per plant biomass between low and high density plots, meaning that neither competition nor facilitation was detected. In the buried treatment, however, high density plots had significantly greater survival and greater per plant biomass than the low density plots, indicating net facilitative interactions. Thus facilitation occurred in the buried treatment and not in the unburied control plots, supporting the hypothesis that facilitation increases with increasing disturbance severity. The hypothesis that facilitation increases with increasing species richness was not supported. Richness did not affect survival or biomass, and there was no richness by burial treatment interaction, indicating that richness did not influence the response of the community to burial. The influence of the disturbance on plant interactions was thus consistent across levels of richness, increasing the generality of the relationship between disturbance and facilitation.

The Resurrection Initiative: Storing Ancestral Genotypes to Capture Evolution in Action

ABSTRACT In rare circumstances, scientists have been able to revive dormant propagules from ancestral populations and rear them with their descendants to make inferences about evolutionary responses to environmental change. Although this is a powerful approach to directly assess microevolution, it has previously depended entirely upon fortuitous conditions to preserve ancestral material. We propose a coordinated effort to collect, preserve, and archive genetic materials today for future studies of evolutionary change—a “resurrection paradigm.” The availability of ancestral material that is systematically collected and intentionally stored using best practices will greatly expand our ability to illuminate microevolutionary patterns and processes and to predict ongoing responses of species to global change. In the workshop “Project Baseline,” evolutionary biologists and seed storage experts met to discuss establishing a coordinated effort to implement the resurrection paradigm.

Herbivory by Introduced Insects Reduces Growth and Survival of Melaleuca quinquenervia Seedlings

Abstract We studied the influence of herbivory by two introduced insect herbivores on the survival and performance of seedlings of Melaleuca quinquenervia (Cav.) Blake (Myrtaceae), an invasive tree that threatens the Florida Everglades ecosystem. Boreioglycaspis melaleucae (Moore) (Homoptera: Psyllidae) nymphs and Oxyops vitiosa (Pascoe) (Coleoptera: Curculionidae) larvae were transferred onto Melaleuca seedlings within replicated 0.25-m2 caged plots in Palm Beach County, FL. The treatments included three densities of Boreioglycaspis first instars at 1, 15, and 50 nymphs per seedling, one treatment of a single first Oxyops larval instar per seedling, another treatment of both one Oxyops larva and one Boreioglycaspis nymph per seedling, and caged and uncaged controls. Herbivory by Oxyops did not affect Melaleuca seedling height, leaf number, or survival. Feeding by Boreioglycaspis decreased survival, height, and leaf number, with these measures of plant performance ≈50% lower in the high and medium densities compared with controls. In a field plot adjacent to the experimental area, we measured growth, survival, and naturally occurring insect density and damage on 1,100 seedlings. Although insect densities were on average lower in the field plot than in the experiment, mortality and growth rates of the seedlings were comparable with those in the experiment. The results indicate that, above a threshold density, Boreioglycaspis herbivory may be effective in reducing growth and survival of Melaleuca at the potentially critical seedling life stage. It also seemed that effects of the insects were independent rather than antagonistic or synergistic.

No evolution of increased competitive ability or decreased allocation to defense in Melaleuca quinquenervia since release from natural enemies

If invasive plants are released from natural enemies in their introduced range, they may evolve decreased allocation to defense and increased growth, as predicted by the evolution of increased competitive ability (EICA) hypothesis. A field experiment using the invasive tree Melaleuca quinquenervia was conducted to test this hypothesis. Seeds were collected from 120 maternal trees: 60 in Florida (introduced range) and 60 in Australia (home range). Plants grown from these seeds were either subjected to herbivory by two insects from Australia that have recently been released as biological control agents or protected from herbivores using insecticides. Genotypes from the introduced range were initially more attractive to herbivores than genotypes from the home range, supporting EICA. However, genotypes from the introduced and home range did not differ in resistance to insects or in competitive ability, which does not support EICA. Plants from the introduced range had a lower leaf hair density, lower leaf: stem mass ratio, and a higher ratio of nerolidol: viridifloral chemotypes compared to plants from the native range. Plants with an intermediate density of leaf hairs and with high specific leaf area were more susceptible to herbivory damage, but there were no effects of leaf toughness or chemotype on presence of and damage by insects. Herbivory had a negative impact on performance of Melaleuca. Other than an initial preference by insects for introduced genotypes, there was no evidence for the evolution of decreased defense or increased competitive ability, as predicted by the EICA hypothesis. It does not appear from this study that the EICA hypothesis explains patterns of recent trait evolution in Melaleuca.