Plant evolutionary ecology: molecular genetics, global warming and invasions, and the novel approaches we are using to study adaptations
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1st Joint Congress on Evolutionary Biology, American Society of Naturalists (ASN), Canadian Society for Ecology and Evolution (CSEE), European Society for Evolutionary Biology (ESEB), Society for the Study of Evolution (SSE), and the Society of Systematic Biologists (SSB), University of Ottawa and Carleton University, in Ottawa, Ontario, Canada, July 2012
The 1st Joint Congress on Evolutionary Biology was an international meeting hosted jointly by the University of Ottawa and Carleton University (Ontario, Canada), that brought together nearly 2400 delegates from 45 countries representing the five major societies for evolutionary biology. As one might imagine, there was a very rich variety of research presented in all systems, asking a wide range of interesting questions in evolutionary ecology. Although there were abundant talks and posters (c. 1300 and 650, respectively), several exciting areas of plant research stood out, including studies on the molecular genetics of complex traits, ecological responses to climate change, evolution in invasive plants, and species interactions. Collectively, the sheer breadth of plant research at the meeting – which we cannot cover fully here – highlights the progress being made in plant evolutionary biology and ecology.
‘…the promise of merging interesting ecology with current genomic tools to explore the genetic basis and ecological function of traits that have major consequences on both fitness and life history, in nonmodel systems.’
Molecular genetics of complex traits
One of the prevalent subjects at the meeting was characterizing the genetic architecture of ecologically important traits in nonmodel systems; a challenge that continues to get easier with the increasing accessibility of genome-wide molecular markers (Stinchcombe & Hoekstra, 2008). For example, Thomas Parchman (University of Wyoming, Laramie, WY, USA) and colleagues were able to develop > 95 000 single-nucleotide polymorphism (SNPs) in lodgepole pine (Pinus contorta) to identify 11 candidate loci that explain 50% of the variation in pine cone serotiny (the maintenance of closed pine cones until a fire triggers their opening). Parchman et al. (2012) accomplished this without the prior development of genomic tools in P. contorta. Jannice Friedman (Syracuse University, Syracuse, NY, USA) combined ecological experimentation with next generation sequencing technology to explore the photoperiod and vernalization requirements across the Mimulus guttatus (monkey flower) complex. Through the use of growth chamber experiments, she discovered that most of the variation in these requirements could be explained by annual vs perennial life histories. She then employed bulk-segregant analysis and next-gen Illumina sequencing to identify quantitative trait loci (QTL) involved in this life history adjustment that contain several known flowering time loci. These are only two of the many talks that exemplified the promise of merging interesting ecology with current genomic tools to explore the genetic basis and ecological function of traits that have major consequences on both fitness and life history, in nonmodel systems.
Phenotypic response to climate change
Identifying the major environmental variable(s) that underlie climate-driven phenotypic change is crucial for predicting the future response of plant populations to global warming, which was emphasized by Susana Wadgymar (University of Toronto, Toronto, Ontario, Canada), who explored the influence of climate warming on plant reproductive phenology. She simulated warming by using heating arrays deployed in the field. Wadgymar observed a general acceleration and compression of the reproductive cycle in warmed plots, and then tested whether plants exhibited true thermal responses, or if they simply advanced their phenology temporally to occupy the same thermal niche (temporal plasticity). To explore this, she compared the accumulated growing degree days (GDDs: an estimate of the total amount of thermal energy available for growth) between heated and unheated plots, and discovered that these traits truly exhibited thermal plasticity because they generally had higher GDDs at the onset of each life history trait in heated plots. While Wadgymar's work explores phenotypic plasticity in the face of climate change, which is typical for many global warming studies (Gienapp et al., 2008; Hendry et al., 2008), what are we learning about the evolutionary responses of plants to global warming? Many authors, including Jill Anderson (University of South Carolina, Columbia, SC, USA) are beginning to address plant adaptation to climate change. Anderson summarized results from a 38-yr field survey, demonstrating that flowering phenology had significantly accelerated from 1973 to 2011 in Boechera stricta, which agreed with contemporary studies indicating strong directional selection for earlier flowering. Anderson and her colleagues estimated that current levels of selection can account for up to 20% of the phenological shift (Anderson et al., 2012), suggesting, at least in part, an adaptive flowering time change.
Trait variation and geography
While next-generation studies and climate change/conservation continue to be at the forefront of plant research, the meeting also hosted a wealth of research employing traditional approaches to address interesting questions about plant adaptation. One such strategy that was common throughout the meeting was to study geographically varying traits to understand how spatially varying selection shapes trait distributions. For example, Nicholas Kooyers (Washington University in St Louis, MO, USA) examined three separate, but parallel cyanogenesis clines in the white clover, Trifolium repens, to determine if the target of selection is the presence/absence of cyanogenesis, or if selection is acting independently on the alleles responsible for its two underlying biochemical components (glucosides and linamarase). He found that all three clines exhibit adaptive variation in cyanogenesis, with cyanogenic plants dominating warmer climates. However, the patterns at the underlying genes are different between each transect suggesting that different selective forces are acting to create similar clinal patterns in different parts of the world. Chris Muir (Indiana University, Bloomington, IN, USA) took a slightly different approach by employing interspecific rather than intraspecific geographical variation. He examined trait patterns between 16 wild relatives of the cultivated tomato, to understand how leaf mass per area (LMA; proxy for leaf toughness) and drought tolerance may influence the geographical distributions of various tomato species. Muir found, contrary to common observations, that species originating from drier habitats had a lower LMA. Currently, Muir and his colleagues have evidence that lower LMA may increase both water use efficiency and photosynthesis, suggesting that tomato plants with low LMA may avoid drought while growing rapidly.
Muir's talk also underscores another important aspect of current plant research. Ackerly et al. (2000), more than a decade ago, stressed the importance of studying plant physiological ecology in an evolutionary context to understand how natural selection affects ecophysiological traits (i.e. traits that influence nutrient uptake and utilization, and are likely to have major fitness consequences). Since their review, there has arguably not been enough progress to this end, with the exception of a few good examples (Nakazato et al., 2008; Agrawal et al., 2009). The 1st Joint Congress, however, demonstrated that plant evolutionary biologists, as exemplified by Kooyers, Muir, and others at the joint congress, are increasingly recognizing the importance of evolutionary ecophysiology.
Evolutionary consequences of plant invasion
Understanding how and why exotic plants become invasive beyond their native range has been a major goal in the invasive biology research program. A fundamental hypothesis that can explain the success of an invasive plant species beyond its native ranges is through release or escape from native competitors and enemies (Elton, 1958). Having received much attention for decades, two studies at the meeting provided key insights into this hypothesis. Richard Lankau (University of Georgia, Athens, GA, USA) presented a study on the coevolution between invasive and allelopathic garlic mustard (Alliaria petiolata) and its native North American competitors. He found that the garlic mustard derived from areas with high interspecific competition expressed more toxic allelochemical than individuals from areas of low competition. Likewise, native competitors from areas of high invasion express relatively more tolerance suggesting a coevolutionary dynamic. Furthermore, he demonstrated that more tolerant native competitors were less fit in common gardens where invasives were rare, suggesting that tolerance comes at a cost (Lankau, 2012). Lankau's work demonstrates that evaluating ecologically relevant traits of native competitors provide key information necessary to understand how invasive plants become established in exotic ranges.
Carolyn Beans (University of Virginia, Charlottesville, VA, USA) examined in greater detail how interspecific competition from an invasive plant, via competition for pollinators or pollen, can affect the evolution of floral traits in a North American native, Impatiens capensis. Impatiens capensis produces showy outcrossing flowers and small selfing flowers within individual plants and is often found competing with an invasive congener, I. glandulifera, which produces large showy flowers. In a quantitative genetic field experiment, she demonstrated that the presence of the congener changed selection patterns on several floral morphology traits including, spur length, corolla length and color spotting. Consistent with experimental results, she also found that natural populations of I. capensis competing with I. glandulifera had longer spurs. Natural populations also tended to produce fewer outcrossing flowers, but she added that follow up studies will confirm whether the change in the allocation to selfing and outcrossing flowers is genetic rather than plastic. Beans' study suggests that interspecific competition with a plant invader, via pollen or pollinator competition, could potentially have a large impact on the costs and benefits of floral display traits, and alter selection patterns on those traits on native flora.
Exotic plants may also become invasive because release from their natural enemies enables increased allocation to competitive ability rather than defense, otherwise known as the evolution of increased competitive ability (EICA) hypothesis (Blossey & Notzold, 1995). Blossey & Notzold (1995) found evidence that an invasive Lythrum salicari (purple loosestrife) had evolved increased competitive ability in North America due to release from their natural enemies. Given the assumed trade-off between defense and plant competition, what remains untested is how defense traits are impacted once an invasive evolves increased competitive ability in its exotic range and natural enemies are introduced into the system. Taking advantage of the known introduction history of Lythrum and its biological control agents, Galerucella calmariensis and G. pusilla (leaf chewing beetles that specialize on Lythrum in their native range), Gina Quiram (University of Minnesota, Minneapolis, MN, USA) demonstrated that introduced populations exposed to higher levels of herbviory have evolved increased tolerance to beetle damage compared to other Lytrhum populations within North America. However, the populations with higher herbivore tolerance did not show decreased competitive ability with native competitors, as predicted by the EICA hypothesis. In fact, tolerant populations exposed to the control agent generally became more vigorous against native competitors. Quiram's study raises many concerns on how effective biological control agents are in regulating population growth of invasive plants in the long term.
More generally, all three of these studies highlight the important role of altered species interactions, especially plant competition, in understanding how invasive plants become successful in exotic ranges.
We have highlighted here only a handful of studies, as there were many other excellent presentations and posters. We believe that the next step in plant ecology and evolution should be to connect some of these exciting fields of research through integrated studies. Investigating the molecular genetics of geographically varying traits will provide key insights into how evolutionary processes are behaving both spatially and temporally to produce trait differentiation. Exploring how climate change will affect species interactions or the propensity for invasive species to spread will be critical areas of research in a changing world. By integrating our knowledge on gene and gene regulation function, population genetics and agents of selection in an ecologically relevant context, plants will continue to provide ideal study systems to understand the fundamental mechanics of adaptation in a changing world.
The authors thank all of the presenters mentioned, as well as those they could not include who were kind enough to share information with them after the meeting. The work was supported by both NSERC graduate scholarships (A.K.S. and B.E.C.) and a Discovery Grant to John Stinchcombe.