Recipient of the 2014 molecular ecology prize: Johanna Schmitt.

Abstract

Johanna Schmitt It is a great pleasure to help honour the 2014 recipient of the Molecular Ecology Prize: Johanna Schmitt, Professor of Evolution and Ecology and of Population Biology at the University of California, Davis. Johanna, or Annie as she is known by friends and colleagues, has had tremendous influence on the field of ecological genetics throughout her career, and her recent work on the genetic basis of adaptation in Arabidopsis thaliana is some of the most ambitious applications of genomic methods to test hypotheses of ecological and evolutionary dynamics. Entering the field of evolutionary genetics and genomics from the field of ecology, she has infused genetic studies of adaptation with a rich and nuanced view of the ecological environment as seen from the perspective of her study organisms. Anyone who has walked in the woods with her will recognize her plants' eye view in her research. As her former postdoc John Stinchcombe observed, ‘one of the things I find remarkable about Annie (among many) is that as the field has transitioned from a few genes or anonymous markers to whole genome level variation, she's never lost her “feel for the organism” or sight of the larger ecological or evolutionary questions that motivated her to go down this path’. Annie majored in Biology at Swarthmore College and continued her PhD in Biology at Stanford University, with Ward Watt as her advisor. There, she wrote her dissertation on the pollination biology of Scenecio and Linanthus, cultivating interests in the population genetic consequences of density-dependent pollination dynamics (e.g. Schmitt 1983a,b). It was during her postdoctoral work at Duke University, with Janis Antonovics (whom she admired as a great female role model, until she met him in person), that she developed her signature methodology of applying genetic designs to clever and complex field experiments. This approach had two important consequences for her own research and for the field of ecological genetics: first, it illustrated how ecological manipulations can be combined with genetic analysis to test evolutionary hypotheses. For example, her work at Duke tested how genetic diversity within local neighbourhoods can influence competitive interactions and adverse effects of herbivores, relating these dynamics to the evolution of sexual reproduction (Schmitt & Antonovics 1986b; Schmitt & Ehrhardt 1987; Kelley et al. 1988). The focus on sexual reproduction also motivated her to distinguish maternal vs. paternal effects on progeny phenotypes, bringing into focus the phenomenon of maternal effects or cross-generational phenotypic plasticity (Antonovics & Schmitt 1986; Schmitt & Antonovics 1986a). Second, this approach illustrated the strong environmental context of the expression of genetically based traits. Her subsequent work, which she continued at her first faculty appointment at Brown University, engaged the evolutionary and ecological consequences of this environment-dependent genetic expression or genotype–environment interaction. She made phenotypic plasticity a central focus of her research programme (Schmitt et al. 1992; Schmitt 1993, 1995). It was this work that pioneered methods for testing the adaptive significance of phenotypic plasticity, both within and across generations (Schmitt 1993, 1997; Wulff et al. 1994, Schmitt et al. 1999). Her combination of environmental manipulations, phenotypic and genetic manipulations, and measurements of environment-dependent natural selection became the gold standard of tests for adaptive plasticity. Her work on shade avoidance responses in Impatiens capensis unambiguously demonstrated adaptive plasticity and documented that not only did phenotypes change in response to environmental conditions, but genetic variances and covariances did as well (Dudley & Schmitt 1996; Schmitt & Dudley 1996; Donohue et al. 2000a,b). That is, the genetic basis of traits under selection, and the genetic relationships among them, depended strongly on the ecological environment they experienced. Annie's work on shade avoidance responses engaged not only the quantitative genetic basis of this complex trait, but the molecular genetic pathways associated with it as well. Shade avoidance—the ability of plants to elongate in response to vegetation shade—was long known to be mediated by the plant photoreceptors, phytochromes (Schmitt & Wulff 1993). During a sabbatical at the University of Leicester, she collaborated with Alex McCormac and Harry Smith to test how the genetic disruption of phytochrome function would alter shade avoidance and fitness. Using transgenic lines of tobacco whose shade avoidance ability had been blocked, and constitutively shade-avoiding mutants of Brassica, they demonstrated a significant fitness disadvantage of inappropriate shade avoidance responses (Schmitt et al. 1995). This was her first work that employed tools of molecular genetics to test ecological hypotheses. While continuing to investigate the quantitative genetic basis of diverse plastic responses to vegetation shade, Annie began to explore other genetic methods to evaluate their genetic architecture. Like other evolutionary geneticists at the time, she discovered the utility of employing natural genetic variation in ecologically important traits to investigate their genetic basis through quantitative trait locus (QTL) mapping. At the time when QTL analysis was just beginning to be broadly applied to identify loci associated with ecologically significant phenotypes, Annie and her associates implemented a highly ambitious QTL study using Arabidopsis thaliana under field conditions to map not only well-defined phenological and morphological phenotypes, but fitness itself. This intense collaborative effort, initially supported by an NSF FIBR grant, was among the very first to map loci associated with fitness under natural conditions in contrasting geographical sites (Weinig et al. 2002, 2003a,b,c). By demonstrating that some genetic loci were associated with fitness only in one location but neutral in another, while other genetic loci were associated with fitness in both locations, but in opposite directions, this study illustrated how QTL analysis could be employed to resolve long-standing issues of trade-offs in adaptation across geographical locations—specifically revealing instances of conditional neutrality and evidence of antagonistic pleiotropy. The success of this research programme spawned a monster, according to the numerous participants of the next major research effort. Encouraged by the success of the two-site field study with numerous recombinant inbred lines, the team, with some new recruits, initiated a study using four sites across the native range of A. thaliana, from Oulu, Finland to Valencia, Spain, in which hundreds of natural ecotypes combined with a strategic array of mutants, were planted for continuous monitoring. Simultaneously with this ambitious field experiment, creative modelling efforts were being developed to predict the flowering time of specific genotypes under diverse climatic scenarios using agronomic models. This synthesis of genetics, ecology, agronomy and mathematical modelling was unique, and it provided unique insight into the genetic basis of adaptation. Their synthetic approach revealed, for example, that even well-known flowering time genes are expected to exhibit (and did exhibit) effects on flowering time only under certain ecological circumstances and life history backgrounds (Wilczek et al. 2009; Chew et al. 2012). The feat of bringing evolutionary ecologists (Cynthia Weinig, Tonia Korves, Amity Wilczek) in dialogue with population geneticists (Michael Purugganan), molecular geneticists (George Coupland, Rick Amasino, Caroline Dean) and modellers (Steve Welch), while engaging international collaborators (Outi Savolainen, Matthias Hoffmann) in fieldwork, was a Herculean accomplishment. A series of articles from this work was published in Science, PNAS, Molecular Ecology and a number of other prominent journals. Among the most notable findings of this programme were that A. thaliana shows evidence of climate adaptation, with geographic clines in adaptively significant life history traits as well as the loci associated with those traits (Caicedo et al. 2004; Stinchcombe et al. 2004, 2005; Korves et al. 2007; Wilczek et al. 2010). Moreover, genome-wide association studies revealed associations of loci with climate factors across the genome (Fournier-Level et al. 2011, 2013). Most recently (Wilczek et al. 2014), the team found evidence that climate change has caused banked seeds to no longer be optimally adapted to their locations of collection, but that that ecotypes from historically warmer locations performed better under current (warmer) conditions than banked seeds in their native location. As such, immigration of more warm-adapted genotypes into areas with climate change, not emergence from the seed bank or introduction of local banked seeds, is expected to be more effective at maintaining populations in the face of climate change. These empirical data, combined with predictive modelling, establishes a new standard for predictions of how organisms can respond to climate change. Annie was involved at the beginning stages of developing model genetic organisms into model ecological organisms. She helped shape the sorts of questions that could be addressed with this sort of collaboration and made ecological genetics a collaborative endeavour between ecologists, population geneticists and molecular geneticists. Always promoting collaboration over competition, she brokered many matches between PIs studying related phenomena and proposed opportunities to combine efforts in synergistic directions. The field has her to thank for the open and collaborative spirit she has infused it with. In addition to shaping the collaborative nature of the field of ecological genetics, Annie has been a valuable mentor to people at all stages. At Brown, she worked closely with her undergraduate students to involve them with every step of their research projects, from helping to design experiments to data collection, and analysis and presentation. Many of us are grateful for this effort, which has produced so many excellent students who have joined our laboratories as graduate students or technicians. It was here, too, that so many of her postdocs learned the craft of designing undergraduate projects that were self-contained, challenging and rewarding, providing a model for tapping the unique resources of undergraduates in research. Her numerous postdocs also benefitted from being members of such a cohesive laboratory, in which laboratory members could count on each other for technical help and conceptual exchange. Annie's generosity of time, creativity and opportunity were critical to the professional development of many of us. Personally, I will never take for granted the extreme generosity she extended to me when, after a very ill-timed postdoc in Yemen during what turned into its civil war, I found myself evacuated back stateside with no backup plan. I basically knocked on her door to ask for a short-term landing pad, and she opened it up in a manner I could never have expected. At that critical, awkward and very tricky time in my career, she welcomed me into her laboratory, involved me in the ongoing research and gave me new skills, intellectual companionship and a model for how to run a laboratory that was collegial, engaging and effective. I am certain that anyone who spent time in her laboratory benefitted in the same way, and several of her former postdocs (including Susan Dudley, Massimo Pigliucci, Cynthia Weinig, John Stinchcombe, Amity Wilczek and others) have expressed the same appreciation over the years. Annie has amassed several honours as a result of her creative contributions, including election to the National Academy of Sciences, the American Academy of Arts and Sciences, the American Association for the Advancement of Sciences and an Alexander von Humboldt Award, among others. She has been the President of the major professional societies in her field: the Society for the Study of Evolution and the American Society of Naturalists. While at Brown University, she was Stephen T. Olney Professor of Natural History, and she was also the director of the Environmental Change Initiative there, where she exercised her remarkable ability to communicate and synthesize across scientific subfields. UC Davis is now the beneficiary of Annie's energy and expertise, after she moved there in 2012. This Molecular Ecology Prize serves to honour her past accomplishments and inspire curiosity for what is to come.