Whither plant evo‐devo?

Plant evolutionary developmental biology has come a long way in the years since its transformation at the beginning of the molecular era. Gone are the naïve hopes that developmental genetics would provide unambiguous solutions to questions of homology and evolutionary novelty that had stymied plant biologists for centuries. Also gone is the simplistic notion that understanding the molecular genetics of Arabidopsis thaliana might reveal universal properties of plant (or even just angiosperm) development (Jaramillo & Kramer, 2007). On the other hand, life's complexity is surely what makes all of us enjoy being biologists. So perhaps, while plant evo-devo has not answered all (or even many) of the questions it initially set out to address, it is timely to ask where this young field is going, or perhaps more importantly, where this young field could and should go. Such was the vision of a recent meeting of plant evolutionary biologists with strong interests in integrating plant developmental biology into the broader spectrum of botanical disciplines. ‘... we risk the sophistication and power of genetic tools outstripping our ability to interpret the data and “know” the phenotype.’ Investigating the evolution of plant form: conceptual integration from the molecular to the ecological, was an intensive, three-day minicourse organized by the Molecular and Organismic Research in Plant History (MORPH) Research Coordination Network (part of the US National Science Foundation Research Coordination Network Program) that took place in mid-December at the University of Colorado in Boulder. The overarching goal of MORPH has been to promote interdisciplinary research on the evolution of plant form through the integration of concepts and approaches from across the hierarchy of biological organization. This has primarily been accomplished over the last five years through the sponsorship of more than 40 interdisciplinary research training experiences for undergraduates, graduate students, postdoctoral individuals and junior faculty; through assistance to 95 students to attend interdisciplinary plant evo-devo symposia at national and international meetings; and development of a website for the highly diverse and international community of plant evolutionary developmental biologists (http://www.colorado.edu/eeb/MORPH/). The MORPH minicourse represented a new tack in attempting to bridge interdisciplinary chasms and engage the next generation of plant evolutionists and developmentalists. This minicourse provided the opportunity for a select group of 14 doctoral students, from across the USA and Mexico, to interact with 11 seasoned researchers (Scott Armbruster, University of Portsmouth, UK; Spencer Barrett, University of Toronto, Canada; Peter Crane, University of Chicago, USA; Pamela Diggle, University of Colorado, USA; Michael Donoghue, Yale University, USA; Peter Endress, University of Zurich, Switzerland; William Friedman, University of Colorado, USA; Larry Hufford, Washington State University, USA; Vivian Irish, Yale University, USA; Amy Litt, New York Botanical Garden, USA; and Michael Purugganan, New York University, USA), whose work spans the spectrum from evolutionary ecology to developmental genetics (for a listing of talks, go to http://www.colorado.edu/eeb/MORPH/grants/minicourses/minicourse2007.html). Both researchers and students gave research presentations that were followed by extensive discussions of best approaches, potential pitfalls and interdisciplinary insights on the evolution of plant form. By bringing together students and faculty from diverse backgrounds, this meeting served to increase the dialogue between botanical subdisciplines that, while fundamentally interested in plant structure and diversity, rarely attend the same meetings or sit at the same table. In a single room, paleobotanists working on reproductive structures in Cretaceous angiosperms and outgroups to flowering plants (e.g. Friis et al., 2006) sat side-by-side with molecular geneticists examining the roles of gene duplication and subfunctionalization in floral evolution (e.g. Irish & Litt, 2005) and ecologists whose goals of explaining floral diversity require fitness assays in wild populations (Barrett, 2008). The two organizers, Larry Hufford (Washington State University, USA) and William Friedman (University of Colorado, USA), hoped that by the end of the meeting, the participants would be able to identify both common ground and difficult areas where future interdisciplinary collaboration is required to develop new paradigms. The comfort zone necessary for cross-disciplinary synthesis can be remarkably narrow in any new area. While most biologists recognize the great potential of plant evolutionary developmental biology in this molecular era, it has yet to deliver an understanding of the morphological diversity characteristic of the vast majority of clades in nature. Moreover, plant evo-devo has not as yet forged a meaningful union with ecology and microevolution. Success in plant evolutionary developmental genetics to date has largely involved the use of a limited number of model organisms. Even these few models, however, provide tantalizing glimpses of the possibilities that may be achieved through the power of comparative approaches to developmental and evolutionary biology. The rapid rate of whole-genome sequencing, currently underway along with the development of new technologies, suggests that plant biologists will soon have many more systems to compare to infer the general rules of plant development (Bowman et al., 2007). However, with the emerging promise of large-scale genomic initiatives, a key challenge will be to link comparative developmental genetics to existing bodies of knowledge, notably the more than 200 yr of plant morphological tradition that date to the work of Goethe (Versuch die Metamorphose der Pflanzen zu erklären, 1790) and the hypothesis-driven approaches used in evolutionary ecological studies of adaptation and population divergence (e.g. Barrett, 2008 and articles contained therein). This integration will be absolutely critical as the phylogenetic, structural and ecological breadth of plant taxa open to study expands, and the sophistication of the questions asked increases in complexity. Discussions at the MORPH minicourse did indeed focus on the growing recognition that plant evo-devo requires a broad set of study systems and genetic tools that can be readily applied to diverse groups to study the molecular genetic basis of morphological novelty and ecological function. In turn, these new study systems and genetic tools will allow us to examine at what levels regulatory or structural genes, networks and modules change and/or are co-opted for new and different developmental outcomes in different taxa. We need to understand whether there are different ways in which gene networks are recruited for different types of traits (Irish & Benfey, 2004). Are there certain types of traits that arise by frequent recruitment of different genetic pathways, pointing to lability in the ways such traits evolve? Or does most variability arise from redeployment of a basic set of pathways, presumably through evolutionary tweaking of levels and timing of gene expression? And, further, is the ‘primacy of regulatory evolution’ really primary? The MORPH minicourse demonstrated that the ‘candidate gene approach’ remains a common starting point for many of the projects that are attempting to move beyond model systems. Explicit or implicit in this approach are the assumptions that (1) gene function is highly conserved and (2) there is a ‘toolkit’ of developmental genes (or networks) that have been co-opted repeatedly to perform the same function at a new time or location, or in a new context. Tests of these assumptions (and perhaps tests of the primacy of regulatory evolution) will depend, in part, on the correct assessment of gene function (Ehrenreich et al., 2007) and what ‘sameness’ is in the context of diverse organisms. Each use of the candidate gene approach depends critically on a careful consideration of how the function of the candidate gene was assessed, how its function is manifest in different model systems and how it might be expressed in the system of interest. These steps, regardless of the genetic tools available, require explicit comparative morphological (and anatomical) analyses as both the starting and ending points (Friedman et al., 2004; Endress, 2006). Conclusions about organism-level developmental evolution depend critically on the correct evaluation of phenotypes and the organism-specific developmental phenomena that underlie those phenotypes. A description (perhaps better yet, hypothesis) of gene function is only as good as the underlying assessment of its associated developmental phenotype. There is a danger in the field of plant evo-devo of overlooking the vast legacies of comparative morphology, systematics and paleobiology. These provide vital analytical tools that are critical for understanding the evolutionary changes that yield morphological and functional diversity. The MORPH Research Coordination Network has attempted to overcome this problem with interdisciplinary training opportunities for students to move between molecular and organismic labs. However, if we are to achieve the goals of plant evo-devo, training in organismic biology must be sustained in academic institutions – a trend that clearly is not occurring. Relatively few major universities now count trained plant morphologists and anatomists or paleobotanists among their faculty. As it stands now, we risk the sophistication and power of genetic tools outstripping our ability to interpret the data and ‘know’ the phenotype. Ultimately, the recurring themes of many of the presentations of how to analyze homology, homoplasy and structural innovation will require just as much of a look backward to the historical and conceptual depths of morphology as a look forward to the leading edges of technology and genomics. Developmental geneticists rely on the constancy of certain phenotypes in their analyses; however, it is clear that adaptive plasticity and phenotypic variance are essential prerequisites for evolutionary tinkering (Diggle, 2002; Armbruster et al., 2004; Mitchell-Olds & Schmidt, 2006). Indeed, many questions were raised as to how plant evo-devo can best incorporate the complexities of the extensive natural variation found in highly metameric continuously developing organisms. To what extent can we capture this type of intra-organism and inter-organism variation through comparative developmental genetic studies? How are such changes translated into phenotypic differences? In fact, what kinds of diversity at the organismic, tissue, cell and genetic levels are there? What kind of diversity is represented in the fossil record? And how does this diversity inform our understanding of extant modes of development resulting in particular morphologies? Does the iterative and indeterminate growth of plants impact the types of developmental processes that can be recruited for such changes? The use of morphological polymorphisms in which individuals possess alternative states of a trait, but have common genetic backgrounds, might provide powerful experimental systems to relate intraspecific developmental variation to ecological or functional adaptation (Kalisz et al., 2006). Unfortunately, despite their simple Mendelian inheritance, evo-devo studies of polymorphisms have rarely been undertaken. Discussion focused on the future use of polymorphic systems to link developmental genetic differences to trait function in natural environments. The holy grail of ecological evolutionary developmental biology ultimately will be to integrate these contrasting approaches by linking genes through morphology to adaptation and fitness in wild populations. Clearly, if plant evo-devo and plant ecology are to have a meaningful relationship, much work needs to be accomplished to integrate the vastly different perspectives of these disciplines. Functional analyses differ depending on which level of the genealogical hierarchy is investigated. The language and approach change as one moves from the species, to the population, through the individual organism, to the molecular level. Charles Darwin initiated a functional view of plant diversity by proposing adaptive hypotheses for diverse plant traits, particularly those associated with reproduction. Currently, a significant research program within evolutionary ecology focuses on testing functional hypotheses. Presentations at the meeting on the ecological function of traits used manipulative field studies and measures of fitness to illustrate one approach to examining biological function in the Darwinian tradition. One of the challenges for an integrative field of biology, such as ‘evo-devo’, is finding a common conceptual framework and language. This issue was a recurrent theme at the Boulder meeting where there were lively discussions on the precise meaning and usage of terms and concepts after several presentations. No better example of the plethora of meanings was evident following the innocent question – what precisely is a module? Ecologists, morphologists and molecular biologists proposed strikingly different definitions that were characterized by what was and what was not included within an individual module. Attempts to formulate universal definitions that will satisfy everyone remain an important challenge. This meeting showed that the next generation of plant biologists is becoming increasingly sophisticated at learning different discipline-specific languages and interweaving information from each field. There is good reason to believe that this intellectual potential will result in a community of scientists that can seamlessly weave these threads into new and dynamic views of how novel plant structures have been fashioned through time. In the final analysis, the recent MORPH meeting raised many more issues than it solved – but the issues discussed provided us with a greater appreciation of how traditionally distinct fields of research can interface in new and productive ways. One promising and important theme that emerged from the meeting is that graduate students are becoming savvier – more aware of the interdisciplinary implications of their work. They are thinking about adaptation and developmental variation as important components of their research; they are carefully considering the phylogenetic context of their study systems; and they are worrying about how best to bring new levels of sophistication to our understanding of the evolutionary diversification of plant life. That is very good news for the field. The key will be to ensure that graduate and postdoctoral training is unburdened from the canalized thinking and intellectual approaches of the subdisciplines of ecology, organismic biology and molecular genetics. Beyond the need for future small meetings that bring diverse perspectives together in a single room, we need to continue to promote interdisciplinary training at every possible venture. As exemplified by the robust and lively interactions at the MORPH meeting, a modest investment in interdisciplinary dialogue and training can pay off handsomely.

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