The Journal of Ecology Editors are delighted to announce that Helen Alexander is our Eminent Ecologist award winner for 2019. In recognition of her work, we have asked Helen to put together a special Virtual Issue of some of her excellent contributions to the journal. Helen was interviewed by Executive Editor David Gibson at the last ESA annual meeting to discuss her career and ecological inspirations. Helen has also written this blog, summarising her career, research and personal experiences.

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Helen is a professor in the Department of Ecology and Evolutionary Biology, at the University of Kansas, Kansas, USA. Helen is also a member of the University of Kansas Field Station‘s Executive Committee which guides the long-term direction of this well-known facility. Helen is a plant population ecologist, she obtained her PhD in botany and genetics from Duke University, and she has made major contributions in exploring the ecology and evolution of plant-pathogen interactions. 

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I am very honored that the Editors of Journal of Ecology have decided to create a virtual issue of some of my papers. I am deeply appreciative of all my coauthors, which include undergraduate and graduate students. These colleagues, and the many people listed in the Acknowledgments section of papers, are smart and creative scientists. Furthermore, they are kind, generous, and fun — essential traits for enjoyable and productive science, especially after long days in the field or on the computer.

My research is in plant population biology. This discipline intrigues me because whether a population grows or declines, and the degree to which it is genetically variable, are features that are central to questions in ecology, evolution, and conservation. My 11 chosen papers (spanning from 1985 to 2017) cover three research themes: Theme 1 – Ecology and evolution of plant-pathogen interactions, Theme 2 – Seed and seed bank ecology, and Theme 3 – Ecology of long-lived herbaceous plants and the challenge of “detectability.”

Theme 1 – Ecology and evolution of plant-pathogen interactions

Pathogens of plants, including fungi, bacteria, and viruses, are ubiquitous and have long been an important focus in agriculture. Early work by Harper (1977) and Burdon (1987) emphasized that pathogens can also shape the ecology and evolution of plants outside the crop field. I began studies of fungal plant disease as a graduate student with Janis Antonovics and Mark Rausher in the late 70’s/early 80’s. After a postdoc in plant pathology, I followed up on Janis’ enthusiastic suggestion to check out a dioecious plant, the white campion (Silene latifolia, formerly S. alba) that was infected by an anther smut fungus (Microbotryum violaceum, formerly Ustilago violacea). Infection by this fascinating fungus results in anthers in the flowers being filled with spores instead of pollen. In female plants, the ovary aborts and is replaced by spore-producing anthers (Fig. 1). Since one of the modes of disease transmission is by flower-visiting insects, anther smut shares properties with venereal diseases. Three of my chosen papers used these organisms to ask questions about disease ecology and evolution. 

My first chosen paper, Alexander & Antonovics (1988) combined my field studies of plant survival, reproduction, and disease transmission with a population model developed by Janis. I have fond memories of Janis peppering me with questions about plant demography and disease spread as he built the first version of the model on a Mountain Lake Biological Station (Virginia) blackboard one evening. This model showed that rates of plant recruitment and disease spread affected whether one would expect coexistence of the plant and fungus, local extinction of the plant due to fungal infection, or local extinction of the fungus.

My second and third chosen papers, Alexander, Antonovics et al. (1993) and Alexander & Antonovics (1995) addressed evolutionary questions: What is the extent of genetic variation in resistance in plant population? Are particular plant traits associated with resistance? Is there evidence for fitness costs of resistance? To assess genetic variation under realistic conditions, we created experimental populations where healthy plants with known genetic relationships (clones or progeny of crosses) were planted in a field along with infected plants to provide a source of fungal spores. Establishing these populations was hard work (Fig. 2) and required multiple attempts, but yielded fascinating results. A single field site had genotypes that ranged from very resistant to very susceptible, and we found high heritability for resistance in experiments using progeny of crosses. Given the challenges of field experiments, we were curious if variation in resistance among clones in our field studies could be replicated by greenhouse inoculation studies. In general, we found similar resistance ranking in the two kinds of experiments. However, some genotypes that had low disease levels in greenhouse inoculations had high disease levels in the field, underscoring the importance of field experimentation. These disease-prone genotypes tended to produce flowers early in the season; such plants are likely exposed to fungal spores for a longer period of time and have a longer time for fungal infection to grow into the plant. We expect that resistance may have a fitness cost, since early flowering families that were more prone to infection are likely to have high fitness in the absence of the disease. Janis played a pivotal role in all these studies, which I particularly appreciated since my time was pulled in many directions as I combined science with being a young mom.

In 1987, I become a professor at the University of Kansas. With two young children, I wanted my research to be based in Kansas. Janis and others continued the anther smut research, and the plant and fungus have become model systems (Bernasconi, Antonovics et al. 2009), with work in diverse areas such as distribution of the disease across the Caryophyllaceae (Hood, Mena-Ali et al. 2010), disease transmission (Bruns, Antonovics et al. 2017), evolution of host resistance (Carlsson-Graner & Thrall 2015), and sex chromosome evolution in the fungus (Branco, Carpentier et al. 2018).

In Kansas, I continued working with disease. My fourth chosen paper, Holah & Alexander (1999) is the work of a bright Ph.D. student, Jenny Holah. She explored the world of soil microbes with two prairie plants, a dominant long-lived grass (big blue stem, Andropogon gerardii) and an annual legume (showy partridge pea, Chamaecrista fasiculata). Her research revealed that soil fungi associated with C. fasiculata were detrimental to A. gerardii; such fungi could potentially play a role in the persistence of C. fasiculata in the perennial prairie landscape. Jenny’s work was part of the wave of interest in soil pathogens as important drivers of species coexistence that started in the 90’s and continues today (Bever, Mangan et al. 2015).  

Alexander, Price et al. (2007), my fifth chosen paper, focused on a topic central to ecological inquiry, species distributions. We asked whether diseases are less common as one reaches the edge of the host’s geographical range. Our work took advantage of shifts in tree cover in Kansas: we compared populations of a woodland sedge, Carex blanda, from eastern Kansas (where trees are common) to central Kansas (where woodlands are patchy; edge of the sedge’s range). Field work was challenging: an amazing undergraduate, Sarah (Sam) Price, took many solo trips across Kansas searching for the most western locations of the sedge. We found that plant populations at the edge of their range were less likely to be infected by both a smut (Fig. 3) and a rust fungus. Our field results were generally consistent with surveys we performed with herbarium sheets (Fig. 3), where we adapted clever approaches developed by Antonovics, Hood et al. (2003). Our conclusions that edge host populations were less likely to have disease is consistent with theoretical expectations for pathogens likely transmitted by wind and water. In contrast, vector-transmitted diseases are predicted to lack such a “disease-free halo,” as recently demonstrated with empirical studies of anther-smut diseases (Bruns, Antonovics et al. 2019, see also Emily’s video podcast).

My sixth chosen paper, Alexander, Bruns et al. (2017), illustrates my current fascination with plant viruses. In close collaboration with Carolyn Malmstrom, I explored the effects of virus infection on plant fitness. Although we often assume virus infection will have negative effects on plants, viruses can also potentially act as mutualists (Roossinck 2011). Few field data on fitness effects exist on this topic, especially for perennial plants. We set up a field experiment with two ecotypes of switchgrass (Panicum virgatum): plants were or were not inoculated with the barley yellow dwarf virus, BYDV (Fig. 4). Our collaborator Emily Bruns analyzed multiyear data on survival and reproduction with the program “aster” (Shaw, Geyer et al. 2008) and found that the virus reduced plant fitness by 30% over two years. This reduction was greater than predicted from individual fitness components and occurred despite few overt symptoms of infection. We also followed virus presence in the field plants over time, and found evidence for ecotypic variation in resistance to the virus. I see plant virus ecology as a particularly important area for future research: viruses have broad host ranges, mobility across landscapes due to arthropod vectors, and likely a range of effects on plant fitness (Alexander, Mauck et al. 2014, Malmstrom and Alexander 2016, Shates, Sun et al. 2019). 

This post continues in Eminent Ecologist 2019: Helen Alexander (part 2)