Disease and species range limits

Infectious disease is a ubiquitous force on the evolution and ecology of species. However, at a very fundamental level, our understanding of how pathogens influence the distributions of their host species is lacking, yet it is relevant for understanding and predicting species ranges. Recent studies have suggested that species range margins are hotspots for disease emergence and host-pathogen co-evolutionary processes. The goal of our research is to understand how disease affects host species margins, and how co-evolutionary and ecological feedbacks determine disease incidence at range edges.

We are studying anther-smut disease (caused by the fungus Microbotryum) and its impact on the genus Dianthus (wild carnations) in natural alpine populations. Anther-smut disease is transmitted by pollinators and infected plants are sterilized. The study sites in the Maritime Alps have 'replicate' valley systems with steep elevational gradients. We are testing the prediction that sterilizing diseases with frequency-dependent transmission limit the distribution of host populations. We are using theoretical modeling, in situ field experiments, lab cross inoculation studies, and long-term seed and pathogen storage to investigate how co-evolutionary processes in marginal populations affect range limits.

This research is being carried out in conjunction with Drs. Martin Wu at the University of Virginia, Michael Hood at Amherst College, and with scientists in Italy in the Marguareis Park (Dr. Valentina Carasso).


Antonovics, J., Newman, T. J., and Best, B. J. 2001. Spatially explicit studies on the ecology and genetics of population margins. In: Silvertown, J. and Antonovics, J. (eds.) Integrating Ecology and Evolution in a Spatial Context. pp. 91-116. Blackwell, Oxford. PDF

Antonovics, J., McKane, A. J., and Newman, T. 2006. Spatio-temporal dynamics at population margins. American Naturalist 167: 16-27. PDF

Antonovics, J. 2009. The effect of sterilizing diseases on host abundance and distribution along environmental gradients. Proceedings of the Royal Society of London, Series B 276: 1443-1448. PDF

Hood, M.E., Mena-Ali, J.I., Gibson, A. K., Oxelman, B., Giraud, T., Yockyeng, R., Arroyo, M., Conti, F., Pedersen, A., Gladieux, P., and Antonovics, J. 2010. The global distribution of the anther-smut fungus Microbotryum on species of the Caryophyllaceae as assessed from natural history collections. New Phytologist 187: 217-229. PDF

Antonovics, J. and Edwards, M. 2011. Spatio-temporal dynamics of bumblebee nest parasites (Bombus subgenus Psythirus spp.) and their hosts (Bombus spp.). Journal of Animal Ecology 80: 999-1011. PDF

Best, A., Webb, S., Antonovics, J. and Boots, M. 2012. Local transmission processes and disease-driven host extinctions. Theoretical Ecology 5: 211-217. PDF

Support: NSF-DEB 1115899 Collaborative Research: Disease at the margins of species ranges: anther-smut on alpine species.


Metapopulation dynamics of disease

Understanding evolutionary processes in natural populations is of practical applied importance for conservation biology, management of genetically modified crops, invasion biology, and for understanding the potential of populations to respond to global change. The Silene-Microbotryum interaction has become a model system for understanding the impact of disease on natural as well as human populations.

The theory of interconnected populations (metapopulations) has shown that conclusions regarding ecological and evolutionary dynamics derived from single populations can be radically different when considered in a spatial context. Nevertheless there is a lack of field data on spatially distributed populations over extended periods of time to guide and focus this theory.

We have been studying the metapopulation biology of the plant Silene latifolia and its associated pathogen, Microbotyrum violaceum for 25 years. Our annual census data has provided long-term demographic, sex ratio and disease incidence data for more than 800 populations of Silene latifolia, which in turn has generated key insights into how extinction and colonization affects the larger scale population dynamics of the host and pathogen.

In this research we are using our existing knowledge of the age structure of populations, as well as the periodic collection of genetic data, to test hypotheses about the forces determining genetic structure (using neutral markers) and selection (as instantiated by evolution of disease resistance to Microbotryum). Using a high throughput marker approach and likelihood methods, we are assessing the source of colonists and migrants and the degree to which source composition and the founding events affect the genetic composition of demes, and over what time scale.

Using large scale disease resistance screening experiments, we are estimating how founder effects and disease history of source populations drive phenotypic evolution. Specifically, we will test the hypothesis that disease persistence involves inter-demic processes, especially greater founding rates by susceptible genotypes. The census is continuing as is the banking of seeds, collection of DNA and of pathogen cultures. This will provide a multi-year longitudinal data set on evolution in spatially structured populations.


Antonovics, J. 2004. Long term study of a plant-pathogen metapopulation. In Hanski,I., and Gaggiotti, O. (eds.) Ecology, Genetics, and Evolution of Metapopulations. Pp. 471-488. Academic Press. PDF

Moody-Weis, J., Antonovics, J., Alexander, H. M., and Pilson, D. 2008. Predicting local colonization and extinction dynamics from coarser-scale surveys. Ecography 31: 61-72. PDF

Alexander, H. M., Foster, B. L., Ballantyne, F., Collins, C.D., Antonovics, J., Holt, R.D. 2012. Metapopulations and metacommunities: combining spatial and temporal perspectives in plant ecology. Journal of Ecology 100: 88-103. PDF

Support: NSF-DEB 0842296 LTREB: Genetic analysis of metapopulation processes in the Silene-Microbotryum host-pathogen system.


Evolution of host-pathogen genetic systems

The genetics of host-pathogen interactions is notoriously complex; for example, understanding how gene-for-gene systems function, and what determines their genetics, is a challenge both empirically and theoretically.

Most often, the genetic mechanisms of host resistance and pathogen infectivity are explained by the underlying molecular mechanisms, much as genetic segregation and recombination are explained by the mechanics of meiosis. However, the underlying genetic mechanisms of host-pathogen interactions are themselves the product of co-evolution, and so for the past few years I have been rather obsessed with how such co-evolution works and how it may feed back to change the genetics of resistance in the host, and the genetics of infectivity of the pathogen.

My work here is mostly theoretical, with far flung collaborators (see co-authors below), but it has also involved analyzing data sets from research on plants, animals and humans. We are asking how specify among host pathogen interactions evolves, what components of a host-pathogen interacting system are likely to be genetically most variable, and how these processes are influenced by spatial ecology and numerical dynamics.


Fenton, A., Antonovics, J., Brockhurst, M.A. 2009. Host-parasite coevolutionary dynamics under gene-for-gene and inverse gene-for-gene infection genetics. American Naturalist 174: E230–242. PDF

Best, A., White, A., Kisdi, E., Antonovics, J., Brockhurst, M. A., and Boots, M. 2010. The coevolution of host range. .American Naturalist 176: 63-71. PDF

Antonovics, J., Thrall, P. H., Burdon, J. J, and Laine, A. 2011. Partial resistance in natural populations of the Linum-Melamspora host-pathogen system: does partial resistance make the red queen run slower? Evolution 65: 512-522. PDF

Antonovics, J., Boots, M., Ebert, D., Koskella, B., Poss, M., Sadd, B. M. 2012. The origin of specificity by means of natural selection: evolved and non-host resistance in host-pathogen systems. Evolution (DOI: 10.1111/j.1558-5646.2012.01793.x). PDF

Baker, C., and Antonovics, J. 2012. Evolutionary determinants of genetic variation in susceptibility to infectious diseases in humans PlosOne 7 (1) e29089 1-9. PDF

Fenton, A., Antonovics, J., Brockhurst, M.A. 2012. Two-step infection processes can lead to coevolution between functionally independent infection and resistance pathways. Evolution 66: 2030-241. PDF

Support: NSF-DEB 1115899 Collaborative Research: Disease at the margins of species ranges: anther-smut on alpine species. Humboldt Foundation.


Silene angelica: hybrid neo-species or ancestral relict?

Along the banks of the Moorman's River, in Albemarle County and not 10 km from the University of Virginia, there are populations of a species that superficially resembles Silene caroliniana, but differs in being taller and having beautiful bright orange-red flowers. It seems no-one has recorded or studied these populations before. At first sight the plants looks like perhaps a hybrid derivative from a cross between S. caroliniana (with light pink flowers) and S. virginica (with deep red flowers). Tentatively, we have called it S. carolinana ssp. angelica, after the Our Lady of the Angels Monastery, near which it grows and where the sisters have been kind enough to allow us to go on their land to study the plant.

We are now trying to establish the evolutionary status of Silene angelica. Studies using AFLP's by Dr. Steve Keller (now at U. of Maryland) suggest it is as divergent from S. caroliniana and S. virginica as these latter are from each other. All three 'species' cross freely with each other with no evidence of reproductive isolation in the F1, but the hybrid between S. virginica and S. caroliniana does not resemble S. angelica. We therefore wonder whether it is an ancestral species, rather than a neo-species.

Our plan is to use single copy genes to more precisely situate it as derived or ancestral with regard to S. caroliniana and S. virginica. Plants in two of the populations of S. angelica are also infected with anther-smut caused by Microbotryum . Since pathogens are often stated to be better taxonomists than people, we are currently sequencing ITS from the pathogen to see if this can give us additional clues as to the host's origin. Establishing the status of S. angelica is also important because there are very few populations and with one exception, all of them are very small.

References (marginally relevant)

Antonovics, J., Hood, M. E., Thrall, P., Abrams, J. Y, and Duthie, M. 2003. Herbarium studies on the distribution of anther-smut disease (Microbotryum violaceum) and Silene species in the eastern United States. American Journal of Botany 90:1522-1531. PDF


Linnaeus, anther-smut and the germ theory of disease

In 1737 Linnaeus mistakenly named a plant whose floral morphology had been altered by anther-smut disease as a new species; in 1753 he reduced it to a variety and eventually removed it from his classifications. We are examining the origins of Linnaeus' mistake, and the factors that may have led to his realization that he had been dealing not with a new species but with a diseased specimen. We then trace his interest in disease causation, which eventually culminated in his inclusion of the smut diseases under the genus Ustilago in his twelfth edition of the Systema Natura, these being the first named disease-causing microorganisms. We then briefly examine why Linnaeus' realization that living organisms could cause disease failed to convince others of the generality of the germ-theory of disease.


Hood, M. E. and Antonovics, J. 2003. Plant species descriptions show signs of disease. Proceedings of the Royal Society London Series B (Suppl.) 270: S156-S158. PDF


Lydia Becker, Darwin, and disease

Lydia Becker (1827-1890) was a pioneer in the Women's suffragette movement, as well as an enthusiastic botanist. We are researching the interactions between Lydia Becker and Charles Darwin from two major perspectives. First, we are studying the scientific reception of Becker's work by her contemporaries, focusing especially on the debate about the causes of the morphological changes that occur when anther-smut disease induces sex-changes in the flowers of red-campion. We are tracing the scientific thread of Becker's work, and focusing on some of the difficulties her ideas had in being accepted by the predominantly male scientific community, including Darwin himself. Second, we use the correspondence between Darwin and Becker as a mirror against which to gauge Darwin's own involvement in topics related to diseases in humans and plants. Darwin's dislike of medical school is well documented in his own autobiography, especially his revulsion to witnessing operations on children carried out without anesthesia. We are studying why Darwin (perhaps because of his medical school experiences or for some other other reasons) was remarkably disinterested in disease at the intellectual level, and simply did not become involved in the controversies relating to the germ theory of disease, spontaneous generation, or even in the adaptations of parasites to their hosts. Nor did he, like some of his close contemporaries, elaborate on how evolutionary ideas might impinge on our understanding of epidemics. We use these contemporaries as 'controls' to emphasize that these issues were in the forefront of the minds of people at the time, if not in Darwin's. We then suggest that Darwin's disinterest in disease had long term consequences, especially when Darwinian ideas were revitalized as part of the Evolutionary Synthesis in late 1940's.

Support: Much of this work is a continuation of an earlier grant, NSF-DEB 0640777 Collaborative Research: OPUS: Anther-smut as a Disease Model - Traversing Disciplines.


Wilhelm Ludwig: the life of a biologist in wartime Germany

Wilhelm Ludwig (1901-1958) was a German evolutionary biologist who did extensive research on gene frequency change, sex ratio bias, and methods of paternity analysis. He also developed a cogent theory of sympatric speciation. We are studying why his work has been largely ignored, and researching the circumstances of his life before, during and after the second world war as an example of an academic that survived but did not embrace the Nazi regime.


Antonovics, J. 1990. Wilhelm Ludwig and his contributions to population genetics. Trends in Ecology and Evolution 5: 87-90. PDF

Support: Much of this work is a continuation of an earlier grant, NSF-DEB 0640777 Collaborative Research: OPUS: Anther-smut as a Disease Model - Traversing Disciplines.


Florence Nightingale

Florence Nightingale is usually thought of as the giving nurse, as a gentle "Lady with the Lamp", ministering to wounded soldiers in the military hospital during the Crimean war. Less appreciated is the fact that Florence Nightingale was an extremely hard-headed, intransigent, stubborn and determined woman whose main contributions were scientific and political. She did indeed change the nursing profession, but less by example, and more by her powers of organization, of persistence, and strong quantitative background and belief in the power of statistics. All this occurred while she herself was bed-ridden probably as a result of brucellosis acquired during her time in the Crimea. I am researching these "scientific" aspects of her life, especially how she used statistical data in lobbying for better hospital conditions, yet never fully accepted the germ theory of disease. Much of this is using "secondary sources" but it is a story that has not really been told in any complete way before.

Support: Much of this work is a continuation of an earlier grant, NSF-DEB 0640777 Collaborative Research: OPUS: Anther-smut as a Disease Model - Traversing Disciplines.


Unpublished manuscripts and lectures


Antonovics, J. A lecture given to the Dragons Secret Society of Biologists - 1961. PDF

Antonovics, J., and Watson, J. Experimental ecological genetics in Plantago. I. Genetic changes during self-thinning in P. lanceolata. PDF

Tabaee, A., Antonovics, J., and Crone, E.E. Soil toxicity and vegetation composition under electricity pylons, and zinc tolerance in Panicum scoparius. PDF

Antonovics, J. Transmission mode and disease thresholds in host communities. PDF


Translations of classical papers


Aimen, J. 1760. Memoirs presented to the Academy. Research on the progress and cause of floral blight. Tome Troisieme. pp. 68-85. DOC

Goldschmidt, V. 1928. Genetic studies with the biological species of anther-smut (Ustilago violacea Pers). Zeitschrift fur Botanik 21:1-90. DOC

Ludwig, W. 1942. Agrometeorological population genetic contemplation. Unpublished poem sent to Charlotte Boost ca. 1942. DOC

Ludwig, W. 1950. On the theory of competition. Annidation as the fifth evolutionary factor. Neue Ergebnisse und Probleme der Zoologie (Klatt-Festschrift). DOC

Vuillemin, P. 1891. On the effect of parasitism by Ustilago antherarum. Comptes Rendus, Paris 113: 662-665. DOC


Techniques and methods

Seed sterilization

Growing seedlings

Preparing spore samples

Spore germination and bias assays

Single-meristem stage inoculation

Inoculum dilution


5% Chelex DNA extraction

CTAB DNA extraction

Standard Paq polymerase PCR


Agar plates

Silene soil mix