Our laboratory is examining a broad range of evolutionary questions, including the evolution of sex and recombination, the evolution of microsatellites in lower organisms, microevolutionary events that take place in the course of infection in the genomes of pathogens, the evolution of HIV and other viruses, the timing of genetic events that have taken place during the history of our species, and the evolutionary divergence of distantly related proteins. We are also examining the maintenance of diversity in complex genetic systems and complex ecosystems. We have found that the major gene directing sexual recombination, the MAT locus, has pleiotropic effects that range far beyond meiotic and mitotic recombination and DNA repair, to encompass cellular processes as different as the uptake of exogenous DNA and the regulation of mitochondrial activity. Our results strongly support the concept that the evolution of sex had its beginnings in the uptake and incorporation by cells of exogenous genetic material. We are investigating large numbers of polymorphic microsatellites in yeast, some of which may be correlated with fitness. Such microsatellites are surprisingly common in lower organisms, and we have shown that microsatellites of the pathogenic fungus Candida albicans undergo alterations in the course of infection in AIDS patients. We have also found abundant polymorphic microsatellites in the important viral pathogen cytomegalovirus.
We are also developing a selective PCR system in Saccharomyces cerevisiae which will allow us to follow the accumulation of microsatellite length mutations over time in stressed and unstressed populations.
We have developed a number of methods for increasing the amount of evolutionary information in phylogenetic trees. This has enabled us to obtain a more accurate estimate of the date, and the probable geographic location, of the mitochondrial Eve. This methodology has also enabled us to determine more accurate human retrovirus evolutionary trees. Using this approach, we were able to show that the evolution of n-glycosylation sites ("sequons") in the envelope gene has proceeded at three times the rate in HIV-1 that it has in the less pathogenic HIV-2. This is the largest difference in evolutionary rate that has yet been detected in these viruses, and is likely to be connected to their interaction with the host immune system.
Another research direction in the laboratory has been the mechanisms maintaining genetic diversity. We recently proposed a model of "genetic herd-immunity" to explain the maintenance of such highly polymorphic genetic systems as MHC. This frequency-dependent model permits a genetically heterogeneous host population to keep many pathogens at bay simultaneously. Stephen Hubbell, Richard Condit and I have recently extended this model to the maintenance of diversity in the rainforest, and have evidence from well-studied rainforests in Panama and Malaysia that herd-immunity at the level of species is in fact operating.
Most recently, we have shown that for seven different tropical rainforests, in both the Old and New Worlds, cohorts of trees increase in diversity over time because the locally commoner species have a higher mortality than the locally rarer ones. These results, which show that there are strong non-random processes increasing diversity in these forests, are consistent with several frequency-dependent models for the maintenance of diversity.
I have published a number of books about evolution for general readers, most recently “The Darwinian Tourist” (Oxford University Press, 2010). The book deals with how ecosystems throughout the world have been shaped by the process of evolution. My new book on ecology, evolution, and our interactions with the natural world, "Green Equilibrium: Balancing the Futures of Our Species and Our Planet," will be published by Oxford University Press in early 2013.
Recent papers and books
Wills, C., and J. Bada. (2000). The Spark of Life: Darwin and the Primeval Soup. Perseus Books, Cambridge, MA.
Birdsell, J., and C. Wills. (2003). The evolutionary origin and maintenance of sexual recombination: a review of contemporary models. Evolutionary Biology 33:27-138.
Metzgar, D., L. Liu, C. Hansen, K. Dybvig, and C. Wills. (2002). Domain-level differences in microsatellite distribution and content result from different relative rates of insertion and deletion mutations. Genome Research 12:408-413.
Wills, C., R. Condit, S. P. Hubbell, R. B. Foster, and N. Manokaran. (2004). Comparable nonrandom forces act to maintain diversity in both a New World and an Old World rainforest plot. Pp. 384-407 in E. C. Losos and E. G. J. Leigh, eds. Tropical Forest Diversity and Dynamism: Findings from a Large-Scale Network. University of Chicago Press, Chicago.
Wills, C., K. E. Harms, R. Condit, D. King, J. Thompson, F. He, H. C. Muller-Landau, P. Ashton, E. Losos, L. Comita, S. Hubbell, J. LaFrankie, S. Bunyavejchewin, H. S. Dattaraja, S. Davies, S. Esufali, R. Foster, N. Gunatilleke, S. Gunatilleke, P. Hall, A. Itoh, R. John, S. Kiratiprayoon, S. L. de Lao, M. Massa, C. Nath, M. N. S. Noor, A. R. Kassim, R. Sukumar, H. S. Suresh, I.-F. Sun, S. Tan, T. Yamakura, and J. Zimmerman. (2006). Nonrandom processes maintain diversity in tropical forests. Science 311:527-531.
Wills, C. (2005). Revision of the evolution section of Campbell’s Biology, 7th edition. This text, the most widely used introductory biology text, provides an introduction to evolution for 150,000 beginning biology majors each year.
Wills, C. (2010). The Darwinian Tourist, Oxford University Press. This book, illustrated with 150 of the author’s photographs from above and under the water around the world, shows how the world’s living systems have been shaped by the process of evolution. It was called probably the year’s most important travel book” by Conde Nast Traveler.
Veretnik, S., C. Wills, P. Youkharibache, R. E. Valas, and P. E. Bourne (2009). Sm/Lsm Genes Provide a Glimpse into the Early Evolution of the Spliceosome. PLoS Comput. Biol. 5.
Wills, C. (2011a). Genetic and phenotypic consequences of introgression between humans and Neanderthals. Advances in genetics 76:27-54.
Wills, C. (2011b). Rapid recent human evolution and the accumulation of balanced genetic polymorphisms. High Altitude Medicine & Biology 12:149-155.
Wills, C. (2013). Green Equilibrium: Balancing the Futures of Our Species and Our Planet. Oxford University Press, in press.http://biology.ucsd.edu/faculty/wills...