We study evolutionary processes in the crucible of nature. Variation within and between populations over geographic latitudes from Florida to northern Manitoba and from sea level to the Appalachian highlands provides abundant end-products of natural evolutionary events. Questions asked in our laboratory are encompassed in the broader question, " What is the molecular genetic basis of evolutionary change in natural populations?" Our primary research organism is Wyeomyia smithii, a small mosquito that develops only within the water-filled leaves of the purple pitcher plant. The fact that this mosquito is capable of blood-feeding makes it tractable for studies of the molecular genetics and evolution of the blood-feeding phenotype and for investigating the shifting patterns of vector/host interactions in the face of rapid climate change. This arm of our research has far-reaching implications for control of mosquito-borne disease in general, including malaria, dengue, yellow fever, and an array of encephalitises. Facilities unique to our lab include computer-controlled environment rooms in which we are able to recreate any environment from the tropics to polar regions of Earth. We use a variety of quantitative genetic, molecular, and genomic tools to address a broad spectrum of questions including the following ongoing research projects:
We currently enjoy collaborations with members within IE2 as well as outside collaborations with Indiana University, University of California Davis, University of Birmingham (UK), University of Notre Dame and Kansas State University. We typically mentor 15-20 students in the lab from undergraduates to post-docs.
1972, 1974, 1980. First action spectra varying both wavelength and intensity for dawn and dusk transitions in photoperiodic response, thereby providing the first estimates in any animal for the astronomic limits that constitute a photoperiodic "day" in nature. Science 175:1361-1362; Biol. Bull. 146:11-19; Oecologia 44:311-316.
1974. First flora of the Canary Islands covering the Cruciferae, the Crassulaceae and the ferns and their allies. An. INIA/Ser.: Prod. Veg. 4: 165-273.
1976, 1977. First determination of the relationship between altitude and latitude in photoperiodic response, establishing that photoperiodic response tracks the seasonal gradient of North America more closely than any other known ecogeographic trait. This conclusion persists to this day. Nature 262:384-386.; Evolution 31:546-567.
1983, 1988. Non-equilibrium communities of tree-hole mosquitoes in nature are maintained by habitat segregation, drought and predation; the determinants of habitat segregation among the constituent species are genus-level traits and are therefore not a consequence of competitively driven, co-evolved niche shifts as previously predicted by ecological theory. Oecologia 57: 239-256; Oecologia 74:507-514.
1989. Density-dependent development over a wide geographic range in nature is not correlated with either capacity for increase or carrying capacity. r- and K-selection theory is totally without universal predictive power in natural populations. Am. Nat. 133:869-887.
1993, 1997, 2005. Evolution between and within natural populations of Wyeomyia smithii involves complex gene-gene interaction (epistasis). Geographically close sub-populations within a single bog show distinct genetic fingerprints, indicating that population subdivision occurs over a very fine scale or that unique genetic trajectories underlie the evolution of similar phenotypes. Subdivided populations are capable of rapid response to selection and may account for evolution over contemporary time scales. Am. Nat. 142:457-473; Evolution 51:451-458; Genetics 147:1873-1883; 169:485-488.
1995, 1997, 2002. The optimal degree of protandry that maximizes fitness depends not only on the time of emergence of males relative to females, but also on female fecundity and the emergence times of other males in the population. Protandry can be a consequence of natural as well as sexual selection. Ecology 76:1242-1250; 78:969-976; 83:607-611.
2001, 2006, 2008. The first demonstration of a genetic response driven by recent rapid climate change. This genetic shift was shown to occur over as short a time span as five years in photoperiodic response of Wyeomyia smithii. Subsequent studies showed a genetic component in response to climate change in the timing of seasonal events of insects, birds, mammals and plants, but in no case has there been shown to be a genetic shift in thermal optimum or heat tolerance associated with recent rapid climate change in populations in nature. PNAS 98:14509-14511, Science 312:1477-1478; Mol. Ecol. 17:157-166.
2003, 2006, 2009, 2010, 2012. Evolution of the seasonal photoperiodic timer has evolved independently of the daily circadian clock over the climatic gradient of North America in Wyeomyia smithii. It is therefore difficult to argue that circadian clock is an integral, co-dependent component of photoperiodic time measurement. Am. Nat. 161:735-748; 167:601-605; J. Comp. Physiol. A. 195:385-391; J. Biol. Rhythms 25:155-165; Heredity 108:473-479.
2004. During evolutionary dispersal of Wyeomyia smithii throughout the climatic gradient of North America, photoperiodic adaptation has been a more important determinant of fitness than thermal adaptation. In fact, when northern populations are subjected to 180 years of climate warming at its present rate, year-long fitness is improved. However, when they experience parallel, incorrect photic cues (day lengths), they lose 80% fitness. Hence, selection should be expected to favor more rapid evolution of photoperiodic response than thermal tolerance during periods of rapid climate change. Evolution 58:1748-1762.
2007. The first QTL map of photoperiodic response in any animal revealed a "hot" spot in the Wyeomyia smithii genome that includes genes responsible for interpreting day length, for the determination of diapause, and for the hormonal regulation of development and molting. Genetics 176:391-402.
2009. Regulatory, physiological and developmental processes can be tightly integrated into units (modules) made up of multiple genes. Using the core genes comprising the daily circadian clock of Drosophila and other Diptera, we show that simply because a single gene constitutes an important component of a module does not preclude its having a separate and important ancillary function outside of its modular unit. This underappreciated but essential distinction between modular and gene pleiotropy has revolutionized the field of biological time-keeping mechanisms. Trends Genetics 25:217-225.
2010. The first fine-scale phylogeography using second-generation high throughput sequencing in any animal. PNAS 107:16196-16200.
2012. This study presents the first direct evidence that the genetic basis of seasonal photoperiodic timing is highly complex, not only across climatic gradients through evolutionary time, but even among individuals within single populations of a species. Hence, seeking genetic commonalities among diverse species is going to be far more elusive than the historical progress made in identifying common genetic mechanisms in daily circadian time keeping. Proc. R. Soc. B 279:4551-4558.
2013. The first test for repeatability of phylogenetic inference among natural populations within a single species using second-generation high throughput sequencing. A composite maximum parsimony tree of 46 populations of the pitcher-plant mosquito was created and verified with reference to the historical biogeography of flora associated with pitcher plants during sequential recession of the Laurentide Ice Sheet. The resulting phylogeography presents a fine scale example of post-glacial range expansion and points out the essential importance of redundant sampling, particularly in areas of geological disruption. PLoS ONE 8:e72262.
2015. Relative rate of circadian clock gene evolution between the sabethine mosquito Wyeomyia smithii and six other insect taxa does not differ between core feedback-loop genes and their post-translational modifiers. BMC Genomics 16:754.