Jeffrey Robert Powell

Professor of Ecology and Evolutionary Biology, of Epidemiology (Microbial Diseases) and of Forestry And Environmental Studies

Research Summary

Our laboratory focuses on genetic aspects of the evolutionary process. The majority of our work is based on analysis of DNA, although the results are applied to issues of basic evolution, population biology, phylogeography, and phylogenies. We use molecular data to understand higher level phenomena.

There are 3 major research programs of interest: Anopheles and Aedes mosquito genetics, the evolution of codon usage bias in Drosophila, and conservation genetics of Galápagos Tortoises. While these may seem like rather disparate areas of research, much of the empirical data is the same, as are the analytical techniques and conceptual issues. These are simply examples of the application of modern evolutionary genetics in different contexts.

Extensive Research Description

1. Speciation: History: The genetic changes that initiate the first steps of the speciation processes and the population processes stimulating these changes have been perplexing problems in evolution and genetics. How does one lineage become two? While Darwin’s famous book was titled “Origin of Species” ironically it did not, in fact, address that problem.

My contributions:One line of research I followed was to investigate the role of founder events, the founding of new populations by one or a few individuals, producing an extreme population bottleneck, as an initiating factor in speciation. I chose to model the process in laboratory populations of Drosophila. This resulted in evolution of the first stages of genetic isolation between populations, unexpectedly by inducing changes in mating preferences (1 and 2). A second line of research focused on the mosquito Anopheles gambiae and it very close relatives. We studied the genetics of reproductive isolation between very closely related species and confirmed a major role for the X chromosome (3). In addition, using this complex of mosquitoes we provided evidence supporting the chromosome theory of speciation (4).

1. Powell, J.R. 1978 The founder-flush speciation theory: an experimental approach. Evolution 32:465-474.

2. Dodd, D.M.B. and J.R. Powell. 1985. Founder-flush speciation: An update on experimental results with Drosophila. Evolution 39:1388-1392.

3. Slotman, M.A., A. della Torre, and J. R. Powell. 2004 The genetics of inviability and sterility in hybrids between Anopheles gambiae and An. arabiensis. Genetics 167:275-287.

4. Manoukis, N., J. R. Powell, M. B. Touré, A. Sacko, F. E. Edillo, S. F. Traoré, C. E. Taylor, and N. J. Besansky. 2008. A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae. Proc. Natl. Acad. Sci. USA 105:2940-2945.

2. Chromosomal inversions: History: Naturally occurring chromosomal inversions are among the most important genetic variants in understanding selection and adaptations in dipteran insects. In fact they were the first type of genetic variants demonstrated to be under very strong selection. Drosophila and anopheline mosquitoes that have polytene chromosomes amenable to rapid identification of inversions are paradigms in the study of inversions.

My contributions: In Drosophila, I was involved in studies of inversions in natural populations including studies that spanned forty years as well as studied their role in habitat choice. I edited and contributed two chapters to the only book on the subject (1). In anopheline mosquitoes, I’ve worked on issue of introgression of inversions between species (2) and their role in adaptations to a variety of environmental variables (3).

1. Krimbas, C. B. and J. R. Powell (eds). 1992 Drosophila Inversion Polymorphisms CRC Press, Boca Raton, Florida.

2. della Torre, A., L. Merzagora, J. R. Powell and M. Coluzzi. 1997. Selective introgression of paracentric inversions between two sibling species of the Anopheles gambiae complex. Genetics 146:239-244..

3. Powell, J. R., A. Caccone, V. Petrarca, A. della Torre, and M. Coluzzi. 1999. Population structure, speciation, and introgression in the Anopheles gambiae complex. Parassitologia 41:101-115.

3. Molecular evolution: History: As molecular technologies became increasingly used in evolutionary genetic, the entire field of molecular evolution blossomed and I became heavily involved. This was particularly true after PCR matured as a convenient and efficient way to study DNA variation in virtually any targeted part of a genome, in a very broad range of organisms. This has led to a quantum leap in evolutionary biology and genetics.

My contributions: My work in molecular evolution falls into four main categories.

(a) In the 1980s, a state of the art method for determining genetic changes was DNA-DNA hybridization. I showed that mitochondrial DNA (mtDNA) and nuclear DNA were evolving at similar rates in Drosophila (unlike most eukaryotes studied at the time) as well as examined the rate of protein-coding DNA relative to total DNA. The relative rates of genes expressed at different times of development was also determined. At that time there was considerable controversy concerning the relationship of humans and apes and we produced what many considered the definitive result (1). (b) I discovered that mtDNA was able to cross species boundaries more easily than nuclear DNA (2). This was the first time this had been shown and it is now widely accepted. (c) I have studied the issue of codon usage bias (CUB) in a number of contexts. We provided strong evidence that synonymous substitutions are not always neutral and that selection for codon usage occurs primarily during translation (3). We provided evidence that tRNAs play a critical role in CUB. We also studied whether genes expressed at different stages of development exhibit different levels of CUB. Most recently, we develop an experimental methodology to examine the effects of codon usage on translation and transcription (4). My work in molecular evolution led to my election as president of the most prestigious society in the field, the Society for the Study of Molecular Biology and Evolution.

1. Caccone, A. and J.R. Powell. 1989 DNA divergence among hominoids. Evolution 43:925-942.

2. Powell, J.R.1983. Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: Evidence from Drosophila. Proc. Natl Acad. Sci., USA 80:492-495.

3. Powell, J. R. and E. N. Moriyama. 1997 Evolution of codon usage bias in Drosophila. Proc. of the Natl. Acad.Sci.USA, 94:7784-7790.

4. Powell,J.R. and K. Dion. 2015. Effects of codon usage on gene expression: empirical studies on Drosophila. J. Molecular Evolution 80:219-226.

4. Vector genetics: History: Genetic studies of arthropods that transmit human diseases is has proven a very fruitful venue of research for basic understanding of evolution as well as providing insights important in understanding and control many important infectious diseases such as malaria and dengue fever. Ultimately, the dream is to use genetics to manipulate populations to render the vectors incapable of transmitting pathogens.

My contributions: Population genetics of Aedes aegypti has been a major focus of my research for 40 years. We produced the first worldwide study of the genetic diversity of this species (1) that has been characterized by others as “monumental” and “pathbreaking”. We have expanded and improved on this previous work by harnessing modern DNA-based methods including a SNP chip. These newer methods have allowed us to refine understanding of the genetic diversity of Ae. aegypti especially impacts on association with humans (2) as well as identifying the origin of new introductions. We have also proposed a new method of using genetics to control disease transmission (3). I am also involved in population genetic analyses of releases of transgenic mosquitoes in Brazil. In anophelines, I have studied the molecular evolution of genes involved in innate immunity. A major finding was identifying the gene LRIM-1 as being crucial (4), a finding since confirmed and now this gene is the focus of research in many labs.

1. Tabachnick, W. and J. R. Powell. 1979. A worldwide survey of genetic variation in the yellow fever mosquito, Aedes aegypti. Genetical Research 34:215-229.

2. Brown, J. E., B. Evans, W. Zheng, V. Abas, L. Barrera-Martinez, A. Egizi, H. Zhao, A. Caccone, and J. R. Powell. 2014. Human impacts have shaped historical and recent evolution in Aedes aegypti, the dengue and yellow fever mosquito. Evolution 68:514-525.

3. Powell, J. R. and W. J. Tabachnick. 2014. Genetic shifting: A novel approach for controlling vector-borne diseases. Trends Parasitology 30:282-288.

4. Slotman, M. A., A. Parmakelis, J. C. Marshall, P. Awono-Ambene, C. Antonio-Nkondjio, F. Simard, A. Caccone and J. R. Powell. 2007 Patterns of selection in anti-malarial immune genes in malaria vectors: evidence for adaptive evolution in LRIM1 in Anopheles arabiensis. PloS One 8:e793.

5. Conservation genetics: History: Because modern genetic technology can be used to study genetic variation in virtually any organism, the field of conservation genetics has arisen. Understanding patterns and levels of genetic variation in endangered species allows guidance in design of programs to protect them and their genetic diversity. Serendipitously, I became involved in genetic studies of giant tortoises on the Galapagos Islands, which led to other conservation studies. My contributions: I have 27 publications that deal with conservation genetics including cetaceans (1) and rhinoceros (2). However most work has been on Galapagos tortoises including the first phyloegeographic studies (3) and genetic analyses of a successful repatriation program (4). I also started and continue to teach the only conservation biology course at Yale.

1. Milinkovitch, M., A. Meyer, and J. R. Powell. 1994. Phylogeny of all major groups of cetaceans based on DNA sequences from three mitochondrial genes. Molecular Biology and Evolution 11:939-948.

2. Amato, G. D., D. Wharton, Z. Z. Zainuddin, and J. R. Powell. Assessment of conservation units for the Sumatran rhinoceros (Dicerorhinus sumatrensis). Zoo Biology 14:395-402.

3. Caccone, A., G. Gentile, J. P. Gibbs, T. H. Fritts, H. L. Snell, Jessica Betts, and J. R. Powell. 2002. Phylogeography and history of giant Galápagos tortoises. Evolution 56:2052-2066.

4. Milinkovitch, M. C., D. Monteyne, M. Russello, J. P. Gibbs, H. L. Snell, W. Tapia, C..Marquez, A. Caccone, and J. R. Powell. 2007. Giant Galápagos tortoises: Molecular genetic analysis of a repatriation program of an endangered taxon. BMC Ecology 7:2.

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