Over the last 10,000 years Drosophila melanogaster and D. simulans have spread through the world in the wake of human migration. As a consequence, these now cosmopolitan species have been exposed to a variety of novel environments and habitats. For flies living in temperate environments, winter cold represents a novel environment and these species have evolved in response to cold temperatures in several distinct ways. D. melanogaster has evolved a diapause syndrome that confers extreme lifespan extension, reduction in metabolic rate, and elevated stress tolerance;although diapause increases winter survival, individuals able to diapause suffer a fitness disadvantage during the summer and thus this adaptation remains at intermediate frequencies even at high latitudes. D. simulans, on the other hand, appears to have a more modest adaptive response to winter conditions: this species performs well at cool temperatures but does not appear have the capacity to survive prolonged exposure to the harsh temperate winter. Little is known about other overwintering mechanisms in D. simulans, or indeed any evolutionary response to novel temperate environments. Herein, we propose to identify polymorphisms underlying adaptation to temperate climates in D. melanogaster and D. simulans, link these polymorphisms to function and test hypotheses about the evolutionary origin of these polymorphisms. To do this, we will collect large samples of individuals from both of these species (i) across latitude on the East and West coasts of North America, (ii) through the growing season at several sites near Philadelphia, PA and (iii) along an altitudinal transect in Northern California for four replicate years. First, we will identify polymorphisms that vary in consistent fashion through time and space through high- throughput sequencing technologies and we will verify changes in allele frequency through pyrosequencing. Second, we will identify the functional consequences of a subset of these polymorphisms using quantitative genetic and transcriptomic techniques. We hypothesize that many of the polymorphisms we identify will be associated with phenotypes known to vary in a clinal fashion amongst many drosophilid flies. Finally, we will test hypotheses about the evolutionary origin of these polymorphisms by assessing worldwide haplotype diversity at surrounding loci. We hypothesize that most of these adaptive alleles will be subject to soft- sweeps which are characteristic of species with extremely large population sizes or those with large amounts of genetic variation in ancestral populations such as both D. melanogaster and D. simulans.

Public Health Relevance

Using the model organisms, Drosophila melanogaster and D. simulans, this project seeks to identify genetic polymorphisms underlying adaptation to novel environments, determine their function and test hypotheses about their evolutionary origin. Heuristic and analytic methods developed under this proposal can be applied to genomic data in humans to aid in identifying disease causing loci that have become prevalent in humans as we have colonized the world and been exposed to novel environments.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM100366-02
Application #
8468718
Study Section
Genetic Variation and Evolution Study Section (GVE)
Program Officer
Eckstrand, Irene A
Project Start
2012-05-15
Project End
2016-04-30
Budget Start
2013-05-01
Budget End
2014-04-30
Support Year
2
Fiscal Year
2013
Total Cost
$398,734
Indirect Cost
$105,335
Name
Stanford University
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
009214214
City
Stanford
State
CA
Country
United States
Zip Code
94305
McCoy, Rajiv C; Taylor, Ryan W; Blauwkamp, Timothy A et al. (2014) Illumina TruSeq synthetic long-reads empower de novo assembly and resolve complex, highly-repetitive transposable elements. PLoS One 9:e106689
Bergland, Alan O; Behrman, Emily L; O'Brien, Katherine R et al. (2014) Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet 10:e1004775
Zhu, Yuan O; Siegal, Mark L; Hall, David W et al. (2014) Precise estimates of mutation rate and spectrum in yeast. Proc Natl Acad Sci U S A 111:E2310-8
McCoy, Rajiv C; Garud, Nandita R; Kelley, Joanna L et al. (2014) Genomic inference accurately predicts the timing and severity of a recent bottleneck in a nonmodel insect population. Mol Ecol 23:136-50
Staubach, Fabian; Baines, John F; Kunzel, Sven et al. (2013) Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS One 8:e70749
Messer, Philipp W; Petrov, Dmitri A (2013) Frequent adaptation and the McDonald-Kreitman test. Proc Natl Acad Sci U S A 110:8615-20
Lawrie, David S; Messer, Philipp W; Hershberg, Ruth et al. (2013) Strong purifying selection at synonymous sites in D. melanogaster. PLoS Genet 9:e1003527