Genome differentiation of Drosophila melanogaster from a microclimate contrast in Evolution Canyon, Israel

Significance The microclimatic contrast between opposing slopes of “Evolution Canyon” (Mount Carmel, Israel) provides a natural laboratory for testing the effects of abiotic factors on biodiversity and population genetic differentiation in a geographical microscale. Drosophila melanogaster fruitflies originating from the opposite canyon slopes are subject to divergent selection leading to slope-specific adaptations, accompanied by incipient mating isolation, all in the face of pervasive demographic processes, including ongoing genetic exchange. We demonstrate that interslope genetic changes in this species accumulate in a number of chromosomal differentiation “islands” and that gene networks related to adaptive responses and reproductive processes are thus significantly affected. The opposite slopes of “Evolution Canyon” in Israel have served as a natural model system of adaptation to a microclimate contrast. Long-term studies of Drosophila melanogaster populations inhabiting the canyon have exhibited significant interslope divergence in thermal and drought stress resistance, candidate genes, mobile elements, habitat choice, mating discrimination, and wing-shape variation, all despite close physical proximity of the contrasting habitats, as well as substantial interslope migration. To examine patterns of genetic differentiation at the genome-wide level, we used high coverage sequencing of the flies’ genomes. A total of 572 genes were significantly different in allele frequency between the slopes, 106 out of which were associated with 74 significantly overrepresented gene ontology (GO) terms, particularly so with response to stimulus and developmental and reproductive processes, thus corroborating previous observations of interslope divergence in stress response, life history, and mating functions. There were at least 37 chromosomal “islands” of interslope divergence and low sequence polymorphism, plausible signatures of selective sweeps, more abundant in flies derived from one (north-facing) of the slopes. Positive correlation between local recombination rate and the level of nucleotide polymorphism was also found.

[1]  Russell B. Corbett-Detig,et al.  Population Genomics of Sub-Saharan Drosophila melanogaster: African Diversity and Non-African Admixture , 2012, PLoS genetics.

[2]  C. Schlötterer,et al.  Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America , 2012, Molecular ecology.

[3]  A. Futschik,et al.  Detecting Selective Sweeps from Pooled Next-Generation Sequencing Samples , 2012, Molecular biology and evolution.

[4]  E. Nevo.  “Evolution Canyon,” a potential microscale monitor of global warming across life , 2012, Proceedings of the National Academy of Sciences.

[5]  E. Nevo,et al.  Differential expression of small heat shock protein genes Hsp23 and Hsp40, and heat shock gene Hsr-omega in fruit flies (Drosophila melanogaster) along a microclimatic gradient. , 2011, The Journal of heredity.

[6]  Bryan D. Kolaczkowski,et al.  Genomic Differentiation Between Temperate and Tropical Australian Populations of Drosophila melanogaster , 2011, Genetics.

[7]  Kevin R. Thornton,et al.  Genome-wide analysis of a long-term evolution experiment with Drosophila , 2010, Nature.

[8]  Philipp W. Messer,et al.  Evidence that Adaptation in Drosophila Is Not Limited by Mutation at Single Sites , 2010, PLoS genetics.

[9]  Michael S. Taylor,et al.  Widespread genomic divergence during sympatric speciation , 2010, Proceedings of the National Academy of Sciences.

[10]  E. Nevo,et al.  Peculiarities of the courtship song in the Drosophila melanogaster populations adapted to gradient of microecological conditions , 2009, Journal of Evolutionary Biochemistry and Physiology.

[11]  E. Nevo,et al.  Adaptive Response to DNA-Damaging Agents in Natural Saccharomyces cerevisiae Populations from “Evolution Canyon”, Mt. Carmel, Israel , 2009, PloS one.

[12]  D. Petrov,et al.  Pervasive Natural Selection in the Drosophila Genome? , 2009, PLoS genetics.

[13]  E. Nevo,et al.  Deletions in the desaturase2 gene in Israeli populations of Drosophila melanogaster: possible role in mate recognition , 2009, Insect molecular biology.

[14]  E. Nevo,et al.  Drosophila at the "Evolution Canyon" Microsite, MT. Carmel, Israel: Selection Overrules Migration , 2008 .

[15]  E. Nevo,et al.  Drosophila flies in “Evolution Canyon” as a model for incipient sympatric speciation , 2006, Proceedings of the National Academy of Sciences.

[16]  V. Loeschcke,et al.  Climatic adaptation of Drosophila buzzatii populations in southeast Australia , 2006, Heredity.

[17]  E. Nevo,et al.  Adaptive differentiation of thermotolerance in Drosophila along a microclimatic gradient , 2006, Heredity.

[18]  E. Nevo,et al.  Assortative Mating in Drosophila Adapted to a Microsite Ecological Gradient , 2005, Behavior genetics.

[19]  E. Nevo,et al.  Adaptation and incipient sympatric speciation of Bacillus simplex under microclimatic contrast at "Evolution Canyons" I and II, Israel. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  E. Nevo,et al.  Sequence polymorphism of candidate behavioural genes in Drosophila melanogaster flies from ‘Evolution canyon’ , 2005, Molecular ecology.

[21]  Matthew W. Hahn,et al.  Genomic Islands of Speciation in Anopheles gambiae , 2005, PLoS biology.

[22]  Ary A. Hoffmann,et al.  Relative importance of plastic vs genetic factors in adaptive differentiation: geographical variation for stress resistance in Drosophila melanogaster from eastern Australia , 2005 .

[23]  V. Loeschcke,et al.  Variation of life‐history and morphometrical traits in Drosophila buzzatii and Drosophila simulans collected along an altitudinal gradient from a Canary island , 2004 .

[24]  R. Nielsen,et al.  Linkage Disequilibrium as a Signature of Selective Sweeps , 2004, Genetics.

[25]  D. Schluter,et al.  Evidence for ecology's role in speciation , 2004, Nature.

[26]  J. David,et al.  Male Sterility Thermal Thresholds in Drosophila: D. simulans Appears More Cold-adapted Than its Sibling D. melanogaster , 2002, Genetica.

[27]  D. Fournier,et al.  Mutations of acetylcholinesterase which confer insecticide resistance in Drosophila melanogaster populations , 2004, BMC Evolutionary Biology.

[28]  W. Swanson,et al.  POPULATION GENETICS OF ACCESSORY GLAND PROTEINS AND SEXUAL BEHAVIOR IN DROSOPHILA MELANOGASTER POPULATIONS FROM EVOLUTION CANYON , 2003, Evolution; international journal of organic evolution.

[29]  Ary A. Hoffmann,et al.  Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches , 2003 .

[30]  Tomáš Pavlíček,et al.  Microclimatic interslope differences underlying biodiversity contrasts in "Evolution Canyon", Mt. Carmel, Israel , 2003 .

[31]  Pawel Michalak,et al.  Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements. , 2003, Molecular biology and evolution.

[32]  C. Schlötterer,et al.  Microsatellite analysis of Drosophila melanogaster populations along a microclimatic contrast at lower Nahel Oren canyon, Mount Carmel, Israel. , 2002, Molecular biology and evolution.

[33]  Mark Kirkpatrick,et al.  Speciation by Natural and Sexual Selection: Models and Experiments , 2002, The American Naturalist.

[34]  K. Iliadi.  Sexual and reproductive behaviour of Drosophila melanogaster from a microclimatically interslope differentiated population of ‘Evolution Canyon’ (Mount Carmel, Israel) , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  E. Nevo,et al.  Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in “Evolution Canyon,” Israel , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  D. Schluter.  Ecology and the origin of species. , 2001, Trends in ecology & evolution.

[37]  P. Andolfatto,et al.  Regions of lower crossing over harbor more rare variants in African populations of Drosophila melanogaster. , 2001, Genetics.

[38]  M. Feder,et al.  A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression. , 2001, The Journal of experimental biology.

[39]  E Nevo,et al.  Evolution of genome–phenome diversity under environmental stress , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[40]  L. Duret,et al.  Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[41]  E. Nevo,et al.  Nonrandom mating in Drosophila melanogaster laboratory populations derived from closely adjacent ecologically contrasting slopes at "Evolution Canyon". , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Justin C. Fay,et al.  Hitchhiking under positive Darwinian selection. , 2000, Genetics.

[43]  A. Hoffmann,et al.  Desiccation and starvation resistance in Drosophila: patterns of variation at the species, population and intrapopulation levels , 1999, Heredity.

[44]  A. Korol,et al.  A complex adaptive syndrome in Drosophila caused by microclimatic contrasts , 1998, Heredity.

[45]  J. David,et al.  Growth temperature and phenotypic plasticity in two Drosophila sibling species: probable adaptive changes in flight capacities , 1997 .

[46]  E. Nevo.  Evolution in action across phylogeny caused by microclimatic stresses at "Evolution Canyon". , 1997, Theoretical population biology.

[47]  M. Feder,et al.  Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. , 1997, Cell stress & chaperones.

[48]  J. David,et al.  Growth temperature and phenotypic plasticity in two , 1997 .

[49]  Eviatar Nevo,et al.  Asian, African and European biota meet at ‘Evolution Canyon’ Israel: local tests of global biodiversity and genetic diversity patterns , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[50]  A. C. James,et al.  Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations , 1995 .

[51]  R. Hudson,et al.  How can the low levels of DNA sequence variation in regions of the drosophila genome with low recombination rates be explained? , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[52]  A. Korol,et al.  Recombination Variability and Evolution: Algorithms of estimation and population-genetic models , 1994 .

[53]  C. Aquadro,et al.  Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster , 1992, Nature.

[54]  N L Kaplan,et al.  The "hitchhiking effect" revisited. , 1989, Genetics.

[55]  F. Tajima.  Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[56]  M. Aguadé,et al.  Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. , 1989, Genetics.

[57]  P. Spierer,et al.  The Ace locus of Drosophila melanogaster: structural gene for acetylcholinesterase with an unusual 5′ leader. , 1986, The EMBO journal.

[58]  J. M. Smith,et al.  The hitch-hiking effect of a favourable gene. , 1974, Genetical research.