Modification of Heat-Shock Gene Expression in Drosophila melanogaster Populations via Transposable Elements

Lerman, Daniel N.; Michalak, Pawel; Helin, Amanda B.; Bettencourt, Brian R.; Feder, Martin E.

doi:10.1093/molbev/msg015

Cited by 89 publications

(94 citation statements)

References 55 publications

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“…Until recently, the role of transposable elements in adaptive evolution of Drosophila was thought to be minimal because surveys of particular element insertions suggested that they occur only at low frequency within species and are never fixed between species (39). However, recent studies have shown that transposon insertions play a large role in transcriptional regulation of hsp70 in Drosophila (40,41) and in the evolution of regulatory and coding sequences of genomes in general (42)(43)(44). Our data are consistent with the notion that transposable element insertions occasionally act as beneficial mutations, particularly with respect to transcriptional regulation.…”

Section: Discussionsupporting

confidence: 90%

Strong selective sweep associated with a transposon insertion inDrosophila simulans

Schlenke

Begun

2004

Proc. Natl. Acad. Sci. U.S.A.

223

190

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We know little about several important properties of beneficial mutations, including their mutational origin, their phenotypic effects (e.g., protein structure changes vs. regulatory changes), and the frequency and rapidity with which they become fixed in a population. One signature of the spread of beneficial mutations is the reduction of heterozygosity at linked sites. Here, we present population genetic data from several loci across chromosome arm 2R in Drosophila simulans. A 100-kb segment from a freely recombining region of this chromosome shows extremely reduced heterozygosity in a California population sample, yet typical levels of divergence between species, suggesting that at least one episode of strong directional selection has occurred in the region. The 5 flanking sequence of one gene in this region, Cyp6g1 (a cytochrome P450), is nearly fixed for a Doc transposable element insertion. Presence of the insertion is correlated with increased transcript abundance of Cyp6g1, a phenotype previously shown to be associated with insecticide resistance in Drosophila melanogaster. Surveys of nucleotide variation in the same genomic region in an African D. simulans population revealed no evidence for a high-frequency Doc element and no evidence for reduced polymorphism. These data are consistent with the notion that the Doc element is a geographically restricted beneficial mutation. Data from D. simulans Cyp6g1 are paralleled in many respects by data from its sister species D. melanogaster.T he spread of beneficial mutations is expected to reduce variation at linked sites, a phenomenon known as genetic hitchhiking (1, 2). All else being equal, the size of the swept region depends on the selection coefficient of the beneficial mutant and the local recombination rate. Theoretical results show that for regions of normal recombination in Drosophila, hitchhiking effects associated with moderately strong selection should result in localized regions of reduced heterozygosity (3). Thus, in principle, the frequency and locations of selective sweeps can be determined by scanning chromosomes for ''valleys'' of reduced variation (4). The paucity of large genomic regions of severely reduced heterozygosity from recombining regions in Drosophila and other organisms (4-7) suggests that novel mutations with large positive selection coefficients are rare, although it does not rule out the evolutionary importance of such mutations.In this study, we document the existence of a 100-kb chromosomal region that has extremely reduced heterozygosity in a Drosophila simulans population sample from California, but not in a sample from Africa, indicating the recent and geographically restricted sweep of a unique, beneficial mutation. Furthermore, we report the unusual observation of an intact transposable element in this region, which occurs at very high frequency in the California, but not Africa, sample. The transposon insertion is associated with increased transcript abundance of the downstream cytochrome P450 gene Cyp6g1. These data are...

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Section: Discussionsupporting

confidence: 90%

Strong selective sweep associated with a transposon insertion inDrosophila simulans

Schlenke

Begun

2004

Proc. Natl. Acad. Sci. U.S.A.

223

190

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“…In the 'Evolution Canyon' populations, naturally occurring P transposable elements disrupt the proximal promoters of at least two of the five Hsp70-encoding genes. Such disruptions can reduce hsp70 mRNA transcription, Hsp70 protein levels, and thermotolerance (Lerman et al, 2003;Lerman and Feder, 2004). In the 'Evolution Canyon' Drosophila, hsp70 alleles in which the P element is present or absent segregate in a balanced polymorphism, but at higher allelic frequencies in the NFS population than in the SFS population.…”

Section: Discussionmentioning

confidence: 99%

Adaptive differentiation of thermotolerance in Drosophila along a microclimatic gradient

et al. 2006

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We examined whether a remarkable occurrence -the physiological evolution of two Drosophila melanogaster populations, despite a spatial separation of only 100-400 m, was idiosyncratic and temporary, or persisted over multiple years. We ascertained the high-temperature tolerance of Drosophila descended from populations on the north-facing slope (NFS) and south-facing slope (SFS) of 'Evolution Canyon' (Lower Nahal Oren, Mt Carmel, Israel), which were collected in 1997, 1999, and 2000. Results for these Drosophila uniformly resembled other studies in many respects: an inverse relationship between survival and heat-shock temperature, male-female differences in thermotolerance, and inducible thermotolerance. Importantly, for all years of collection, SFS flies consistently exceeded NFS flies in basal and inducible thermotolerance after diverse heat shocks, with and without thermal pretreatment, and whether isofemale lines, synthetic populations, or inbred lines were compared. Inbred lines, however, had lower thermotolerance than outbred lines. Several nonexclusive processes may explain the evolution of such physiological differentiation.

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“…Transposons interfering with the expression of hsp70s can alter several organismal fitness features. Natural selection has been reported against these hsp70 promoter insertions in populations experiencing thermal stress (Michalak et al, 2001;Lerman et al, 2003).…”

Section: The Importance Of Regulatory Change In Micro-evolutionmentioning

confidence: 99%

Molecular mechanisms of heavy metal tolerance and evolution in invertebrates

Janssens¹,

Roelofs²,

Straalen³

2009

Insect Science

149

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Following the genomics revolution, our knowledge of the molecular mechanisms underlying defenses against stress has been greatly expanded. Under strong selective pressure many animals may evolve an enhanced stress tolerance. This can be achieved by altering the structure of proteins (through mutations in the coding regions of genes) or by altering the amount of protein (through changes in transcriptional regulation). The latter type of evolution can be achieved by substitutions in the promoter of the gene of interest (cisregulatory change) or by altering the structure or amount of transcriptional regulator proteins (trans-regulatory change). The metallothionein system is one of the best studied stress response systems in the context of heavy metals. Metallothionein expression is assumed to be regulated by metal transcription factor 1 (MTF-1); however, up to now the involvement of MTF-1 has only been proven for some vertebrates and Drosophila. Data on invertebrates such as nematodes and earthworms suggest that other mechanisms of metallothionein induction may be present. A detailed study of Cd tolerance was done for a species of soilliving springtail, Orchesella cincta. The metallothionein gene of this species is overexpressed in metal-exposed field populations. Analysis of the metallothionein promoter has demonstrated extensive polymorphisms that have a functional significance, as shown in bioreporter assays. In a study comparing 20 different populations, the frequency of a high-expresser promoter allele was positively correlated with the concentration of metals in soil, especially Cd. The springtail study shows that cis-regulatory change of genes involved in the cellular stress response may contribute to evolution of metal tolerance.

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Modification of Heat-Shock Gene Expression in Drosophila melanogaster Populations via Transposable Elements

Cited by 89 publications

References 55 publications

Strong selective sweep associated with a transposon insertion inDrosophila simulans

Strong selective sweep associated with a transposon insertion inDrosophila simulans

Adaptive differentiation of thermotolerance in Drosophila along a microclimatic gradient

Molecular mechanisms of heavy metal tolerance and evolution in invertebrates

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