Limits...
Indy gene variation in natural populations confers fitness advantage and life span extension through transposon insertion.

Zhu CT, Chang C, Reenan RA, Helfand SL - Aging (Albany NY) (2014)

Bottom Line: However, antagonism between life span and reproductive success frequently poses a dilemma pitting the cost of fecundity against longevity.The transposon insertion also regulates Indy expression level, which has experimentally been shown to affect life span and fecundity.Thus, in the wild, evolution reaffirms that the mechanism of heterozygote advantage has acted upon the Indy gene to assure increased reproductive fitness and, coincidentally, longer life span through regulatory transposon mutagenesis.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Cell Biology and Biochemistry, Division of Biology and Medicine, Brown University, Providence, RI 02912.

ABSTRACT
Natural selection acts to maximize reproductive fitness. However, antagonism between life span and reproductive success frequently poses a dilemma pitting the cost of fecundity against longevity. Here, we show that natural populations of Drosophila melanogaster harbor a Hoppel transposon insertion variant in the longevity gene Indy (I'm not dead yet), which confers both increased reproduction and longevity through metabolic changes. Heterozygosity for this natural long-lived variant has been maintained in isolates despite long-term inbreeding under laboratory conditions and advantageously confers increased fecundity. DNA sequences of variant chromosome isolates show evidence of selective sweep acting on the advantageous allele, suggesting that natural selection acts to maintain this variant. The transposon insertion also regulates Indy expression level, which has experimentally been shown to affect life span and fecundity. Thus, in the wild, evolution reaffirms that the mechanism of heterozygote advantage has acted upon the Indy gene to assure increased reproductive fitness and, coincidentally, longer life span through regulatory transposon mutagenesis.

Show MeSH

Related in: MedlinePlus

World-wide heterozygosity of Hoppel insertion in IndyFrequency of Hoppel insertion in isofemale inbred lines. Each part of the pie chart represents a line from a different geographic origin. The colored area in each represents the frequency of Hoppel + allele in that line (Table S1).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3927810&req=5

Figure 1: World-wide heterozygosity of Hoppel insertion in IndyFrequency of Hoppel insertion in isofemale inbred lines. Each part of the pie chart represents a line from a different geographic origin. The colored area in each represents the frequency of Hoppel + allele in that line (Table S1).

Mentions: In the course of our molecular analyses of Indy gene structure in different Drosophila isolates from around the globe, we found a natural polymorphism present in numerous independent populations. This variant comprises the presence or absence of the transposable element, Hoppel, which has been implicated in regulating gene expression through effects on local chromatin structure [9, 10]. We sought to examine whether heterozygosity for the Hoppel insertion in Indy is maintained in other wild strains. Hoppel is an intronless, defective mobile element related to the P element, is about 1.2kb in average length, and is estimated to have 105 insertions in D. melanogaster euchromatin [11]. Using a PCR based screen, we found that the Hoppel insertion is polymorphic among 22 natural isolate lines (obtained from the Drosophila Species Stock Center, Table S1). Strikingly, many lines were not fixed for the insertion or wild-type alleles (12 of 22 examined lines), even after 5-50 years of inbreeding (60-600 generations) and still maintained the insertional allele at between 6-95 % frequency (Fig. 1). Located in the chromosomal map 75E region, the Indy gene is far from any common natural chromosomal inversions [12]. Thus, heterozygosity for this natural Indy variant is not likely a result of genetic hitchhiking.


Indy gene variation in natural populations confers fitness advantage and life span extension through transposon insertion.

Zhu CT, Chang C, Reenan RA, Helfand SL - Aging (Albany NY) (2014)

World-wide heterozygosity of Hoppel insertion in IndyFrequency of Hoppel insertion in isofemale inbred lines. Each part of the pie chart represents a line from a different geographic origin. The colored area in each represents the frequency of Hoppel + allele in that line (Table S1).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3927810&req=5

Figure 1: World-wide heterozygosity of Hoppel insertion in IndyFrequency of Hoppel insertion in isofemale inbred lines. Each part of the pie chart represents a line from a different geographic origin. The colored area in each represents the frequency of Hoppel + allele in that line (Table S1).
Mentions: In the course of our molecular analyses of Indy gene structure in different Drosophila isolates from around the globe, we found a natural polymorphism present in numerous independent populations. This variant comprises the presence or absence of the transposable element, Hoppel, which has been implicated in regulating gene expression through effects on local chromatin structure [9, 10]. We sought to examine whether heterozygosity for the Hoppel insertion in Indy is maintained in other wild strains. Hoppel is an intronless, defective mobile element related to the P element, is about 1.2kb in average length, and is estimated to have 105 insertions in D. melanogaster euchromatin [11]. Using a PCR based screen, we found that the Hoppel insertion is polymorphic among 22 natural isolate lines (obtained from the Drosophila Species Stock Center, Table S1). Strikingly, many lines were not fixed for the insertion or wild-type alleles (12 of 22 examined lines), even after 5-50 years of inbreeding (60-600 generations) and still maintained the insertional allele at between 6-95 % frequency (Fig. 1). Located in the chromosomal map 75E region, the Indy gene is far from any common natural chromosomal inversions [12]. Thus, heterozygosity for this natural Indy variant is not likely a result of genetic hitchhiking.

Bottom Line: However, antagonism between life span and reproductive success frequently poses a dilemma pitting the cost of fecundity against longevity.The transposon insertion also regulates Indy expression level, which has experimentally been shown to affect life span and fecundity.Thus, in the wild, evolution reaffirms that the mechanism of heterozygote advantage has acted upon the Indy gene to assure increased reproductive fitness and, coincidentally, longer life span through regulatory transposon mutagenesis.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Cell Biology and Biochemistry, Division of Biology and Medicine, Brown University, Providence, RI 02912.

ABSTRACT
Natural selection acts to maximize reproductive fitness. However, antagonism between life span and reproductive success frequently poses a dilemma pitting the cost of fecundity against longevity. Here, we show that natural populations of Drosophila melanogaster harbor a Hoppel transposon insertion variant in the longevity gene Indy (I'm not dead yet), which confers both increased reproduction and longevity through metabolic changes. Heterozygosity for this natural long-lived variant has been maintained in isolates despite long-term inbreeding under laboratory conditions and advantageously confers increased fecundity. DNA sequences of variant chromosome isolates show evidence of selective sweep acting on the advantageous allele, suggesting that natural selection acts to maintain this variant. The transposon insertion also regulates Indy expression level, which has experimentally been shown to affect life span and fecundity. Thus, in the wild, evolution reaffirms that the mechanism of heterozygote advantage has acted upon the Indy gene to assure increased reproductive fitness and, coincidentally, longer life span through regulatory transposon mutagenesis.

Show MeSH
Related in: MedlinePlus