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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.

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Related in: MedlinePlus

Hoppel insertion in Indy is associated with a reproductive advantageAccumulative number of eggs laid per female for each of the three Hoppel genotypes representing genomes with either no copies of Hoppel in Indy (−/−; in black), one copy of Hoppel in Indy (+/−; in red) or two copies of Hoppel in Indy (+/+; in green), isolated from three different populations collected from distant places or times from the wild (Oahu, Hawaii 1955, Captain Cook, Hawaii 2007 and Hidalgo, Mexico 2005).
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Figure 2: Hoppel insertion in Indy is associated with a reproductive advantageAccumulative number of eggs laid per female for each of the three Hoppel genotypes representing genomes with either no copies of Hoppel in Indy (−/−; in black), one copy of Hoppel in Indy (+/−; in red) or two copies of Hoppel in Indy (+/+; in green), isolated from three different populations collected from distant places or times from the wild (Oahu, Hawaii 1955, Captain Cook, Hawaii 2007 and Hidalgo, Mexico 2005).

Mentions: Heterozygosity for P{lacW} transgene insertion at the Indy locus has been shown to result in life span extension without a decrement in fecundity under normal laboratory culture conditions, but with a distinct cost under reduced caloric intake [13]. We isolated Hoppel insertion homozygotes (referred to as +/+) and non-insertion homozygotes (referred to as −/−) from three natural lines which demonstrated heterozygosity: Oahu, Hawaii collected in 1955; Captain Cook, Hawaii collected in 2007; and Hidalgo, Mexico collected in 2005. Congenic heterozygotes (−/+) were produced by intercrossing these homozygous genotypes isolated from each natural line (Fig. S1). To examine effects on reproductive fitness, we determined the fecundity of heterozygotes and homozygotes. In all cases, we found that a single copy of the Indy Hoppel insertion conferred highest fecundity (Fig. 2). The strong selection for maximized fecundity in wild populations favors the preservation of the insertion allele, conferring a large benefit (~10% increased egg production) on heterozygotes over the first 15 days of reproduction. Thus, we suggest that the Indy gene has been the subject of selection by the process of heterosis, or heterozygote advantage.


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)

Hoppel insertion in Indy is associated with a reproductive advantageAccumulative number of eggs laid per female for each of the three Hoppel genotypes representing genomes with either no copies of Hoppel in Indy (−/−; in black), one copy of Hoppel in Indy (+/−; in red) or two copies of Hoppel in Indy (+/+; in green), isolated from three different populations collected from distant places or times from the wild (Oahu, Hawaii 1955, Captain Cook, Hawaii 2007 and Hidalgo, Mexico 2005).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Hoppel insertion in Indy is associated with a reproductive advantageAccumulative number of eggs laid per female for each of the three Hoppel genotypes representing genomes with either no copies of Hoppel in Indy (−/−; in black), one copy of Hoppel in Indy (+/−; in red) or two copies of Hoppel in Indy (+/+; in green), isolated from three different populations collected from distant places or times from the wild (Oahu, Hawaii 1955, Captain Cook, Hawaii 2007 and Hidalgo, Mexico 2005).
Mentions: Heterozygosity for P{lacW} transgene insertion at the Indy locus has been shown to result in life span extension without a decrement in fecundity under normal laboratory culture conditions, but with a distinct cost under reduced caloric intake [13]. We isolated Hoppel insertion homozygotes (referred to as +/+) and non-insertion homozygotes (referred to as −/−) from three natural lines which demonstrated heterozygosity: Oahu, Hawaii collected in 1955; Captain Cook, Hawaii collected in 2007; and Hidalgo, Mexico collected in 2005. Congenic heterozygotes (−/+) were produced by intercrossing these homozygous genotypes isolated from each natural line (Fig. S1). To examine effects on reproductive fitness, we determined the fecundity of heterozygotes and homozygotes. In all cases, we found that a single copy of the Indy Hoppel insertion conferred highest fecundity (Fig. 2). The strong selection for maximized fecundity in wild populations favors the preservation of the insertion allele, conferring a large benefit (~10% increased egg production) on heterozygotes over the first 15 days of reproduction. Thus, we suggest that the Indy gene has been the subject of selection by the process of heterosis, or heterozygote advantage.

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