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Abstract Numerous studies have revealed a signature of strong adaptive evolution in the piwi-interacting RNA (piRNA) machinery of Drosophila melanogaster, but the cause of this pattern is not understood. Several hypotheses have been proposed. One hypothesis is that transposable element (TE) families and the piRNA machinery are co-evolving under an evolutionary arms race, perhaps due to antagonism by TEs against the piRNA machinery. A related, though not co-evolutionary, hypothesis is that recurrent TE invasion drives the piRNA machinery to adapt to novel TE strategies. A third hypothesis is that ongoing fluctuation in TE abundance leads to adaptation in the piRNA machinery that must constantly adjust between sensitivity for detecting new elements and specificity to avoid the cost of off-target gene silencing. Rapid evolution of the piRNA machinery may also be driven independently of TEs, and instead from other functions such as the role of piRNAs in suppressing sex-chromosome meiotic drive. We sought to evaluate the impact of TE abundance on adaptive evolution of the piRNA machinery in D. melanogaster and 2 species with higher repeat content—Drosophila ananassae and Drosophila willistoni. This comparison was achieved by employing a likelihood-based hypothesis testing framework based on the McDonald–Kreitman test. We show that we can reject a faster rate of adaptive evolution in the piRNA machinery of these 2 species. We propose that the high rate of adaptation in D. melanogaster is either driven by a recent influx of TEs that have occurred during range expansion or selection on other functions of the piRNA machinery.
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Spoink, a LTR retrotransposon, invaded D. melanogaster populations in the 1990s
During the last few centuriesD. melanogasterpopulations were invaded by several transposable elements, the most recent of which was thought to be theP-element between 1950 and 1980. Here we describe a novel TE, which we namedSpoink, that has invadedD. melanogaster. It is a 5216nt LTR retrotransposon of the Ty3/gypsy superfamily. Relying on strains sampled at different times during the last century we show thatSpoinkinvaded worldwideD. melanogasterpopulations after theP-element between 1983 and 1993. This invasion was likely triggered by a horizontal transfer from theD. willistonigroup, much as theP-element.Spoinkis probably silenced by the piRNA pathway in natural populations and about 1/3 of the examined strains have an insertion into a canonical piRNA cluster such as42AB. Given the degree of genetic investigation ofD. melanogasterit is perhaps surprising thatSpoinkwas able to invade unnoticed.
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- Award ID(s):
- 2032756
- PAR ID:
- 10574675
- Editor(s):
- Feschotte, Cédric
- Publisher / Repository:
- PLoS Genetics
- Date Published:
- Journal Name:
- PLOS Genetics
- Volume:
- 20
- Issue:
- 3
- ISSN:
- 1553-7404
- Page Range / eLocation ID:
- e1011201
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pgen.1011201
