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P-element invasion fuels molecular adaptation in laboratory populations of Drosophila melanogaster.

ABSTRACT: Transposable elements (TEs) are mobile genetic parasites that frequently invade new host genomes through horizontal transfer. Invading TEs often exhibit a burst of transposition, followed by reduced transposition rates as repression evolves in the host. We recreated the horizontal transfer of P-element DNA transposons into a Drosophila melanogaster host and followed the expansion of TE copies and evolution of host repression in replicate laboratory populations reared at different temperatures. We observed that while populations maintained at high temperatures rapidly go extinct after TE invasion, those maintained at lower temperatures persist, allowing for TE spread and the evolution of host repression. We also surprisingly discovered that invaded populations experienced recurrent insertion of P-elements into a specific long non-coding RNA, lncRNA:CR43651, and that these insertion alleles are segregating at unusually high frequency in experimental populations, indicative of positive selection. We propose that, in addition to driving the evolution of repression, transpositional bursts of invading TEs can drive molecular adaptation.

SUBMITTER: Wang L

PROVIDER: S-EPMC10078945 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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P-element invasion fuels molecular adaptation in laboratory populations of Drosophila melanogaster.

Wang Luyang L Zhang Shuo S Hadjipanteli Savana S Saiz Lorissa L Nguyen Lisa L Silva Efren E Kelleher Erin E

Evolution; international journal of organic evolution 20230401 4

Transposable elements (TEs) are mobile genetic parasites that frequently invade new host genomes through horizontal transfer. Invading TEs often exhibit a burst of transposition, followed by reduced transposition rates as repression evolves in the host. We recreated the horizontal transfer of P-element DNA transposons into a Drosophila melanogaster host and followed the expansion of TE copies and evolution of host repression in replicate laboratory populations reared at different temperatures. W ...[more]

PMID: 36749648

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Project description:Changes in temperature disrupt the fluidity of cellular membranes, which can negatively impact membrane integrity and cellular processes. Many ectotherms, including Drosophila melanogaster (Meigen), adjust the glycerophospholipid composition of their membranes to restore optimal fluidity when temperatures change, a type of trait plasticity termed homeoviscous adaptation.Existing data suggest that plasticity in the relative abundances of the glycerophospholipids phosphatidylethanolamine (PE) and phosphatidylcholine (PC) underlies cellular adaptation to temporal variability in the thermal environment. For example, laboratory populations of D. melanogaster evolved in the presence of temporally variable temperatures have greater developmental plasticity of the ratio of PE to PC (PE/PC) and greater fecundity than do populations evolved at constant temperatures.Here, we extend this work to natural populations of D. melanogaster by evaluating thermal plasticity of glycerophospholipid composition at different life stages, in genotypes isolated from Vermont, Indiana and North Carolina, USA. We also quantify the covariance between developmental and adult (reversible) plasticity, and between adult responses of the membrane to cool and warm thermal shifts.As predicted by physiological models of homeoviscous adaptation, flies from all populations decrease PE/PC and the degree of lipid unsaturation in response to warm temperatures. Furthermore, these populations have diverged in their degree of membrane plasticity. Flies from the most variable thermal environment (Vermont, USA) decrease PE/PC to a greater extent than do other populations when developed at a warm temperature, a pattern that matches our previous observation in laboratory-evolved populations. We also find that developmental plasticity and adult plasticity of PE/PC covary across genotypes, but that adult responses to cool and warm thermal shifts do not.When combined with our previous observations of laboratory-evolved populations, our findings implicate developmental plasticity of PE/PC as a mechanism of thermal adaptation in temporally variable environments. While little is known about the genetic bases of plastic responses to temperature, our observations suggest that both environmentally sensitive and environmentally specific alleles contribute to thermal adaptation of membranes, and that costs of plasticity may arise when the adult environment differs from that experienced during development.

Dataset Information

P-element invasion fuels molecular adaptation in laboratory populations of Drosophila melanogaster.

Publications

P-element invasion fuels molecular adaptation in laboratory populations of Drosophila melanogaster.

Similar Datasets

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