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Inversions and adaptation to the plant toxin ouabain shape DNA sequence variation within and between chromosomal inversions of Drosophila subobscura.

Pegueroles C, Ferrés-Coy A, Martí-Solano M, Aquadro CF, Pascual M, Mestres F - Sci Rep (2016)

Bottom Line: Genetic differentiation was significant between inversions despite extensive recombination inside inverted regions, irrespective of gene distance to the inversion breakpoints.Surprisingly, the highest level of genetic differentiation between arrangements was found for the Atpα gene, which is located outside the O1 and O7 inversions.Similarities in the Atpα variants, conferring ouabain resistance in both arrangements, may be the result of convergent substitution and be favoured in response to selective pressures presumably related to the presence of plants containing ouabain in the geographic locations where both inversions are present.

View Article: PubMed Central - PubMed

Affiliation: Departament de Genètica and IRBio, Facultat de Biologia, Universitat de Barcelona, Barcelona 08028, Spain.

ABSTRACT
Adaptation is defined as an evolutionary process allowing organisms to succeed in certain habitats or conditions. Chromosomal inversions have the potential to be key in the adaptation processes, since they can contribute to the maintenance of favoured combinations of adaptive alleles through reduced recombination between individuals carrying different inversions. We have analysed six genes (Pif1A, Abi, Sqd, Yrt, Atpα and Fmr1), located inside and outside three inversions of the O chromosome in European populations of Drosophila subobscura. Genetic differentiation was significant between inversions despite extensive recombination inside inverted regions, irrespective of gene distance to the inversion breakpoints. Surprisingly, the highest level of genetic differentiation between arrangements was found for the Atpα gene, which is located outside the O1 and O7 inversions. Two derived unrelated arrangements (O3+4+1 and O3+4+7) are nearly fixed for several amino acid substitutions at the Atpα gene that have been described to confer resistance in other species to the cardenolide ouabain, a plant toxin capable of blocking ATPases. Similarities in the Atpα variants, conferring ouabain resistance in both arrangements, may be the result of convergent substitution and be favoured in response to selective pressures presumably related to the presence of plants containing ouabain in the geographic locations where both inversions are present.

No MeSH data available.


Related in: MedlinePlus

(A) Percentage of significant LD among O3+4, O3+4+1 and O3+4+7arrangements within and between genes. (B–D) Pairwise LD measured as R2 for O3+4+7–O3+4, O3+4+1–O3+4 and O3+4+1–O3+4+7 comparisons. Green dots correspond to the significant associations after adjusting for multiple comparisons using Benjamini and Hochberg method (1995). Gene order in O3+4 and O3+4+1 is the same (Fig. 1) and has been used for homogeneity in all comparisons.
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f3: (A) Percentage of significant LD among O3+4, O3+4+1 and O3+4+7arrangements within and between genes. (B–D) Pairwise LD measured as R2 for O3+4+7–O3+4, O3+4+1–O3+4 and O3+4+1–O3+4+7 comparisons. Green dots correspond to the significant associations after adjusting for multiple comparisons using Benjamini and Hochberg method (1995). Gene order in O3+4 and O3+4+1 is the same (Fig. 1) and has been used for homogeneity in all comparisons.

Mentions: If chromosomal inversions are effectively reducing recombination levels, we would expect higher levels of LD within and between genes located inside them. However, levels of LD in these genes were very low and only a strong LD was observed within the Atpα gene (Fig. 3A). Significant associations after adjusting for multiple testing (in green) were obtained only within genes and never between genes regardless of their location in relation to the inversions (Fig. 3B–D). The highest ZnS values were obtained for the Atpα gene with 0.34 and 0.26 when analyzing together inversions O3+4–O3+4+1 and O3+4–O3+4+7, respectively (Table S1). Surprisingly, ZnS values were in general higher for O3+4+1 and O3+4+7 sequences alone, than compared to the O3+4 arrangement, suggesting the presence of recombination events between arrangements.


Inversions and adaptation to the plant toxin ouabain shape DNA sequence variation within and between chromosomal inversions of Drosophila subobscura.

Pegueroles C, Ferrés-Coy A, Martí-Solano M, Aquadro CF, Pascual M, Mestres F - Sci Rep (2016)

(A) Percentage of significant LD among O3+4, O3+4+1 and O3+4+7arrangements within and between genes. (B–D) Pairwise LD measured as R2 for O3+4+7–O3+4, O3+4+1–O3+4 and O3+4+1–O3+4+7 comparisons. Green dots correspond to the significant associations after adjusting for multiple comparisons using Benjamini and Hochberg method (1995). Gene order in O3+4 and O3+4+1 is the same (Fig. 1) and has been used for homogeneity in all comparisons.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4815013&req=5

f3: (A) Percentage of significant LD among O3+4, O3+4+1 and O3+4+7arrangements within and between genes. (B–D) Pairwise LD measured as R2 for O3+4+7–O3+4, O3+4+1–O3+4 and O3+4+1–O3+4+7 comparisons. Green dots correspond to the significant associations after adjusting for multiple comparisons using Benjamini and Hochberg method (1995). Gene order in O3+4 and O3+4+1 is the same (Fig. 1) and has been used for homogeneity in all comparisons.
Mentions: If chromosomal inversions are effectively reducing recombination levels, we would expect higher levels of LD within and between genes located inside them. However, levels of LD in these genes were very low and only a strong LD was observed within the Atpα gene (Fig. 3A). Significant associations after adjusting for multiple testing (in green) were obtained only within genes and never between genes regardless of their location in relation to the inversions (Fig. 3B–D). The highest ZnS values were obtained for the Atpα gene with 0.34 and 0.26 when analyzing together inversions O3+4–O3+4+1 and O3+4–O3+4+7, respectively (Table S1). Surprisingly, ZnS values were in general higher for O3+4+1 and O3+4+7 sequences alone, than compared to the O3+4 arrangement, suggesting the presence of recombination events between arrangements.

Bottom Line: Genetic differentiation was significant between inversions despite extensive recombination inside inverted regions, irrespective of gene distance to the inversion breakpoints.Surprisingly, the highest level of genetic differentiation between arrangements was found for the Atpα gene, which is located outside the O1 and O7 inversions.Similarities in the Atpα variants, conferring ouabain resistance in both arrangements, may be the result of convergent substitution and be favoured in response to selective pressures presumably related to the presence of plants containing ouabain in the geographic locations where both inversions are present.

View Article: PubMed Central - PubMed

Affiliation: Departament de Genètica and IRBio, Facultat de Biologia, Universitat de Barcelona, Barcelona 08028, Spain.

ABSTRACT
Adaptation is defined as an evolutionary process allowing organisms to succeed in certain habitats or conditions. Chromosomal inversions have the potential to be key in the adaptation processes, since they can contribute to the maintenance of favoured combinations of adaptive alleles through reduced recombination between individuals carrying different inversions. We have analysed six genes (Pif1A, Abi, Sqd, Yrt, Atpα and Fmr1), located inside and outside three inversions of the O chromosome in European populations of Drosophila subobscura. Genetic differentiation was significant between inversions despite extensive recombination inside inverted regions, irrespective of gene distance to the inversion breakpoints. Surprisingly, the highest level of genetic differentiation between arrangements was found for the Atpα gene, which is located outside the O1 and O7 inversions. Two derived unrelated arrangements (O3+4+1 and O3+4+7) are nearly fixed for several amino acid substitutions at the Atpα gene that have been described to confer resistance in other species to the cardenolide ouabain, a plant toxin capable of blocking ATPases. Similarities in the Atpα variants, conferring ouabain resistance in both arrangements, may be the result of convergent substitution and be favoured in response to selective pressures presumably related to the presence of plants containing ouabain in the geographic locations where both inversions are present.

No MeSH data available.


Related in: MedlinePlus