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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

Genetic diversity (π) for the O3+4, O3+4+1 and O3+4+7 chromosomal arrangements using the concatenated genes data set.Grey boxes and solid lines underneath mark exonic and intronic regions, respectively.
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f2: Genetic diversity (π) for the O3+4, O3+4+1 and O3+4+7 chromosomal arrangements using the concatenated genes data set.Grey boxes and solid lines underneath mark exonic and intronic regions, respectively.

Mentions: To characterize the genetic content of the O3+4+1 and the O3+4+7 arrangements, we first calculated nucleotide variation and divergence for each of the six gene fragments studied (Table 1). Sequences for O3+4 individuals are from Pegueroles et al.11 and diversity estimates are reported herein to facilitate comparison. The number of haplotypes was approximately the same as the number of analysed lines, except for Sqd and Atpα genes in O3+4+1 arrangement that had lower numbers of haplotypes (Table 1). Considering the variability of the O3+4 arrangement as a baseline, we observed a decrease in variability in the intronic regions of Sqd and Atpα genes at both inverted arrangements (Fig. 2). In contrast, we observed increased variability in the first exonic region of Atpα gene for the O3+4+7 arrangement. Diversity levels were highly variable between genes (Table 1, Fig. 2). The intronic regions of the Pif1A gene showed the highest diversity (π) for all three arrangements despite being located within the O7 inversion. The Yrt gene also showed high π levels despite most of the amplified fragment being exonic and located close to the O1 breakpoint and outside the inversion. Since the proportion of intronic-exonic regions amplified varied among genes, genetic variability was also estimated in silent positions exclusively (i.e., both synonymous and non-coding sites) to avoid biases in diversity estimates (Table 1). In agreement with π results, silent nucleotide variability (πsil) remained highly variable among genes, but quite similar when comparing the two inverted arrangements. No relationship was detected between π and distance to breakpoints, since Pearson correlation values were negative and non-significant for all 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)

Genetic diversity (π) for the O3+4, O3+4+1 and O3+4+7 chromosomal arrangements using the concatenated genes data set.Grey boxes and solid lines underneath mark exonic and intronic regions, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Genetic diversity (π) for the O3+4, O3+4+1 and O3+4+7 chromosomal arrangements using the concatenated genes data set.Grey boxes and solid lines underneath mark exonic and intronic regions, respectively.
Mentions: To characterize the genetic content of the O3+4+1 and the O3+4+7 arrangements, we first calculated nucleotide variation and divergence for each of the six gene fragments studied (Table 1). Sequences for O3+4 individuals are from Pegueroles et al.11 and diversity estimates are reported herein to facilitate comparison. The number of haplotypes was approximately the same as the number of analysed lines, except for Sqd and Atpα genes in O3+4+1 arrangement that had lower numbers of haplotypes (Table 1). Considering the variability of the O3+4 arrangement as a baseline, we observed a decrease in variability in the intronic regions of Sqd and Atpα genes at both inverted arrangements (Fig. 2). In contrast, we observed increased variability in the first exonic region of Atpα gene for the O3+4+7 arrangement. Diversity levels were highly variable between genes (Table 1, Fig. 2). The intronic regions of the Pif1A gene showed the highest diversity (π) for all three arrangements despite being located within the O7 inversion. The Yrt gene also showed high π levels despite most of the amplified fragment being exonic and located close to the O1 breakpoint and outside the inversion. Since the proportion of intronic-exonic regions amplified varied among genes, genetic variability was also estimated in silent positions exclusively (i.e., both synonymous and non-coding sites) to avoid biases in diversity estimates (Table 1). In agreement with π results, silent nucleotide variability (πsil) remained highly variable among genes, but quite similar when comparing the two inverted arrangements. No relationship was detected between π and distance to breakpoints, since Pearson correlation values were negative and non-significant for all 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