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Contrasting patterns of selective constraints in nuclear-encoded genes of the oxidative phosphorylation pathway in holometabolous insects and their possible role in hybrid breakdown in Nasonia.

Gibson JD, Niehuis O, Verrelli BC, Gadau J - Heredity (Edinb) (2010)

Bottom Line: Mitochondrial genes accumulate substitutions more quickly than nuclear genes, yet the impact of selection on mitochondrial genes is significantly reduced relative to nuclear genes because of the non-recombining nature of the mitochondrial genome and its predicted smaller effective population size.Although nuclear OXPHOS genes are typically highly conserved, we found significant evidence for elevated amino acid divergence in 4 of the 59 studied nuclear-encoded OXPHOS genes.We also found that three of these four genes, as well as six other OXPHOS genes, contain amino acid substitutions between Nasonia species at evolutionarily constrained sites.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA. jdgibson@asu.edu

ABSTRACT
The principal energy generating system in animals is the oxidative phosphorylation (OXPHOS) pathway, which depends on the tight interaction of nuclear- and mitochondrial-encoded genes to function properly. Mitochondrial genes accumulate substitutions more quickly than nuclear genes, yet the impact of selection on mitochondrial genes is significantly reduced relative to nuclear genes because of the non-recombining nature of the mitochondrial genome and its predicted smaller effective population size. It has therefore been hypothesized that the nuclear-encoded genes of the OXPHOS pathway are under strong selective pressure to compensate for the accumulation of deleterious nucleotide substitutions in mitochondrial-encoded OXPHOS genes, a process known as compensatory co-adaptation. We evaluated this hypothesis by analyzing nuclear-encoded OXPHOS genes for signatures of positive selection as well as evolutionary constraints at amino acid sites. We considered OXPHOS genes of six holometabolous insects and their orthologs from three Nasonia parasitoid wasps, the hybrids of which suffer from an increased mortality rate caused by cytonuclear genic incompatibilities. Although nuclear OXPHOS genes are typically highly conserved, we found significant evidence for elevated amino acid divergence in 4 of the 59 studied nuclear-encoded OXPHOS genes. We also found that three of these four genes, as well as six other OXPHOS genes, contain amino acid substitutions between Nasonia species at evolutionarily constrained sites. It is possible that these genes account for the reported incompatibility in Nasonia hybrids and their characterization may lead to a better understanding of the role of positive selection in the genetics of speciation.

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Co-localization of OXPHOS genes and cytonuclear incompatibility loci within NasoniaNasonia linkage map adapted from Niehuis et al. (2009). The leftmost scale shows the genetic distance in centimorgans. The horizontal bars in each chromosome (1.01-5.51) represent groups of markers showing no recombination between them, while the space between bars represents recombination. Dark gradient bars to the right of the chromosomes represent incompatibility loci identified by Niehuis et al. (2008); question marks designate locus boundaries that are unclear due to recent expansions of the ends of the linkage groups on the linkage map. The columns to the right of the chromosomes designate the complex (I-V) of each OXPHOS gene.Empty arrows = genes with amino acid substitutions with non-significant impact scores.Filled arrows = genes with amino acid substitutions predicted to significantly disrupt protein structure in Nasonia.stars = genes containing sites that show the signature of positive selection (ω > 1).
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Figure 1: Co-localization of OXPHOS genes and cytonuclear incompatibility loci within NasoniaNasonia linkage map adapted from Niehuis et al. (2009). The leftmost scale shows the genetic distance in centimorgans. The horizontal bars in each chromosome (1.01-5.51) represent groups of markers showing no recombination between them, while the space between bars represents recombination. Dark gradient bars to the right of the chromosomes represent incompatibility loci identified by Niehuis et al. (2008); question marks designate locus boundaries that are unclear due to recent expansions of the ends of the linkage groups on the linkage map. The columns to the right of the chromosomes designate the complex (I-V) of each OXPHOS gene.Empty arrows = genes with amino acid substitutions with non-significant impact scores.Filled arrows = genes with amino acid substitutions predicted to significantly disrupt protein structure in Nasonia.stars = genes containing sites that show the signature of positive selection (ω > 1).

Mentions: We identified 59 of the 65 OXPHOS pathway subunit genes known from Drosophila (MitoDrome database; D'Elia et al., 2006) in the Nasonia genome (Table 1; Supp. I). It is possible that the remaining genes were not identified because our conservative search strategy parameters did not allow us to reliably identify orthologs that have rapidly diverged. For 9 of the 59 genes (i.e., two of complex I, two of complex III, and five of complex IV), EST data suggested alternate transcripts (Table 1; Supp. I, Werren et al., in press). Utilizing the high-density linkage map for Nasonia (Niehuis et al., 2009), we were able to map 56 of the 59 identified nuclear-encoded OXPHOS genes in the Nasonia genome (Fig. 1, Supp. I).


Contrasting patterns of selective constraints in nuclear-encoded genes of the oxidative phosphorylation pathway in holometabolous insects and their possible role in hybrid breakdown in Nasonia.

Gibson JD, Niehuis O, Verrelli BC, Gadau J - Heredity (Edinb) (2010)

Co-localization of OXPHOS genes and cytonuclear incompatibility loci within NasoniaNasonia linkage map adapted from Niehuis et al. (2009). The leftmost scale shows the genetic distance in centimorgans. The horizontal bars in each chromosome (1.01-5.51) represent groups of markers showing no recombination between them, while the space between bars represents recombination. Dark gradient bars to the right of the chromosomes represent incompatibility loci identified by Niehuis et al. (2008); question marks designate locus boundaries that are unclear due to recent expansions of the ends of the linkage groups on the linkage map. The columns to the right of the chromosomes designate the complex (I-V) of each OXPHOS gene.Empty arrows = genes with amino acid substitutions with non-significant impact scores.Filled arrows = genes with amino acid substitutions predicted to significantly disrupt protein structure in Nasonia.stars = genes containing sites that show the signature of positive selection (ω > 1).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2823824&req=5

Figure 1: Co-localization of OXPHOS genes and cytonuclear incompatibility loci within NasoniaNasonia linkage map adapted from Niehuis et al. (2009). The leftmost scale shows the genetic distance in centimorgans. The horizontal bars in each chromosome (1.01-5.51) represent groups of markers showing no recombination between them, while the space between bars represents recombination. Dark gradient bars to the right of the chromosomes represent incompatibility loci identified by Niehuis et al. (2008); question marks designate locus boundaries that are unclear due to recent expansions of the ends of the linkage groups on the linkage map. The columns to the right of the chromosomes designate the complex (I-V) of each OXPHOS gene.Empty arrows = genes with amino acid substitutions with non-significant impact scores.Filled arrows = genes with amino acid substitutions predicted to significantly disrupt protein structure in Nasonia.stars = genes containing sites that show the signature of positive selection (ω > 1).
Mentions: We identified 59 of the 65 OXPHOS pathway subunit genes known from Drosophila (MitoDrome database; D'Elia et al., 2006) in the Nasonia genome (Table 1; Supp. I). It is possible that the remaining genes were not identified because our conservative search strategy parameters did not allow us to reliably identify orthologs that have rapidly diverged. For 9 of the 59 genes (i.e., two of complex I, two of complex III, and five of complex IV), EST data suggested alternate transcripts (Table 1; Supp. I, Werren et al., in press). Utilizing the high-density linkage map for Nasonia (Niehuis et al., 2009), we were able to map 56 of the 59 identified nuclear-encoded OXPHOS genes in the Nasonia genome (Fig. 1, Supp. I).

Bottom Line: Mitochondrial genes accumulate substitutions more quickly than nuclear genes, yet the impact of selection on mitochondrial genes is significantly reduced relative to nuclear genes because of the non-recombining nature of the mitochondrial genome and its predicted smaller effective population size.Although nuclear OXPHOS genes are typically highly conserved, we found significant evidence for elevated amino acid divergence in 4 of the 59 studied nuclear-encoded OXPHOS genes.We also found that three of these four genes, as well as six other OXPHOS genes, contain amino acid substitutions between Nasonia species at evolutionarily constrained sites.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA. jdgibson@asu.edu

ABSTRACT
The principal energy generating system in animals is the oxidative phosphorylation (OXPHOS) pathway, which depends on the tight interaction of nuclear- and mitochondrial-encoded genes to function properly. Mitochondrial genes accumulate substitutions more quickly than nuclear genes, yet the impact of selection on mitochondrial genes is significantly reduced relative to nuclear genes because of the non-recombining nature of the mitochondrial genome and its predicted smaller effective population size. It has therefore been hypothesized that the nuclear-encoded genes of the OXPHOS pathway are under strong selective pressure to compensate for the accumulation of deleterious nucleotide substitutions in mitochondrial-encoded OXPHOS genes, a process known as compensatory co-adaptation. We evaluated this hypothesis by analyzing nuclear-encoded OXPHOS genes for signatures of positive selection as well as evolutionary constraints at amino acid sites. We considered OXPHOS genes of six holometabolous insects and their orthologs from three Nasonia parasitoid wasps, the hybrids of which suffer from an increased mortality rate caused by cytonuclear genic incompatibilities. Although nuclear OXPHOS genes are typically highly conserved, we found significant evidence for elevated amino acid divergence in 4 of the 59 studied nuclear-encoded OXPHOS genes. We also found that three of these four genes, as well as six other OXPHOS genes, contain amino acid substitutions between Nasonia species at evolutionarily constrained sites. It is possible that these genes account for the reported incompatibility in Nasonia hybrids and their characterization may lead to a better understanding of the role of positive selection in the genetics of speciation.

Show MeSH