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Adaptive evolution and functional redesign of core metabolic proteins in snakes.

Castoe TA, Jiang ZJ, Gu W, Wang ZO, Pollock DD - PLoS ONE (2008)

Bottom Line: The evolutionary redesign of snake COI coincided with adaptive bursts in other mitochondrial proteins and substantial changes in mitochondrial genome structure.It also generally coincided with or preceded major shifts in ecological niche and the evolution of extensive physiological adaptations related to lung reduction, large prey consumption, and venom evolution.The parallel timing of these major evolutionary events suggests that evolutionary redesign of metabolic and mitochondrial function may be related to, or underlie, the extreme changes in physiological and metabolic efficiency, flexibility, and innovation observed in snake evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, Colorado, United States of America.

ABSTRACT

Background: Adaptive evolutionary episodes in core metabolic proteins are uncommon, and are even more rarely linked to major macroevolutionary shifts.

Methodology/principal findings: We conducted extensive molecular evolutionary analyses on snake mitochondrial proteins and discovered multiple lines of evidence suggesting that the proteins at the core of aerobic metabolism in snakes have undergone remarkably large episodic bursts of adaptive change. We show that snake mitochondrial proteins experienced unprecedented levels of positive selection, coevolution, convergence, and reversion at functionally critical residues. We examined Cytochrome C oxidase subunit I (COI) in detail, and show that it experienced extensive modification of normally conserved residues involved in proton transport and delivery of electrons and oxygen. Thus, adaptive changes likely altered the flow of protons and other aspects of function in CO, thereby influencing fundamental characteristics of aerobic metabolism. We refer to these processes as "evolutionary redesign" because of the magnitude of the episodic bursts and the degree to which they affected core functional residues.

Conclusions/significance: The evolutionary redesign of snake COI coincided with adaptive bursts in other mitochondrial proteins and substantial changes in mitochondrial genome structure. It also generally coincided with or preceded major shifts in ecological niche and the evolution of extensive physiological adaptations related to lung reduction, large prey consumption, and venom evolution. The parallel timing of these major evolutionary events suggests that evolutionary redesign of metabolic and mitochondrial function may be related to, or underlie, the extreme changes in physiological and metabolic efficiency, flexibility, and innovation observed in snake evolution.

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Mitochondrial proteins have experienced extraordinarily elevated rates of amino acid replacement early in the evolution of snakes.The conservative transversion-based approximations of the relative rates of non-synonymous to synonymous substitution (dNTV12 / dSTV4x) rates are shown as open or colored circles for each branch of the phylogenetic tree; linear regression lines (excluding points in the red ellipse) are shown in black (A and B). The calculations shown are from (A) all mitochondrial proteins and (B) cytochrome C oxidase subunit 1 (COI). Blue-shaded areas of A and B indicate very long branches with high dSTV4x values where the (dNTV12 / dSTV4x) estimate may be inaccurate, possibly due to dSTV4x saturation and underestimation. Note that early snake branches have very high dNTV12, far greater than branches of comparable length (dSTV4x). This is strong evidence for extraordinarily accelerated rates of amino acid replacement early in snake evolution. The phylogenetic tree of relationships among species in our comparative dataset is shown in (C). Branches with extremely high values of dNTV12 / dSTV4X for COI are indicated with colored lines (black, blue, red) following the key in the bottom left. The circles for branches in (A) and (B) were colored according to the same legend for ratios of COI (dNTV12 / dSTV4x).
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pone-0002201-g001: Mitochondrial proteins have experienced extraordinarily elevated rates of amino acid replacement early in the evolution of snakes.The conservative transversion-based approximations of the relative rates of non-synonymous to synonymous substitution (dNTV12 / dSTV4x) rates are shown as open or colored circles for each branch of the phylogenetic tree; linear regression lines (excluding points in the red ellipse) are shown in black (A and B). The calculations shown are from (A) all mitochondrial proteins and (B) cytochrome C oxidase subunit 1 (COI). Blue-shaded areas of A and B indicate very long branches with high dSTV4x values where the (dNTV12 / dSTV4x) estimate may be inaccurate, possibly due to dSTV4x saturation and underestimation. Note that early snake branches have very high dNTV12, far greater than branches of comparable length (dSTV4x). This is strong evidence for extraordinarily accelerated rates of amino acid replacement early in snake evolution. The phylogenetic tree of relationships among species in our comparative dataset is shown in (C). Branches with extremely high values of dNTV12 / dSTV4X for COI are indicated with colored lines (black, blue, red) following the key in the bottom left. The circles for branches in (A) and (B) were colored according to the same legend for ratios of COI (dNTV12 / dSTV4x).

Mentions: To estimate a transversion-based dN/dS estimate, the synonymous transversion rate was averaged over all 3rd codon positions in the mtDNA with conserved four-fold redundancy (dSTV4X; Figure S9), while the non-synonymous transversion rate was measured at first and second codon positions (dNTV12) for each gene under consideration. Non-synonymous transversions at first and second codon positions result primarily in amino acid replacements with radical physico-chemical differences and major functional effects, but there is a strong correlation between dNTV12 and overall amino acid replacement rates (r2 = 0.95; p<<0.001; Figure S10). The dNTV12/dSTV4X ratios strongly support the finding that mitochondrial proteins endured massive bursts of amino acid replacement early in snake evolution compared to other tetrapod lineages (Figure 1). For all mitochondrial proteins combined, dNTV12 values at the base of snake origins were about 3-fold greater than expected compared to other tetrapod lineages (Figure 1A), and were most accelerated in COI (Figures 1B–C). For example, along the branch leading to the Alethinophidia, COI experienced 10-fold more dNTV12 (and thus radical amino acid substitutions) than expected (Figures 1B–1C). As before, high ratios are not maintained in descendant snake lineages (see also Figure S11), indicating that strong purifying selection subsequently dominated snake mitochondrial evolution (Figure 1).


Adaptive evolution and functional redesign of core metabolic proteins in snakes.

Castoe TA, Jiang ZJ, Gu W, Wang ZO, Pollock DD - PLoS ONE (2008)

Mitochondrial proteins have experienced extraordinarily elevated rates of amino acid replacement early in the evolution of snakes.The conservative transversion-based approximations of the relative rates of non-synonymous to synonymous substitution (dNTV12 / dSTV4x) rates are shown as open or colored circles for each branch of the phylogenetic tree; linear regression lines (excluding points in the red ellipse) are shown in black (A and B). The calculations shown are from (A) all mitochondrial proteins and (B) cytochrome C oxidase subunit 1 (COI). Blue-shaded areas of A and B indicate very long branches with high dSTV4x values where the (dNTV12 / dSTV4x) estimate may be inaccurate, possibly due to dSTV4x saturation and underestimation. Note that early snake branches have very high dNTV12, far greater than branches of comparable length (dSTV4x). This is strong evidence for extraordinarily accelerated rates of amino acid replacement early in snake evolution. The phylogenetic tree of relationships among species in our comparative dataset is shown in (C). Branches with extremely high values of dNTV12 / dSTV4X for COI are indicated with colored lines (black, blue, red) following the key in the bottom left. The circles for branches in (A) and (B) were colored according to the same legend for ratios of COI (dNTV12 / dSTV4x).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2376058&req=5

pone-0002201-g001: Mitochondrial proteins have experienced extraordinarily elevated rates of amino acid replacement early in the evolution of snakes.The conservative transversion-based approximations of the relative rates of non-synonymous to synonymous substitution (dNTV12 / dSTV4x) rates are shown as open or colored circles for each branch of the phylogenetic tree; linear regression lines (excluding points in the red ellipse) are shown in black (A and B). The calculations shown are from (A) all mitochondrial proteins and (B) cytochrome C oxidase subunit 1 (COI). Blue-shaded areas of A and B indicate very long branches with high dSTV4x values where the (dNTV12 / dSTV4x) estimate may be inaccurate, possibly due to dSTV4x saturation and underestimation. Note that early snake branches have very high dNTV12, far greater than branches of comparable length (dSTV4x). This is strong evidence for extraordinarily accelerated rates of amino acid replacement early in snake evolution. The phylogenetic tree of relationships among species in our comparative dataset is shown in (C). Branches with extremely high values of dNTV12 / dSTV4X for COI are indicated with colored lines (black, blue, red) following the key in the bottom left. The circles for branches in (A) and (B) were colored according to the same legend for ratios of COI (dNTV12 / dSTV4x).
Mentions: To estimate a transversion-based dN/dS estimate, the synonymous transversion rate was averaged over all 3rd codon positions in the mtDNA with conserved four-fold redundancy (dSTV4X; Figure S9), while the non-synonymous transversion rate was measured at first and second codon positions (dNTV12) for each gene under consideration. Non-synonymous transversions at first and second codon positions result primarily in amino acid replacements with radical physico-chemical differences and major functional effects, but there is a strong correlation between dNTV12 and overall amino acid replacement rates (r2 = 0.95; p<<0.001; Figure S10). The dNTV12/dSTV4X ratios strongly support the finding that mitochondrial proteins endured massive bursts of amino acid replacement early in snake evolution compared to other tetrapod lineages (Figure 1). For all mitochondrial proteins combined, dNTV12 values at the base of snake origins were about 3-fold greater than expected compared to other tetrapod lineages (Figure 1A), and were most accelerated in COI (Figures 1B–C). For example, along the branch leading to the Alethinophidia, COI experienced 10-fold more dNTV12 (and thus radical amino acid substitutions) than expected (Figures 1B–1C). As before, high ratios are not maintained in descendant snake lineages (see also Figure S11), indicating that strong purifying selection subsequently dominated snake mitochondrial evolution (Figure 1).

Bottom Line: The evolutionary redesign of snake COI coincided with adaptive bursts in other mitochondrial proteins and substantial changes in mitochondrial genome structure.It also generally coincided with or preceded major shifts in ecological niche and the evolution of extensive physiological adaptations related to lung reduction, large prey consumption, and venom evolution.The parallel timing of these major evolutionary events suggests that evolutionary redesign of metabolic and mitochondrial function may be related to, or underlie, the extreme changes in physiological and metabolic efficiency, flexibility, and innovation observed in snake evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, Colorado, United States of America.

ABSTRACT

Background: Adaptive evolutionary episodes in core metabolic proteins are uncommon, and are even more rarely linked to major macroevolutionary shifts.

Methodology/principal findings: We conducted extensive molecular evolutionary analyses on snake mitochondrial proteins and discovered multiple lines of evidence suggesting that the proteins at the core of aerobic metabolism in snakes have undergone remarkably large episodic bursts of adaptive change. We show that snake mitochondrial proteins experienced unprecedented levels of positive selection, coevolution, convergence, and reversion at functionally critical residues. We examined Cytochrome C oxidase subunit I (COI) in detail, and show that it experienced extensive modification of normally conserved residues involved in proton transport and delivery of electrons and oxygen. Thus, adaptive changes likely altered the flow of protons and other aspects of function in CO, thereby influencing fundamental characteristics of aerobic metabolism. We refer to these processes as "evolutionary redesign" because of the magnitude of the episodic bursts and the degree to which they affected core functional residues.

Conclusions/significance: The evolutionary redesign of snake COI coincided with adaptive bursts in other mitochondrial proteins and substantial changes in mitochondrial genome structure. It also generally coincided with or preceded major shifts in ecological niche and the evolution of extensive physiological adaptations related to lung reduction, large prey consumption, and venom evolution. The parallel timing of these major evolutionary events suggests that evolutionary redesign of metabolic and mitochondrial function may be related to, or underlie, the extreme changes in physiological and metabolic efficiency, flexibility, and innovation observed in snake evolution.

Show MeSH
Related in: MedlinePlus