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First published online June 11, 2007
Journal of Experimental Biology 210, 2170-2180 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.004861

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Exceptional longevity in songbirds is associated with high rates of evolution of cytochrome b, suggesting selection for reduced generation of free radicals

Hagai Rottenberg

New Hope Biomedical R&D, 23 W. Bridge Street, New Hope, PA 18938, USA

View larger version (17K): [in this window] [in a new window]   Fig. 1. The rate of cytochrome b evolution (Scytb) modulates the relationships between body mass (M), basal metabolic rate (BMR), mass-specific basal metabolic rate (BMRw) and longevity (L) in Neognathae birds. Data are from Table S2 in supplementary material. Linear regressions of the power laws for the 59 genera of Neognathae birds for which there are complete cytochrome b sequences available, and the M, L and BMRw values, are shown by solid lines. Linear regressions of the genera with the lowest values of Scytb (the lower quadrant of the rate distribution, Scytb<0.069, N=15, full symbols) are shown by dotted lines. The linear regressions of the genera with the highest values of Scytb (the upper quadrant of the rate distribution, Scytb>0.1345, N=15, empty symbols) are shown by dash–dot–dash lines. When the regression was not significant (P>0.05) the lines were omitted. (A) lnBMR as a function of lnM: for the Neognathae clade lnBMR=3.712+0.6633lnM (N=59, r2=0.973, P<0.001); for the high Scytb group lnBMR=3.283+0.8263lnM (N=15, r2=0.903, P<0.001); for the low Scytb group lnBMR=3.715+0.6663lnM (N=15, r2=0.942, P<0.001). The difference in the slopes between the low Scytb group 0.666±0.046 and the high Scytb group 0.826±0.075 is significant (P<0.001). The curves for the low Scytb and the whole clade are nearly identical. (B) LnBMRw as a function of M: for the whole clade lnBMRw=3.712–0.3373lnM (N=59, r2=0.904, P<0.001); for the high Scytb group lnBMRw=3.283–0.1743lnM (N=15, r2=0.291, P=0.038); for the low Scytb group lnBMRw=3.715–0.3343lnM (N=15, r2=0.804, P<0.001). The difference in the slopes between the low Scytb group, –0.334±0.046, and the high Scytb group, –0.175±0.075, is significant. The curves for the low Scytb and the whole clade are nearly identical. (C) lnL as a function of lnM: for the whole clade lnL=1.742+0.193xlnM (N=59, r2=0.473, P<0.001); for the high Scytb group lnL=1.616+0.27xlnM (N=15, r2=0.058, P=0.384); for the low Scytb group lnL=2.23+0.153xlnM (N=15, r2=0.551, P=0.002). (D) lnL as a function of BMRw: for the whole clade lnL=3.733–0.513xlnBMRw (N=59, r2=0.417, P<0.001); for the high Scytb group lnL=3.63–0.451xlnBMRw (N=15, r2=0.017, P=0.643); for the low Scytb group lnL=3.859–0.408xlnBMRw (N=15, r2=0.547, P=0.002).

View larger version (14K): [in this window] [in a new window]   Fig. 2. In the group of genera with accelerated evolution of cytochrome b exceptional longevity and the lifetime expenditure of energy are strong functions of the rate of evolution of cytochrome b. Data are from Table S2 in supplementary material. The genera with high Scytb values (the upper quadrant, Scytb>0.1345) are indicated by open symbols; the genera with the low Scytb values (the lowest quadrant, Scytb<0.069) are indicated by solid symbols. When the linear regression was not significant the regression line was omitted. (A) Exceptional longevity as a function of Scytb. The ratio of observed longevity (Lo) to predicted longevity (Lp), Lo/Lp, is derived from the residuals of the linear regressions (solid curves) of the Neognathae clade shown in Fig. 1C,D. The squares indicate the residuals from L(BMRw) (Fig. 1D) and the circles indicate the residuals from L(M) (Fig. 1C). For the high Scytb group, Lo/Lp(M)=–7.068+57.5xScytb (N=15, r2=0.605, P<0.001) and Lo/Lp(BMRw)=–7.258+58.7xScytb (N=15, r2=0.618, P<0.001). For the low Scytb group, Lo/Lp(M)=0.869+6.8xScytb (N=15, r2=0.013, P=0.689), and Lo/Lp(BMRw)=0.347+16.6xScytb (N=15, r2=0.06, P=0.371). For the whole clade, Lo/Lp(M)=1.02+0.55xScytb (N=59, r2=0.0021, P=0.731) and Lo/Lp(BMRw)=1.13–0.419xScytb (N=59, r2=0.001, P=0.804). (B) Lifetime energy expenditure as a function of body mass. The linear regression for the high Scytb group is LxBMRw=153+15xlnM (N=15, r2=0.004, P=0.854). The linear regression for the low Scytb group is LxBMRw=250–19xlnM (N=15, r2=0.436, P=0.007). For the whole clade, LxBMRw=218–17.2xlnM (N=59, r2=0.217, P<0.001). The correct value of lifetime expenditure of energy can be obtained by multiplying LxBMRw by 31 536 000 (the number of seconds in one year). (C) Lifetime expenditure of energy as a function of Scytb. For the high Scytb group, LxBMRw=–488+9612xScytb (N=15, r2=0.579, P<0.001). For the low Scytb group, LxBMRw=155–514xScytb (N=15, r2=0.0026, P=0.857). For the whole clade, LxBMRw=39.3+982xScytb (N=59, r2=0.206, P<0.001).

View larger version (15K): [in this window] [in a new window]   Fig. 3. The dependence of basal metabolic rates (BMR), mass-specific basal metabolic rate (BMRw), and lifetime expenditure of energy (LxBMRw) on body mass (M) in songbirds (oscines) is different from that of all other birds. The oscines birds genera are indicated by open circles, and all other bird genera are indicated by solid circles; the oscines family Fringillidae (true finches) genera are indicated by inverted triangles. The regression lines for the whole Neognathae clade (N=123) are solid, the lines for all other birds (N=64) are dotted, the oscine birds lines (N=59) are dash–dot–dash, and the Fringillidae lines (N=28) are dash–dot–dot–dash. If the regression was not significant the line was omitted. (A) lnBMR as a function of lnM. For the whole clade, lnBMR=3.765+0.648xlnM (r2=0.966, P<0.001). For oscine birds, lnBMR=3.577+0.735xlnM (r2=0.934, P<0.001). For Fringillidae, lnBMR=3.167+0.857xlnM (r2=0.920, P<0.001); and for all other birds, lnBMR=3.519+0.678xlnM (r2=0.966, P<0.001). The slopes of the three curves were significantly different from each other. (B) lnBMRw as a function of lnM. For the whole clade, lnBMRw=3.765–0.352xlnM (r2=0.893, P<0.001). For oscines, lnBMRw=3.577–0.256xlnM (r2=0.648, P<0.001). For Fringillidae, lnBMRw=3.167–0.143xlnM (r2=0.243, P=0.008). For all other birds, lnBMRw=3.519–0.322xlnM (r2=0.866, P<0.001). The difference in slopes between oscines, –0.256±0.026, and all birds, –0.352±0.011, is highly significant (t=3.13, P=0.001), but the difference in intercept is not significant. (C) ln(LxBMRw) as a function of lnM. For the whole clade, ln(LxBMRw)=5.495–0.155xlnM (r2=0.323, P<0.001). For oscines, ln(LxBMRw)=5.136–0.0139xlnM (r2=0.001, P=0.805). For Fringillidae, ln(LxBMRw)=4.411+0.212xlnM (r2=0.066, P=0.188); and for all other birds: ln(LxBMRw)=5.317–0.136xlnM (r2=0.245, P<0.001). The average value of ln(LxBMRw) was significantly larger for oscines birds, 5.093±0.368, than that of all other birds 4.567±0.562 (t=6.082, P<0.001).

View larger version (21K): [in this window] [in a new window]   Fig. 4. Mass-specific basal metabolic rates (BMRw), exceptional longevity (Lo/Lp), and lifetime expenditure of energy (LxBMRw) are function of the rate of cytochrome b evolution. Data are from Table S2 in supplementary material. (A) Mass-specific basal metabolic rates (BMRw) are function of both body mass (M) and the rate of cytochrome b evolution (Scytb) in the Fringillidae family. Multiple linear regression of lnBMRw as a function of both lnM and Scytb: LnBMRw=2.304–0.157xlnM+6.373xScytb (N=16, r2=0.706, P<0.001, VIF=1.07, P(lnM)<0.001, P(Scytb)=0.002). (B) Lo/Lp as function of Scytb. Open symbols indicate oscines (N=31), inverted triangles indicate Fringillidae (N=16), and solid symbols indicate all other birds (N=28). Lo/Lp (BMRw), the residuals from power law 1, are indicated by squares; Lo/Lp (M), the residuals from power law (3) are indicated by circles. For oscine birds Lo/Lp(BMRw)=–1.143+ 16.5xScytb (r2=0.170, P=0.021, and Lo/Lp(M)=–1.547+19.6xScytb (r2=0.243, P=0.005). For Fringillidae; Lo/Lp(M)=–3.964+36.2xScytb (r2=0.42, P=0.007); Lo/Lp(BMRw)=–4.575+40.35xScytb (r2=0.489, P=0.003). For all other birds: Lo/Lp(BMRw)=1.96–11.9xScytb (N=28, r2=0.300, P=0.003) and Lo/Lp(M)=1.676–8.37xScytb (r2=0.186, P=0.022). (C) LxBMRw as a function of Scytb. Symbols are as in B. For oscine birds LxBMRw=–213+2893xScytb (r2=0.171, P= 0.021); for Fringillidae LxBMRw=–817+7079xScytb (r2=0.507, P=0.002); for all other birds LxBMRw=164–778xScytb (r2= 0.104, P=0.095). The difference in LxBMRw between oscines, 178.7±77, and all other birds 106±47 was significant (t=4.273, P<0.001).

View larger version (27K): [in this window] [in a new window]   Fig. 5. The selected mutations in Serinus are concentrated on the matrix side of cytochrome b in the vicinity of the ubiquinone binding site Qi. Sixteen complete or nearly complete cytochrome b sequences of species of the oscine genus Serinus were aligned and used to derive a consensus sequence, which was aligned with the sequence of the non-oscine genus Empidonex. The location of the substitutions was mapped onto the chicken cytochrome b structure (3BCC) (Zhang et al., 1998), which is shown as a three-dimensional model. The location of a conserved substitution is indicated by a blue ball on the protein backbone, and that of a non-conserved substitution is indicated by a red ball. The top of the structure faces the mitochondrial matrix and includes the Qi ubiquinone binding site (with bound ubiquinone) and the bH heme (blue). The bottom of the structure faces the intermembrane space and includes the Qo ubiquinone binding site (with bound Stigmatellin) and the bL heme (magenta).