Interindividual variation in Complex I activity in Fundulus heteroclitus along a steep thermocline

The first enzyme in the oxidative phosphorylation pathway is Complex I (EC 1.6.5.3). Complex I is a large heteromeric enzyme complex with 45 protein subunits that translocates H(+) ions across the mitochondrial inner membrane. Among northern and southern populations of the teleost fish Fundulus heteroclitus, Complex I subunits have fixed amino acid substitutions. Additionally, there are differences in oxidative phosphorylation activity among populations of F. heteroclitus. To investigate whether these differences are related to Complex I, enzyme activity was measured in 121 individuals from five populations of F. heteroclitus and its sister species Fundulus grandis acclimated to a constant 20°C temperature. Within each population, Complex I activity is highly variable among individuals of F. heteroclitus (coefficient of variation percentage among individuals has a mean of 90% in the five F. heteroclitus populations), and the mean Complex I activity among populations is significantly different at the latitudinal extremes of the range. Importantly, Complex I activity is more similar between F. heteroclitus from the southernmost population and its sister species F. grandis than to the northern populations of F. heteroclitus, suggesting important evolutionary differences. Unexpectedly, the activity is nearly fourfold higher in southern populations than northern populations. Mitochondrial density appears to compensate partially for decreased activity in northern individuals; activity per wet weight is only twofold higher in southern populations. We suggest that some of the variation in Complex I activity is genetically based and thus is being influenced by directional selection. However, this conclusion presents a conundrum: there should not be so much variation in Complex I activity within a population if this variation is biologically important.