Kinetic effects of temperature on rates of genetic divergence and speciation

Abstract

Latitudinal gradients of biodiversity and macroevolutionary dynamics are prominent yet poorly understood. We derive a model that quantifies the role of kinetic energy in generating biodiversity. The model predicts that rates of genetic divergence and speciation are both governed by metabolic rate and therefore show the same exponential temperature dependence (activation energy of approximately 0.65 eV; 1 eV = 1.602 x 10(-19) J). Predictions are supported by global datasets from planktonic foraminifera for rates of DNA evolution and speciation spanning 30 million years. As predicted by the model, rates of speciation increase toward the tropics even after controlling for the greater ocean coverage at tropical latitudes. Our model and results indicate that individual metabolic rate is a primary determinant of evolutionary rates: approximately 10(13) J of energy flux per gram of tissue generates one substitution per nucleotide in the nuclear genome, and approximately 10(23) J of energy flux per population generates a new species of foraminifera.

Fig. 1.

Effect of ocean temperature, 1/kT, on the size-corrected rate of neutral molecular evolution, ln(f_oαM^1/4), for nuclear genomes of planktonic foraminifera. The slope (−0.67 eV) was fitted by using ordinary least-squares regression and is close to the value of −E ≈ −0.65 eV (95% CI, −0.26 to −1.07 eV), which was predicted based on the temperature dependence of individual metabolic rate (Eq. 3). Refer to Appendix 1 for details on this global compilation of SSU rDNA data.

Fig. 2.

Effect of ocean temperature, 1/kT, on genetic divergence, ln(D_s), for nuclear genomes of ecologically distinct genotypes within seven morphospecies of planktonic foraminifera. The sample sizes in the legend refer to the numbers of pairwise comparisons among populations comprising each morphospecies. The data were weighted such that each morphospecies contributed equally to the ordinary least-squares regression slope, which does not differ from the predicted value of 0 (Eq. 7). This conclusion remains unchanged if data points, rather than morphospecies, are weighted equally (P = 0.10). Refer to Appendix 2 for details on this global compilation of SSU rDNA data.

Fig. 3.

Both ecological and macroevolutionary variables exhibit pronounced variation from the poles to the equator. (A) Depicted are the latitudinal gradient in contemporary mean annual sea-surface temperatures (48) (dashed line) and ocean surface area per 0.5° latitude (solid line; negative numbers correspond to southern latitudes). Different shades are used to represent four equal-area latitudinal bands of ≈9.1 × 10⁷ km² ocean area each. (B) Depicted are the effects of ocean temperature on time-averaged speciation rates over the past 30 Ma in each of the four equal-area latitudinal bands. The line was fitted by using ordinary least-squares regression. Speciation rates were calculated based on the latitudinal distribution of >150 FO of foraminifera morphospecies by using the Neptune database (32); 95% CIs (vertical lines) were generated, as described in Appendix 3, by using a randomization procedure that explicitly controls for the effects of variation in sampling efforts on paleontological analyses. The average sea-surface temperature within each latitudinal band over the past 30 Ma was estimated, as described in Appendix 4, by using a robust paleotemperature calibration (33).