BIOLOGICAL SCIENCES / EVOLUTION
Kinetic effects of temperature on rates of genetic divergence and speciation
Andrew P. Allen*,, James F. Gillooly, Van M. Savage, and James H. Brown,¶
*National Center for Ecological Analysis and Synthesis, 735 State Street, Suite 300, Santa Barbara, CA 93101; Department of Zoology, University of Florida, Gainesville, FL 32611; Bauer Center for Genomics Research, Harvard University, Boston, MA 02138; and ¶Department of Biology, University of New Mexico, Albuquerque, NM 87131
Contributed by James H. Brown, May 2, 2006
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 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: 1013 J of energy flux per gram of tissue generates one substitution per nucleotide in the nuclear genome, and 1023 J of energy flux per population generates a new species of foraminifera.
allopatric speciation | biodiversity | macroevolution | metabolic theory of ecology | molecular clock
PNAS, June 13, 2006, vol. 103, no. 24, 9130-9135. OPEN ACCESS ARTICLE.
The latitudinal increase in biodiversity from the poles to the equator is the most pervasive feature of biogeography. For two centuries, since the time of von Humboldt, Darwin, and Wallace, scientists have proposed hypotheses to explain this pattern. New species arise through the evolution of genetic differences among populations from a common ancestral lineage (1–4). Many hypotheses therefore attribute the latitudinal biodiversity gradient to a gradient in speciation rates caused by some independent variable, such as earth surface area or solar energy input (5–7). Some fossil data suggest that speciation rates do indeed increase toward the tropics (8–10), but these findings remain open to debate due in part to our limited understanding of the factors that control macroevolutionary dynamics.
Recent advances toward a metabolic theory of ecology (11) provide new opportunities for assessing the factors that control speciation rates. This recent work indicates that two fundamental variables influencing the tempo of evolution, the generation time, and the mutation rate (3) are both direct consequences of biological metabolism (12–14). Here we combine these recent insights from metabolic theory with the theory of population genetics to derive a model that predicts how environmental temperature, through its effects on individual metabolic rates (Eqs. 1–4), influences rates of genetic divergence among populations (Eqs. 5–7) and rates of speciation in communities (Eqs. 8 and 9). We evaluate the model by using data from planktonic foraminifera, because this group has extensive DNA sequence data for evaluating population-level predictions on genetic divergence combined with an exceptionally complete fossil record for evaluating community-level predictions on speciation rates.