Evolutionary scaling of maximum growth rate with organism size

Abstract

Data from nearly 1000 species reveal the upper bound to rates of biomass production achievable by natural selection across the Tree of Life. For heterotrophs, maximum growth rates scale positively with organism size in bacteria but negatively in eukaryotes, whereas for phototrophs, the scaling is negligible for cyanobacteria and weakly negative for eukaryotes. These results have significant implications for understanding the bioenergetic consequences of the transition from prokaryotes to eukaryotes, and of the expansion of some groups of the latter into multicellularity. The magnitudes of the scaling coefficients for eukaryotes are significantly lower than expected under any proposed physical-constraint model. Supported by genomic, bioenergetic, and population-genetic data and theory, an alternative hypothesis for the observed negative scaling in eukaryotes postulates that growth-diminishing mutations with small effects passively accumulate with increasing organism size as a consequence of associated increases in the power of random genetic drift. In contrast, conditional on the structural and functional features of ribosomes, natural selection has been able to promote bacteria with the fastest possible growth rates, implying minimal conflicts with both bioenergetic constraints and random genetic drift. If this extension of the drift-barrier hypothesis is correct, the interpretations of comparative studies of biological traits that have traditionally ignored differences in population-genetic environments will require revisiting.

Figure 1

Relationship between estimates of maximum interval-specific growth rates and adult body mass for various taxonomic groups (normalized to 20 °C). Open points denote unicellular species; solid points multicellular species. The solid lines denote regressions (only shown for phylogenetic groups where significant), whereas the diagonal dashed line is the approximate upper bound to heterotrophic growth rates across all groups (as described in the text, and excluding larval fish). In the lower panel for autotrophs, the black lines from the profile for heterotrophs are added as reference points. The horizontal dashed black and red lines are the hypothetical upper bounds on growth rates dictated by the translational constraints imposed by the properties of ribosomes (as described in the “Discussion”).

Figure 2

Mean performance (on a 0 to 1 scale) as a function of the effective population size ($N_e$), the selection coefficient (s), and the size of linkage groups, for the case of a biallelic model with the mutation rate to the beneficial allele being $10\times$ the reciprocal rate. All results denote the selection-drift-mutation equilibrium performance (as described in the main text, but equal to the mean frequency of $+$ alleles for the case of single effects). (Upper left) Results are given for the situation in which all sites have equal mutational effects, for four values of the selection coefficient s (bundles of curves) and six linkage-block sizes [color coded as in the inset of the lower left panel]. The cartoons to the right denote arbitrary stretches of linked sites with different fractions of sites containing $+$ alleles (solid balls), increasing as mean performance increases. As s declines by a factor x, the curves shift to the right in an essentially constant pattern, such that a specific level of performance requires an x-fold increase in $N_e$. (Lower left) The latter point is made by plotting the points in the upper left panel against the product $N_{e}s$, which leads to nearly perfectly overlapping curves. (Lower right) Results for the situation in which two types of linked sites are simultaneously selected upon: the numbers and selection coefficients associated with large-effect sites are given within the graph, whereas the small-effect sites are $10\times$ more abundant but have $10\times$ smaller selective effects, such the full performance of the system is equally distributed over the linked sets of large- and small-effect sites.