Kimura’s Theory of Non-Adaptive Radiation and Peto’s Paradox: A Missing Link?

SIMPLE SUMMARY: Karyotype diversity, or the interspecific variation in the number of chromosomes and their different forms and sizes in a genome, and species richness, or the number of different species in a phylogenetic clade, are correlated and vary substantially across different animal lineages belonging to the same taxonomic groups, such as salamanders or mammals. The reasons why some lineages are species rich and others are species poor, and why karyotype diversity should correlate so closely with species richness, remain unclear. The following examines these two questions in the context of Motoo Kimura’s hypothesis of non-adaptive radiation and Peto’s paradox. Species richness appears to be inversely correlated with genome stability in mammals and possibly salamanders: lineages with more stable karyotypes tend to be less species rich. Karyotype stability and genome stability, in turn, depend on the cellular DNA damage detection and repair system, suggesting that differences in species richness might be, in part, attributable to lineage specific differences in DNA repair fidelity and efficiency. ABSTRACT: Karyotype diversity reflects genome integrity and stability. A strong correlation between karyotype diversity and species richness, meaning the number of species in a phylogenetic clade, was first reported in mammals over forty years ago: in mammalian phylogenetic clades, the standard deviation of karyotype diversity (KD) closely corresponded to species richness (SR) at the order level. These initial studies, however, did not control for phylogenetic signal, raising the possibility that the correlation was due to phylogenetic relatedness among species in a clade. Accordingly, karyotype diversity trivially reflects species richness simply as a passive consequence of adaptive radiation. A more recent study in mammals controlled for phylogenetic signals and established the correlation as phylogenetically independent, suggesting that species richness cannot, in itself, explain the observed corresponding karyotype diversity. The correlation is, therefore, remarkable because the molecular mechanisms contributing to karyotype diversity are evolutionarily independent of the ecological mechanisms contributing to species richness. Recently, it was shown in salamanders that the two processes generating genome size diversity and species richness were indeed independent and operate in parallel, suggesting a potential non-adaptive, non-causal but biologically meaningful relationship. KD depends on mutational input generating genetic diversity and reflects genome stability, whereas species richness depends on ecological factors and reflects natural selection acting on phenotypic diversity. As mutation and selection operate independently and involve separate and unrelated evolutionary mechanisms—there is no reason a priori to expect such a strong, let alone any, correlation between KD and SR. That such a correlation exists is more consistent with Kimura’s theory of non-adaptive radiation than with ecologically based adaptive theories of macro-evolution, which are not excluded in Kimura’s non-adaptive theory. The following reviews recent evidence in support of Kimura’s proposal, and other findings that contribute to a wider understanding of the molecular mechanisms underlying the process of non-adaptive radiation.