In Extremis: Breaking Coalescent Models in Small Populations and Concerted Convergence of Mammalian Cyanide Adaptation


Understanding how populations and species evolve in response to their environment is a key objective of population and evolutionary genetics. Extremes are useful to understand both where current models break down and to build new ones. Coalescent models of population genetics are commonly used to estimate current and past genetic diversity, but they assume that the population in question is large and of a stable size. Species of conservation concern, in particular, are generally small and/or declining. Using simulations, I found that coalescent models mischaracterize the genetic diversity of recently-declined populations. Thus current estimates of genetic diversity and management decisions for endangered species that have been based on coalescent models could be dangerously misleading. By their nature, species with extreme adaptations often have small populations. Cyanide adaptation in bamboo specialized mammals is one such adaptation, because cyanide ingestion causes death by inhibition of cellular respiration. Thus the few cyanide adapted mammals, including bamboo lemurs and giant pandas, provide an opportunity to develop a model of genetic concerted convergence, the shared evolution of a suite of traits under similar selective pressures. To determine the biochemical adaptations to cyanide survival, I analyzed urine from wild bamboo lemurs, species that can survive up to 50 times the expected lethal dose of cyanide. Bamboo lemurs excrete higher concentrations of both cyanide and thiocyanate, the primary detoxification product, than recorded in any other mammal, suggesting dual adaptation in both cellular respiration and detoxification. This also implicates adaptations in thyroid function, because thiocyanate is a thyroid antagonist, and taste, because cyanide typically causes an aversive taste response. I identified genes under selection in these four pathways in bamboo lemurs and four other bamboo specialized clades and developed a statistical test to examine concerted convergence in cyanide adaptation. Three clades, including bamboo lemurs, evolved cyanide adaptations in this suite of four traits under a concerted convergence model. This is evidence of both the necessity of adapting to an ecological selection pressure across a common suite of traits, and that an extreme adaptation can be used to develop a new model for understanding the process of adaptation.

In Ecology and Evolution. p. 152. State University of New York at Stony Brook, New York