title: The molecular clock of neutral evolution can be accelerated or slowed by asymmetric spatial structure.
abstract: Over time, a population acquires neutral genetic substitutions as a consequence of random drift. A famous result in population genetics asserts that the rate, K, at which these substitutions accumulate in the population coincides with the mutation rate, u, at which they arise in individuals: K = u. This identity enables genetic sequence data to be used as a "molecular clock" to estimate the timing of evolutionary events. While the molecular clock is known to be perturbed by selection, it is thought that K = u holds very generally for neutral evolution. Here we show that asymmetric spatial population structure can alter the molecular clock rate for neutral mutations, leading to either K<u or K>u. Our results apply to a general class of haploid, asexually reproducing, spatially structured populations. Deviations from K = u occur because mutations arise unequally at different sites and have different probabilities of fixation depending on where they arise. If birth rates are uniform across sites, then K ≤ u. In general, K can take any value between 0 and Nu. Our model can be applied to a variety of population structures. In one example, we investigate the accumulation of genetic mutations in the small intestine. In another application, we analyze over 900 Twitter networks to study the effect of network topology on the fixation of neutral innovations in social evolution.
authors.affiliation: Department of Mathematics, Emmanuel College, Boston, Massachusetts, United States of America; Program for Evolutionary Dynamics, Harvard University, Cambridge, Massachusetts, United States of America; Center for Mathematical Sciences and Applications, Harvard University, Cambridge, Massachusetts, United States of America.
authors.forename: Benjamin
authors.initials: B
authors.lastname: Allen
authors.affiliation: Department of Mathematics, Emmanuel College, Boston, Massachusetts, United States of America.
authors.forename: Christine
authors.initials: C
authors.lastname: Sample
authors.affiliation: Department of Mathematics, Emmanuel College, Boston, Massachusetts, United States of America.
authors.forename: Yulia
authors.initials: Y
authors.lastname: Dementieva
authors.affiliation: Department of Mathematics, Emmanuel College, Boston, Massachusetts, United States of America.
authors.forename: Ruben C
authors.initials: RC
authors.lastname: Medeiros
authors.affiliation: Department of Mathematics, Emmanuel College, Boston, Massachusetts, United States of America.
authors.forename: Christopher
authors.initials: C
authors.lastname: Paoletti
authors.affiliation: Program for Evolutionary Dynamics, Harvard University, Cambridge, Massachusetts, United States of America; Department of Mathematics, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America.
authors.forename: Martin A
authors.initials: MA
authors.lastname: Nowak
mesh_terms: D019295:Computational Biology; D019143:Evolution, Molecular; D040961:Genetic Drift; D005828:Genetics, Population; D006801:Humans; D008957:Models, Genetic; D009154:Mutation