Abstract

How the neutral diversity is affected by selection and adaptation is investigated in an eco-evolutionary framework. In our model, we study a finite population in continuous time, where each individual is characterized by a trait under selection and a completely linked neutral marker. Population dynamics are driven by births and deaths, mutations at birth, and competition between individuals. Trait values influence ecological processes (demographic events, competition), and competition generates selection on trait variation, thus closing the eco-evolutionary feedback loop. The demographic effects of the trait are also expected to influence the generation and maintenance of neutral variation. We consider a large population limit with rare mutation, under the assumption that the neutral marker mutates faster than the trait under selection. We prove the convergence of the stochastic individual-based process to a new measure-valued diffusive process with jumps that we call Substitution Fleming-Viot Process (SFVP). When restricted to the trait space this process is the Trait Substitution Sequence first introduced by Metz et al. (1996). During the invasion of a favorable mutation, a genetical bottleneck occurs and the marker associated with this favorable mutant is hitchhiked. By rigorously analysing the hitchhiking effect and how the neutral diversity is restored afterwards, we obtain the condition for a time-scale separation; under this condition, we show that the marker distribution is approximated by a Fleming-Viot distribution between two trait substitutions. We discuss the implications of the SFVP for our understanding of the dynamics of neutral variation under eco-evolutionary feedbacks and illustrate the main phenomena with simulations. Our results highlight the joint importance of mutations, ecological parameters, and trait values in the restoration of neutral diversity after a selective sweep.

Highlights

  • The science of biodiversity currently faces the challenge of understanding how ecological processes shape evolutionary change, and reciprocally how evolution affects the structure and function of ecological systems (Schoener, 2011)

  • Neutral diversity is restored after each adaptive jump, but as the adaptive trait evolves, population size, the mutation rate, genetic drift and demographic fluctuations change, which causes the rate of neutral polymorphism build-up and the moments of the marker distribution to change too

  • This suggests that the nature and structure of the whole eco-evolutionary feedback loop may be important to explain the extreme disparities in genetic neutral diversity observed among species, even closely related ones and in the absence of differences in recombination profiles (Cutter and Payseur, 2013)

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Summary

Introduction

The science of biodiversity currently faces the challenge of understanding how ecological processes shape evolutionary change, and reciprocally how evolution affects the structure and function of ecological systems (Schoener, 2011). Neutral diversity is restored after each adaptive jump, but as the adaptive trait evolves, population size, the mutation rate, genetic drift and demographic fluctuations change, which causes the rate of neutral polymorphism build-up and the moments of the marker distribution to change too This suggests that the nature and structure of the whole eco-evolutionary feedback loop (i.e. how adaptive traits influence demographic rates and ecological interactions, and how ecological processes shape selection pressures on adaptive traits) may be important to explain the extreme disparities in genetic neutral diversity observed among species, even closely related ones and in the absence of differences in recombination profiles (Cutter and Payseur, 2013). As a conclusion of the proof, we show the convergence to the SFVP in the space of trait-marker-time measures

The stochastic model
Convergence to the Substitution Fleming-Viot Process
Invasion fitness function
Main theorem
Corollary: the Wright-Fisher Evolutionary Process
Extensions to co-existing traits
Semimartingale decomposition of νK
Convergence of the trait-marginal in the trait mutation time scale
Marker distribution in a new adaptive trait mutant population
Conclusion
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