Unraveling coevolutionary dynamics using ecological genomics

Coevolution is a fundamental process shaping species interactions and communities. Coevolution has been mostly studied experimentally as an isolated process involving local reciprocal selection between two species. However, species comprise genetically differentiated populations across space in constant interaction with dynamic abiotic and biotic environments. Coevolution is therefore a dynamic equilibrium. The genes and genomic processes underlying the complexity of coevolution over time and space remain poorly known. A range of new theoretical developments, technological advances, and empirical approaches now allow coevolutionary dynamics to be investigated with genomic data from interacting species. Recent advances in population genomics and genome-wide association studies will enable us to better understand the genetic basis of coevolutionary dynamics. Coevolutionary interactions, from the delicate co-dependency in mutualistic interactions to the antagonistic relationship of hosts and parasites, are a ubiquitous driver of adaptation. Surprisingly, little is known about the genomic processes underlying coevolution in an ecological context. However, species comprise genetically differentiated populations that interact with temporally variable abiotic and biotic environments. We discuss the recent advances in coevolutionary theory and genomics as well as shortcomings, to identify coevolving genes that take into account this spatial and temporal variability of coevolution, and propose a practical guide to understand the dynamic of coevolution using an ecological genomics lens. Coevolutionary interactions, from the delicate co-dependency in mutualistic interactions to the antagonistic relationship of hosts and parasites, are a ubiquitous driver of adaptation. Surprisingly, little is known about the genomic processes underlying coevolution in an ecological context. However, species comprise genetically differentiated populations that interact with temporally variable abiotic and biotic environments. We discuss the recent advances in coevolutionary theory and genomics as well as shortcomings, to identify coevolving genes that take into account this spatial and temporal variability of coevolution, and propose a practical guide to understand the dynamic of coevolution using an ecological genomics lens. dynamics of genotype/trait/allele frequencies in interacting species due to the reciprocal nature of coevolution. locations where interspecific interactions are strong and reciprocal are defined as hotspots, whereas areas where population interactions are asymmetric or nonexistent are defined as coldspots. include population size fluctuations over time and space, which influences the variation in Ne and gene flow among populations. Changes in Ne (the demography history of a population) and gene flow influence the efficiency of selection and thus the strength of coevolution. changes in population size (or population density), here in the context of eco–evo feedbacks in host and parasite populations. the number of individuals that effectively participate in producing the next generation. Ne determines the rate of change in the composition of a population caused by genetic drift (i.e., the random sampling of genetic variants in a finite population). the migration of individuals, and thus of genes/alleles, between populations/demes. statistical congruence between the population genetic structures of interacting species. the set of local abiotic and biotic conditions experienced by one or several populations in a given geographic area. in spatially heterogeneous environments, evolution can lead to the adaptation of populations to their local environmental conditions. A pattern of local adaptation observed is when the mean fitness of a population in its home environment is higher than the mean fitness of populations from elsewhere [64.Williams G. Adaptation and natural selection. Princeton University Press, 1966Google Scholar]. populations connected by gene flow. Individual populations may go extinct and new populations may be established by migrants. a group of individuals who are more genetically similar to each other than they are to individuals outside the subpopulation, as a result of genetic drift, migration, mutation, and selection; also called a ‘deme’ in the metapopulation framework and often assumed as a panmictic group inferred from Bayesian inference methods in population genomics studies [65.Pritchard J.K. et al.Inference of population structure using multilocus genotype data.Genetics. 2000; 155: 945-959Crossref PubMed Scopus (24757) Google Scholar, 66.Raj A. et al.fastSTRUCTURE: variational inference of population structure in large SNP datasets.Genetics. 2014; 197: 573-589Crossref PubMed Scopus (825) Google Scholar, 67.Alexander D.H. et al.Fast model-based estimation of ancestry in unrelated individuals.Genome Res. 2009; 19: 1655-1664Crossref PubMed Scopus (3784) Google Scholar]. spatial variation in the strength of coevolution (hot- and coldspots) among interacting species due to spatial variation in the biotic and selective pressure.