title: Genome-wide congealing and rapid transitions across the speciation continuum during speciation with gene flow.
abstract: Our current understanding of speciation is often based on considering a relatively small number of genes, sometimes in isolation of one another. Here, we describe a possible emergent genome process involving the aggregate effect of many genes contributing to the evolution of reproductive isolation across the speciation continuum. When a threshold number of divergently selected mutations of modest to low fitness effects accumulate between populations diverging with gene flow, nonlinear transitions can occur in which levels of adaptive differentiation, linkage disequilibrium, and reproductive isolation dramatically increase. In effect, the genomes of the populations start to "congeal" into distinct entities representing different species. At this stage, reproductive isolation changes from being a characteristic of specific, divergently selected genes to a property of the genome. We examine conditions conducive to such genome-wide congealing (GWC), describe how to empirically test for GWC, and highlight a putative empirical example involving Rhagoletis fruit flies. We conclude with cautious optimism that the models and concepts discussed here, once extended to large numbers of neutral markers, may provide a framework for integrating information from genome scans, selection experiments, quantitative trait loci mapping, association studies, and natural history to develop a deeper understanding of the genomics of speciation.
authors.affiliation: From the Department of Biological Science, Environmental Change Initiative, and Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN 46556 (Feder); the Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S102TN (Nosil); the Interdisciplinary Quantitative Biology Program, University of Colorado, Boulder, CO 80309 (Wacholder); the Department of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005 (Egan); the Department of Entomology, University of Illinois, Urbana, IL 61801 (Berlocher); and the Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309 (Flaxman).
authors.forename: Jeffrey L
authors.initials: JL
authors.lastname: Feder
authors.affiliation: From the Department of Biological Science, Environmental Change Initiative, and Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN 46556 (Feder); the Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S102TN (Nosil); the Interdisciplinary Quantitative Biology Program, University of Colorado, Boulder, CO 80309 (Wacholder); the Department of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005 (Egan); the Department of Entomology, University of Illinois, Urbana, IL 61801 (Berlocher); and the Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309 (Flaxman).
authors.forename: Patrik
authors.initials: P
authors.lastname: Nosil
authors.affiliation: From the Department of Biological Science, Environmental Change Initiative, and Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN 46556 (Feder); the Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S102TN (Nosil); the Interdisciplinary Quantitative Biology Program, University of Colorado, Boulder, CO 80309 (Wacholder); the Department of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005 (Egan); the Department of Entomology, University of Illinois, Urbana, IL 61801 (Berlocher); and the Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309 (Flaxman).
authors.forename: Aaron C
authors.initials: AC
authors.lastname: Wacholder
authors.affiliation: From the Department of Biological Science, Environmental Change Initiative, and Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN 46556 (Feder); the Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S102TN (Nosil); the Interdisciplinary Quantitative Biology Program, University of Colorado, Boulder, CO 80309 (Wacholder); the Department of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005 (Egan); the Department of Entomology, University of Illinois, Urbana, IL 61801 (Berlocher); and the Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309 (Flaxman).
authors.forename: Scott P
authors.initials: SP
authors.lastname: Egan
authors.affiliation: From the Department of Biological Science, Environmental Change Initiative, and Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN 46556 (Feder); the Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S102TN (Nosil); the Interdisciplinary Quantitative Biology Program, University of Colorado, Boulder, CO 80309 (Wacholder); the Department of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005 (Egan); the Department of Entomology, University of Illinois, Urbana, IL 61801 (Berlocher); and the Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309 (Flaxman).
authors.forename: Stewart H
authors.initials: SH
authors.lastname: Berlocher
authors.affiliation: From the Department of Biological Science, Environmental Change Initiative, and Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN 46556 (Feder); the Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S102TN (Nosil); the Interdisciplinary Quantitative Biology Program, University of Colorado, Boulder, CO 80309 (Wacholder); the Department of Ecology and Evolutionary Biology, Rice University, Houston, TX 77005 (Egan); the Department of Entomology, University of Illinois, Urbana, IL 61801 (Berlocher); and the Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309 (Flaxman). samuel.flaxman@colorado.edu.
authors.forename: Samuel M
authors.initials: SM
authors.lastname: Flaxman
mesh_terms: D000818:Animals; D051456:Gene Flow; D005796:Genes; D049810:Genetic Speciation; D005828:Genetics, Population; D016678:Genome; D049750:Genome, Insect; D015810:Linkage Disequilibrium; D018895:Microsatellite Repeats; D009154:Mutation; D020641:Polymorphism, Single Nucleotide; D040641:Quantitative Trait Loci; D060047:Reproductive Isolation; D012641:Selection, Genetic; D061350:Sympatry; D033621:Tephritidae / Q000235:genetics
keywords: divergent selection; genetic hitchhiking; genomic architecture; linkage disequilibrium; speciation with gene flow