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      Spatially Heterogeneous Environmental Selection Strengthens Evolution of Reproductively Isolated Populations in a Dobzhansky–Muller System of Hybrid Incompatibility

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          Abstract

          Within-species hybrid incompatibility can arise when combinations of alleles at more than one locus have low fitness but where possession of one of those alleles has little or no fitness consequence for the carriers. Limited dispersal with small numbers of mate potentials alone can lead to the evolution of clusters of reproductively isolated genotypes despite the absence of any geographical barriers or heterogeneous selection. In this paper, we explore how adding heterogeneous natural selection on the genotypes (e.g., gene environment associations) that are involved in reproductive incompatibility affects the frequency, size and duration of evolution of reproductively isolated clusters. We conducted a simulation experiment that varied landscape heterogeneity, dispersal ability, and strength of selection in a continuously distributed population. In our simulations involving spatially heterogeneous selection, strong patterns of adjacency of mutually incompatible genotypes emerged such that these clusters were truly reproductively isolated from each other, with no reproductively compatible “bridge” individuals in the intervening landscape to allow gene flow between the clusters. This pattern was strong across levels of gene flow and strength of selection, suggesting that even relatively weak selection acting in the context of strong gene flow may produce reproductively isolated clusters that are large and persistent, enabling incipient speciation in a continuous population without geographic isolation.

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          The molecular evolutionary basis of species formation.

          All plant and animal species arise by speciation - the evolutionary splitting of one species into two reproductively incompatible species. But until recently our understanding of the molecular genetic details of speciation was slow in coming and largely limited to Drosophila species. Here, I review progress in determining the molecular identities and evolutionary histories of several new 'speciation genes' that cause hybrid dysfunction between species of yeast, flies, mice and plants. The new work suggests that, surprisingly, the first steps in the evolution of hybrid dysfunction are not necessarily adaptive.
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            Widespread genetic incompatibility in C. elegans maintained by balancing selection.

            Natural selection is expected to eliminate genetic incompatibilities from interbreeding populations. We have discovered a globally distributed incompatibility in the primarily selfing species Caenorhabditis elegans that has been maintained despite its negative consequences for fitness. Embryos homozygous for a naturally occurring deletion of the zygotically acting gene zeel-1 arrest if their sperm parent carries an incompatible allele of a second, paternal-effect locus, peel-1. The two interacting loci are tightly linked, with incompatible alleles occurring in linkage disequilibrium in two common haplotypes. These haplotypes exhibit elevated sequence divergence, and population genetic analyses of this region indicate that natural selection is preserving both haplotypes in the population. Our data suggest that long-term maintenance of a balanced polymorphism has permitted the incompatibility to persist despite gene flow across the rest of the genome.
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              Genomic divergence during speciation: causes and consequences.

              Speciation is a fundamental process responsible for the diversity of life. Progress has been made in detecting individual 'speciation genes' that cause reproductive isolation. In contrast, until recently, less attention has been given to genome-wide patterns of divergence during speciation. Thus, major questions remain concerning how individual speciation genes are arrayed within the genome, and how this affects speciation. This theme issue is dedicated to exploring this genomic perspective of speciation. Given recent sequencing and computational advances that now allow genomic analyses in most organisms, the goal is to help move the field towards a more integrative approach. This issue draws upon empirical studies in plants and animals, and theoretical work, to review and further document patterns of genomic divergence. In turn, these studies begin to disentangle the role that different processes, such as natural selection, gene flow and recombination rate, play in generating observed patterns. These factors are considered in the context of how genomes diverge as speciation unfolds, from beginning to end. The collective results point to how experimental work is now required, in conjunction with theory and sequencing studies, to move the field from descriptive studies of patterns of divergence towards a predictive framework that tackles the causes and consequences of genome-wide patterns.
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                Author and article information

                Contributors
                Journal
                Front Genet
                Front Genet
                Front. Genet.
                Frontiers in Genetics
                Frontiers Media S.A.
                1664-8021
                24 November 2016
                2016
                : 7
                : 209
                Affiliations
                [1] 1USDA Forest Service, Rocky Mountain Research Station Flagstaff, AZ, USA
                [2] 2Division of Biological Sciences, University of Montana Missoula, MY, USA
                Author notes

                Edited by: Guo-Bo Chen, Evergreen Landscape&Architecture Studio, China

                Reviewed by: Yu-Ping Poh, University of Massachusetts Boston, USA; Olivier Francois, Grenoble Institute of Technology, France

                *Correspondence: Samuel A. Cushman scushman@ 123456fs.fed.us

                This article was submitted to Evolutionary and Population Genetics, a section of the journal Frontiers in Genetics

                Article
                10.3389/fgene.2016.00209
                5121238
                a69cc4df-9def-4d89-aded-9917f11b1ee3
                Copyright © 2016 Cushman and Landguth.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 13 August 2016
                : 10 November 2016
                Page count
                Figures: 3, Tables: 4, Equations: 0, References: 32, Pages: 9, Words: 6183
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: EF-1442597
                Funded by: U.S. Forest Service 10.13039/100006959
                Categories
                Genetics
                Original Research

                Genetics
                cdpop,computer simulations,genotype-environment associations,hybrid-incompatability,landscape genomics

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