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      Chromosome Inversions, Local Adaptation and Speciation

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      Genetics
      Genetics Society of America

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          Abstract

          We study the evolution of inversions that capture locally adapted alleles when two populations are exchanging migrants or hybridizing. By suppressing recombination between the loci, a new inversion can spread. Neither drift nor coadaptation between the alleles (epistasis) is needed, so this local adaptation mechanism may apply to a broader range of genetic and demographic situations than alternative hypotheses that have been widely discussed. The mechanism can explain many features observed in inversion systems. It will drive an inversion to high frequency if there is no countervailing force, which could explain fixed differences observed between populations and species. An inversion can be stabilized at an intermediate frequency if it also happens to capture one or more deleterious recessive mutations, which could explain polymorphisms that are common in some species. This polymorphism can cycle in frequency with the changing selective advantage of the locally favored alleles. The mechanism can establish underdominant inversions that decrease heterokaryotype fitness by several percent if the cause of fitness loss is structural, while if the cause is genic there is no limit to the strength of underdominance that can result. The mechanism is expected to cause loci responsible for adaptive species-specific differences to map to inversions, as seen in recent QTL studies. We discuss data that support the hypothesis, review other mechanisms for inversion evolution, and suggest possible tests.

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          Most cited references71

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          The barrier to genetic exchange between hybridising populations.

          Suppose that selection acts at one or more loci to maintain genetic differences between hybridising populations. Then, the flow of alleles at a neutral marker locus which is linked to these selected loci will be impeded. We define and calculate measures of the barrier to gene flow between two distinct demes, and across a continuous habitat. In both cases, we find that in order for gene flow to be significantly reduced over much of the genome, hybrids must be substantially less fit, and the number of genes involved in building the barrier must be so large that the majority of other genes become closely linked to some locus which is under selection. This conclusion is not greatly affected by the pattern of epistasis, or the position of the marker locus along the chromosome.
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            A Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation

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              A polytene chromosome analysis of the Anopheles gambiae species complex.

              Field-collected specimens of all known taxa in the Anopheles gambiae complex were analyzed on the basis of chromosome inversions with reference to a standard polytene chromosome map. The phylogenetic relationships among the seven described species in the complex could be inferred from the distribution of fixed inversions. Nonrandom patterns of inversion distribution were observed and, particularly on chromosome arm 2R, provided evidence for genetically distinct populations in A. gambiae, A. arabiensis, and A. melas. In A. gambiae from Mali, stable genetic differentiation was observed even in populations living in the same region, suggesting a process of incipient speciation which is being confirmed by studies with molecular markers. The possible role of chromosome differentiation in speciation of the A. gambiae complex and in the emergence of distinct chromosomal forms within the nominal species is discussed in relation to human malaria.
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                Author and article information

                Journal
                Genetics
                Genetics
                Genetics Society of America
                0016-6731
                1943-2631
                May 24 2006
                May 2006
                May 2006
                October 03 2005
                : 173
                : 1
                : 419-434
                Article
                10.1534/genetics.105.047985
                1461441
                16204214
                e64eb6ce-206b-4003-8e4e-f2c74687fd6f
                © 2005
                History

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