InversionIIJFv13.doc - Adaptive chromosomal divergence...

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Adaptive chromosomal divergence driven by mixed geographic mode of evolution Jeffrey L. Feder 1,2 Richard Gejii 3 Tom Powell 1 Patrik Nosil 2,4 1 Dept. of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA. email: [email protected] , [email protected] . 2 Institute for Advanced Study, Wissenschaftskolleg, Berlin, 14193, Germany. 3 Dept. of Mathematics, University of Notre Dame, Notre Dame, IN 46556, USA. email: [email protected] . 4 Department of Ecology and Evolutionary Biology, University of Boulder, Colorado, 80309, USA; email: [email protected] Corresponding author: Jeffrey L. Feder Dept. of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA e-mail: [email protected] Tel: (574)-631-4159 Fax: (574)-631-7413 Chromosomal inversions are ubiquitous in nature and are of great significance for understanding adaptation and speciation ( 1 - 7 ). Here, we show that a mixed geographic mode of evolution involving allopatric separation followed by secondary contact and gene flow generates chromosomal divergence by natural selection under wider conditions than previous hypotheses ( 6 - 13 ). Moreover, the mixed model accounts for several patterns in the geographic distribution of inversions, including increased polymorphism in the center of species ranges ( 14 ), inversion differences in small populations ( 15 ), maladaptive inversions in allopatric populations ( 6 , 7 , 16 , 17 ), and high frequencies of inversions in sympatric populations ( 10 ). As inversion differences often separate closely related taxa ( 6 , 7 ), mixed modes of divergence could be common during adaptation and speciation. Inversions have played a central role in evolutionary biology ( 18 ). Inversions were the first markers used to investigate the genetic structure of natural populations, leading to the concept of coadapted gene complexes ( 1 ). Inversions have also played a key role in advancing theories concerning stochastic processes in evolution ( 6 , 7 ). Because of the presumed underdominance of inversions ( 3 , 10 , 16 ), it was argued that their fixation generally required pronounced genetic drift in small, isolated populations ( 6 , 7 ; but see 19 ). In contrast to underdominance models, more recent genic hypotheses based on the allelic content and reduced recombination of inversions have shown that inversions can spread without drift ( 8 - 13 ). In one class of ‘allopatric origins’ models, an inversion initially rises to high frequency or fixation in a geographically isolated population. On secondary contact, populations remain differentiated for inversions, whereas collinear regions homogenize, due to differences in the effectiveness of selection in regions of low versus high recombination ( 10 , 11 ). There are theoretical difficulties, however, with allopatric origins models ( 12 , 20 ). First, it is hard to explain how inversions arise and initially spread in allopatric populations experiencing homogenous selection pressures ( 12 ), except perhaps by meiotic drive ( 6 , 7 ). Second, if inversions often fix in allopatry prior to secondary contact, then they should commonly
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distinguish allopatric populations. In contrast to this prediction, five of six sympatric pairs of
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