Abstract
Many hypotheses have been put forth to explain the origin and spread of inversions, and their significance for speciation. Several recent genic models have proposed that inversions promote speciation with gene flow due to the adaptive significance of the genes contained within them and because of the effects inversions have on suppressing recombination. However, the consequences of inversions for the dynamics of genome wide divergence across the speciation continuum remain unclear, an issue we examine here. We review a framework for the genomics of speciation involving the congealing of the genome into alternate adaptive states representing species (“genome wide congealing”). We then place inversions in this context as examples of how genetic hitchhiking can potentially hasten genome wide congealing. Specifically, we use simulation models to (i) examine the conditions under which inversions may speed genome congealing and (ii) quantify predicted magnitudes of these effects. Effects of inversions on promoting speciation were most common and pronounced when inversions were initially fixed between populations before secondary contact and adaptation involved many genes with small fitness effects. Further work is required on the role of underdominance and epistasis between a few loci of major effect within inversions. The results highlight five important aspects of the roles of inversions in speciation: (i) the geographic context of the origins and spread of inversions, (ii) the conditions under which inversions can facilitate divergence, (iii) the magnitude of that facilitation, (iv) the extent to which the buildup of divergence is likely to be biased within vs. outside of inversions, and (v) the dynamics of the appearance and disappearance of exceptional divergence within inversions. We conclude by discussing the empirical challenges in showing that inversions play a central role in facilitating speciation with gene flow.
Highlights
Generation DNA sequencing allows large portions of the genomes of organisms to be screened for polymorphism and divergence during the speciation process (Hudson, 2008; Rokas and Abbot, 2009; Stapley et al, 2010)
Even under parameter combinations of m and s that maximized the effects of inversions, these effects were not necessarily expected to be common; a major factor determining how often inversions accelerated divergence was the magnitude of inversion frequency differences between populations at the onset of gene flow
For the parameter values we explored, pronounced effects of inversions were only common when inversions were alternatively fixed between populations upon secondary contact
Summary
Generation DNA sequencing allows large portions of the genomes of organisms to be screened for polymorphism and divergence during the speciation process (Hudson, 2008; Rokas and Abbot, 2009; Stapley et al, 2010). Surveying a genome sequence provides a way to find loci of potential evolutionary interest (e.g., statistical outlier loci with elevated divergence), enabling questions concerning the numbers, types, and distribution of genetic changes involved in adaptation and speciation to be addressed. We have a good understanding of how the core evolutionary forces of mutation, migration, selection, and drift should affect change and population divergence at the level of individual genes (Yeaman and Otto, 2011). The action of these processes on individual loci has been documented empirically (Coyne and Orr, 2004; Gavrilets, 2004; Barrett and Hoekstra, 2011; Nosil, 2012). Genome scans of many species, such as sticklebacks (Jones et al, 2012), Heliconius butterflies
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