Revisiting the Impact of Inversions in Evolution: From Population Genetic Markers to Drivers of Adaptive Shifts and Speciation?

Abstract

There is a growing appreciation that chromosome inversions affect rates of adaptation, speciation, and the evolution of sex chromosomes. Comparative genomic studies have identified many new paracentric inversion polymorphisms. Population models suggest that inversions can spread by reducing recombination between alleles that independently increase fitness, without epistasis or coadaptation. Areas of linkage disequilibrium extend across large inversions but may be interspersed by areas with little disequilibrium. Genes located within inversions are associated with a variety of traits including those involved in climatic adaptation. Inversion polymorphisms may contribute to speciation by generating underdominance owing to inviable gametes, but an alternative view gaining support is that inversions facilitate speciation by reducing recombination, protecting genomic regions from introgression. Likewise, inversions may facilitate the evolution of sex chromosomes by reducing recombination between sex determining alleles and alleles with sex-specific effects. However, few genes within inversions responsible for fitness effects or speciation have been identified.

Gene flow and gene flux shape evolutionary patterns of variation in Drosophila subobscura

“…The low gene transfer between inversions (gene flux) for genes located inside the inverted region observed in some Drosophila species is in agreement with both hypotheses (Laayouni et al, 2003;Schaeffer et al, 2003;Munté et al, 2005;Hoffmann and Rieseberg, 2008). However, despite the fact that Dobzhansky (1950) detected a lower fitness of heterozygous individuals from different populations of D. pseudoobscura in laboratory experiments, molecular studies failed to detect genetic differentiation within inversions sampled from different populations (Schaeffer et al, 2003).…”

“…Several hypotheses have been suggested to explain the maintenance of inversion polymorphism in populations (reviewed in Hoffmann and Rieseberg, 2008). The coadaptation hypothesis (Dobzhansky, 1950) suggests that natural selection maintains favorable combinations of alleles that interact epistatically within and between arrangements in a certain population.…”

No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution

“…The capacity of these mechanisms to generate nonrecombining regions in autosomes has been explored in the large body of theoretical research modelling the spread and maintenance of polymorphic chromosomal rearrangements such as inversions, centric fusions and reciprocal translocations [34]. These chromosomal rearrangements tend to reduce recombination when heterozygous due to reduced pairing and crossing over and to selection against recombinant gametes that contain meiotic abnormalities [35].…”

“…These chromosomal rearrangements tend to reduce recombination when heterozygous due to reduced pairing and crossing over and to selection against recombinant gametes that contain meiotic abnormalities [35]. In most such theoretical studies, it is the recombination-suppressing property of chromosomal rearrangements that is modelled as the character under selection [34]. The models can therefore be extended to encompass the spread and maintenance of any nonrecombining region, whether it originated through a rearrangement or not.…”

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

“…One of the most controversial issues, from both theoretical expectations and empirical results, is the creation and maintenance/ growth of the genomic regions of divergence during speciation with gene flow (Hoffmann and Rieseberg, 2008;Feder and Nosil, 2010;White et al, 2010;Yeaman and Whitlock, 2011;Nachman and Payseur, 2012;Nosil and Feder, 2012;Feder et al, 2012b;Narum et al, 2013). Via (2009Via ( , 2012, proposed that strong divergent selection acting on a few loci generates an inter-population process, which she called divergence hitchhiking (DH), that is characterized by reduced inter-population recombination and gene flow.…”