The role of chromosomal inversions in speciation

Abstract

The chromosomal inversions of D. persimilis and D. pseudoobscura have deeply influenced our understanding of the evolutionary forces that shape natural variation, speciation, and selfish chromosome dynamics. Here, we perform a comprehensive reconstruction of the evolutionary histories of the chromosomal inversions in these species. We provide a solution to the puzzling origins of the selfish Sex-Ratio chromosome in D. persimilis and show that this Sex-Ratio chromosome directly descends from an ancestrally-arranged chromosome. Our results further show that all fixed inversions between D. persimilis and D. pseudoobscura were segregating in the ancestral population long before speciation, and that the genes contributing to reproductive barriers between these species must have evolved within them afterwards. We propose a new model for the role of chromosomal inversions in speciation and suggest that higher levels of divergence and an association with hybrid incompatibilities are emergent properties of ancestrally segregating inversions. These findings force a reconsideration of the role of chromosomal inversions in speciation, not as protectors of existing hybrid incompatibility alleles, but as fertile grounds for their formation.

The Paradox Behind the Pattern of Rapid Adaptive Radiation: How Can the Speciation Process Sustain Itself Through an Early Burst?

“…Challenges remain for theorists to construct predictive models that can incorporate the complexity of the radiation process in any given system, including a distribution of effect sizes for a diverse set of polygenic traits contributing to reproductive isolation, diverse assortative mating mechanisms, complex fitness landscapes, and long-term structural evolution of the genome. In turn, many of the parameters most relevant to rapid radiation are still unknown in most case studies, including the ubiquity of phenotype matching (Kopp et al 2018), the proximity of neighboring fitness peaks in phenotype and genotype space (Blount et al 2012, Erwin 2017, Martin & Wainwright 2013b, and the frequency and timescale of physical linkages among adaptive alleles and DMIs (Fuller et al 2017, Wright et al 2013. Only with these models and data in hand will we be able to predict the full spectrum of the process of adaptive radiation.…”

“…In taxa with labile structural evolution (e.g., fish, mammals), simulations indicate that chromosomal rearrangements are likely to produce physically linked clusters of coadapted alleles (Yeaman 2013). Alternatively, inversions may be segregating within ancient populations, and adaptive alleles may be more likely to fix within them later, as recently found in the Drosophila persimilis and D. pseudoobscura species pair (Fuller et al 2017). More broadly, there are numerous other examples of introgression or sorting of ancient adaptive alleles during adaptive radiation, such as Heliconius butterflies (Heliconius Genome Consortium 2012), Rhagoletis flies (Feder et al 2003), Caribbean pupfishes (Richards & Martin 2017), Cameroon crater lake cichlids (Richards et al 2018), and tomatoes (Pease et al 2016).…”

“…A second broad class of speciation-promoting mechanisms occurs at the level of genetic architecture, including physical linkages between mating loci and ecological loci, between different types of ecological loci involved in adaptation to the same niche (Yeaman & Whitlock 2011), or between ecological loci and intrinsic reproductive incompatibilities (Seehausen 2013). Inversions can capture physically linked adaptive alleles and suppress recombination (Fuller et al 2017, Kirkpatrick & Barton 2006. Physical linkage of ecological or mating loci to DMIs may also promote speciation by effectively reducing the breakdown of beneficial haplotypes due to recombination between divergent species' backgrounds after secondary contact (e.g., Wright et al 2013), or ecological divergence may directly result in DMIs through hybrid gene misregulation (Mack & Nachman 2017.…”

“…Future work should evaluate the prevalence of structural rearrangements, such as inversions, and estimate the age of these events and the adaptive alleles within relative to the age of the radiation (e.g., as recently done for a single species pair, Fuller et al 2017). Absolute divergence time estimates are highly dependent on unknown and highly variable spontaneous mutation rates across taxa at the recent timescales of rapid radiation (Ho et al 2011, Lynch 2010, Martin & Höhna 2017, Martin et al 2017b; however, relative time estimates are feasible, particularly when adaptive alleles are often orders of magnitude older than the species in which they occur (Colosimo et al 2005, Nelson & Cresko 2018.…”

What is Speciation Genomics? The roles of ecology, gene flow, and genomic architecture in the formation of species

“…Pairs of dotted lines are interacting genes: co-adapted gene complexes or genetic incompatibilities. Blue represents low genetic divergence between populations, orange represents high divergence and purple (as in the model of Fuller et al 2017) represents high divergence segregating within populations. In contrast to the other models, higher divergence within inverted regions compared to collinear regions is not a consequence of (differential) gene flow.…”