The emergence of supergenes from inversions in Atlantic salmon

Abstract

Supergenes link allelic combinations into non-recombining units known to play an essential role in maintaining adaptive genetic variation. However, because supergenes can be maintained over millions of years by balancing selection and typically exhibit strong recombination suppression, both the underlying functional variants and how the supergenes are formed are largely unknown. Particularly, questions remain over the importance of inversion breakpoint sequences and whether supergenes capture pre-existing adaptive variation or accumulate this following recombination suppression. To investigate the process of supergene formation, we identified inversion polymorphisms in Atlantic salmon by assembling eleven genomes with nanopore long-read sequencing technology. A genome assembly from the sister species, brown trout, was used to determine the standard state of the inversions. We found evidence for adaptive variation through genotype–environment associations, but not for the accumulation of deleterious mutations. One young 3 Mb inversion segregating in North American populations has captured adaptive variation that is still segregating within the standard arrangement of the inversion, while some adaptive variation has accumulated after the inversion. This inversion and two others had breakpoints disrupting genes. Three multigene inversions with matched repeat structures at the breakpoints did not show any supergene signatures, suggesting that shared breakpoint repeats may obstruct supergene formation. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

Genomic architecture and functional effects of potential human inversion supergenes

“…This allows the generation of highly divergent haplotypes accumulating a large number of sequence differences, which can form coadapted gene complexes [ 5 , 6 ]. In fact, there are many examples of inversion supergenes involved in adaptation in multiple organisms, such as the polymorphic social behaviour of ants, the Batesian mimicry wing colour pattering in butterflies or mating morphs in sparrows and ruffs, among many others [ 7 – 11 ].…”

Genomic architecture of supergenes: connecting form and function

“…[ 58 ] use simulated data to explore the dynamics of capture and gain, while Stenløkk et al . [ 59 ] examine the evidence for capture versus gain using data from the Atlantic salmon.…”

“…Stenløkk et al . [ 59 ] use empirical data to test for capture versus gain of adaptive alleles in Atlantic salmon. The authors take advantage of advances in sequencing and analysis to conduct a comparative analysis of all inversions segregating in the metapopulation of Atlantic salmon across the species range.…”

“…Berdan et al [ 68 ] use simulations to look at mutation accumulation in supergenes and the ensuing consequences, while Stenløkk et al . [ 59 ] look for signatures of this mutation accumulation in Atlantic salmon.…”

“…Stenløkk et al . [ 59 ] directly test for mutation accumulation in inversions segregating in the metapopulation of Atlantic salmon. For each inversion they assess accumulation of deleterious mutations (or lack thereof), and analyse change through time, by comparing the focal inversion to its ancestral state of inversions in a sister species.…”