Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion

Abstract

Supergenes are groups of tightly linked loci whose variation is inherited as a single Mendelian locus and are a common genetic architecture for complex traits under balancing selection [1-8]. Supergene alleles are long-range haplotypes with numerous mutations underlying distinct adaptive strategies, often maintained in linkage disequilibrium through the suppression of recombination by chromosomal rearrangements [1, 5, 7-9]. However, the mechanism governing the formation of supergenes is not well understood and poses the paradox of establishing divergent functional haplotypes in the face of recombination. Here, we show that the formation of the supergene alleles encoding mimicry polymorphism in the butterfly Heliconius numata is associated with the introgression of a divergent, inverted chromosomal segment. Haplotype divergence and linkage disequilibrium indicate that supergene alleles, each allowing precise wing-pattern resemblance to distinct butterfly models, originate from over a million years of independent chromosomal evolution in separate lineages. These "superalleles" have evolved from a chromosomal inversion captured by introgression and maintained in balanced polymorphism, triggering supergene inheritance. This mode of evolution involving the introgression of a chromosomal rearrangement is likely to be a common feature of complex structural polymorphisms associated with the coexistence of distinct adaptive syndromes. This shows that the reticulation of genealogies may have a powerful influence on the evolution of genetic architectures in nature.

Phylogeography of a cryptic speciation continuum in Eurasian spadefoot toads (Pelobates)

“…the window of divergence across which nascent species do not merge, but still frequently hybridize) is remarkably narrow (Roux et al, ): <1 million years separates the admixing subspecies P. b. balcanicus / chloeae (pending proper analyses of their hybrid zone) from the nearly impermeable genomes of P. fuscus and P. vespertinus . In contrast, the alternative situation where barriers to gene flow emerge suddenly, due to few genes or gene complexes (e.g., supergenes) with major effects (Servedio, van Doorn, Kopp, Frame, & Nosil, ), better applies to systems where ecological and behavioural divergence is a major driver of reproductive isolation (e.g., Jay et al, ), not to ecomorphologically cryptic species diverging in allopatry.…”

Geographic contrasts between pre‐ and postzygotic barriers are consistent with reinforcement inHeliconiusbutterflies

“…One of the introgressed color pattern loci, cortex , is trapped in a fixed ∼400 kb inversion in H. pardalinus , with H. elevatus having apparently receiving its uninverted copy of the cortex color locus from a rayed form of H. melpomene (Jay et al. ). Reduced recombination between the inverted and uninverted chromosome could have aided rapid achievement of such tight linkage disequilibrium during putative hybrid speciation of H. elevatus (Noor et al.…”

Chromosome polymorphisms track trans‐Atlantic divergence and secondary contact in Atlantic salmon

“…When ice sheets retreated following glacial maxima, colonization of newly available habitats enabled secondary contact between allopatric lineages from different refugia (Bernatchez & Wilson, ; Hewitt, ). Secondary contact between divergent lineages can have significant evolutionary consequences (Feder et al, ; Jay et al, ; Kirkpatrick & Barrett, ), and the genetic legacy of post‐glacial admixture and range expansion events is present in the modern genomes of many northern species (Bernatchez & Wilson, ; Garcia‐Elfring et al, ; Hewitt, ; Sim, Hall, Jex, Hegel, & Coltman, ; Wares & Cunningham, ).…”

“…The genomic consequences of these secondary contact events can depend on genomic architecture where differences in chromosomal structure (i.e., inversions and/or translocations) can act as post‐zygotic barriers to gene flow (Dobzhansky, ), leading to heterogeneous genomic introgression (Lohse, Clarke, Ritchie, & Etges, ). However, admixture can also introduce new chromosomal variants already shaped by selection (Dobzhansky, ; Kirkpatrick & Barrett, ), such as inversions in the Apple maggot ( Rhagoletis pomonella ) (Feder et al, ) or Robertsonian rearrangements in the house mouse ( Mus musculus domesticus ) (Searle, ), that can facilitate adaptive divergence, range expansions and ultimately speciation (Jay et al, ; Jónsson et al, ; Sinclair‐Waters et al, ). Limited karyotype data suggest that in North American Atlantic salmon, structural rearrangements have reduced the number of chromosome pairs from 29 to 27, including two chromosome fusions (Ssa08/Ssa29 and Ssa26/Ssa28) and one translocation with a fission (Ssa01p/Ssa23 and Ssa01q), although heterogeneity in the two fusion rearrangements has been reported (Brenna‐Hansen et al, ).…”