Multiple chromosomal rearrangements in a hybrid zone betweenLittorina saxatilisecotypes

Abstract

Both classical and recent studies suggest that chromosomal inversion polymorphisms are important in adaptation and speciation. However, biases in discovery and reporting of inversions make it difficult to assess their prevalence and biological importance. Here, we use an approach based on linkage disequilibrium among markers genotyped for samples collected across a transect between contrasting habitats to detect chromosomal rearrangements de novo. We report 17 polymorphic rearrangements in a single locality for the coastal marine snail, Littorina saxatilis . Patterns of diversity in the field and of recombination in controlled crosses provide strong evidence that at least the majority of these rearrangements are inversions. Most show clinal changes in frequency between habitats, suggestive of divergent selection, but only one appears to be fixed for different arrangements in the two habitats. Consistent with widespread evidence for balancing selection on inversion polymorphisms, we argue that a combination of heterosis and divergent selection can explain the observed patterns and should be considered in other systems spanning environmental gradients.

The effect of genetic architecture and selfing on the capacity of a population to expand its range

“…Chromosomal inversions have frequently been implicated in promoting range expansions. For example, this has been empirically observed in species such as threespine stickleback (Gasteroseteus aculeatus; Jones et al 2012), yellow monkeyflower (Mimulus guttatus; Lowry and Willis 2010), rough periwinkle (Littorina saxatilis; Johannesson et al 2017;Westram et al 2018;Faria et al 2019) and red imported fire ant (Solenopsis invicta; Tsutsui and Suarez 2003;Wang et al 2013). Our results that are pertinent to reduced recombination in general, are likely to also be applicable to inversions.…”

Is embryo abortion a post‐zygotic barrier to gene flow between Littorina ecotypes?

“…LGC6.1/2, LGC14.1/2 and LGC17.1 (Faria, Chaube, et al, 2019a) that showed strong and consistent clines at the three study sites (A.M. Westram, R. Faria, K. Johannesson, R.K. Butlin, unpublished data). We calculated inversion heterozygosity as the proportion of the inversions that were heterokaryotypic in each female.…”

“…Individuals that had genotype data for fewer than 50 SNPs after this filtering were excluded. We also considered the effect of genotype for each of five inversions LGC1.1, LGC2.1, LGC6.1/2, LGC14.1/2 and LGC17.1 (Faria, Chaube, et al, ) that showed strong and consistent clines at the three study sites (A.M. Westram, R. Faria, K. Johannesson, R.K. Butlin, unpublished data). We calculated inversion heterozygosity as the proportion of the inversions that were heterokaryotypic in each female.…”

“…Incompatibilities, if present, might have evolved as by-products of strong divergent selection under gene flow (Kulmuni & Westram, 2017) and/or during short periods of allopatry (Bierne, Welch, Loire, Bonhomme, & David, 2011). Furthermore, several large and presumably old inversions segregate between ecotypes (Faria, Chaube, et al, 2019a;Morales et al, 2019;Westram et al, 2018) and these might have generated additional opportunities for DMIs to evolve as by-products of divergent selection, or during earlier periods of isolation.…”

Genomic architecture of parallel ecological divergence: beyond a single environmental contrast

“…In particular, chromosomal inversions, which suppress recombination in heterozygotes, may facilitate adaptive divergence by maintaining sets of co-adapted alleles (18)(19)(20). Inversions can act as reservoirs of adaptive standing variation and as vehicles to redistribute adaptive variation by gene flow, thus promoting parallel divergence with a shared genetic basis (21)(22)(23)(24). On the other hand, inversions can confound inferences of the genetic basis of parallel divergence because they can modify apparent genetic sharing by capturing neutral loci within large haplotype blocks.…”