Lack of gene flow: Narrow and dispersed differentiation islands in a triplet of Leptidea butterfly species

Abstract

Genome scans in recently separated species can inform on molecular mechanisms and evolutionary processes driving divergence. Large‐scale polymorphism data from multiple species pairs are also key to investigate the repeatability of divergence—whether radiations tend to show parallel responses to similar selection pressures and/or underlying molecular forces. Here, we used whole‐genome resequencing data from six wood white (Leptidea sp.) butterfly populations, representing three closely related species with karyomorph variation, to infer the species' demographic history and characterize patterns of genomic diversity and differentiation. The analyses supported previously established species relationships, and there was no evidence for postdivergence gene flow. We identified significant intraspecific genetic structure, in particular between karyomorph extremes in the wood white (L. sinapis)—a species with a remarkable chromosome number cline across the distribution range. The genomic landscapes of differentiation were erratic, and outlier regions were narrow and dispersed. Highly differentiated (FST) regions generally had low genetic diversity (θπ), but increased absolute divergence (DXY) and excess of rare frequency variants (low Tajima's D). A minority of differentiation peaks were shared across species and population comparisons. However, highly differentiated regions contained genes with overrepresented functions related to metabolism, response to stimulus and cellular processes, indicating recurrent directional selection on a specific set of traits in all comparisons. In contrast to the majority of genome scans in recently diverged lineages, our data suggest that divergence landscapes in Leptidea have been shaped by directional selection and genetic drift rather than stable recombination landscapes and/or introgression.

Evolution of multiple sex-chromosomes associated with dynamic genome reshuffling in Leptidea wood-white butterflies

“…The three Leptidea species showed a considerably lower level of genome-wide diversity than most other butterflies examined, indicating reduced effective population sizes (Talla et al 2019b). They also showed a significantly reduced genetic diversity on the 'ancestral' Z-linked genes (corresponding to Z 1 in this study, multiple Z-chromosomes were not considered) and a significantly higher level of genetic differentiation on the 'ancestral' Z-linked genes in comparison with the 'ancestral' autosomal genes (Talla et al 2019a). Especially the latter results are consistent with the so-called 'Faster-Z effect', which means that the sexlinked genes are subjected to a faster rate of evolution (Mank et al 2010).…”

“…Z and W chromosomes are coloured grey and black, respectively. The phylogenetic relationships and estimated divergence times (My, million years) between the species are shown below the lower panel (Šíchová et al 2015 ; Talla et al 2017 , 2019a ). …”

Genomic differentiation across the speciation continuum in three hummingbird species pairs

“…Calculating d xy across the genome and locating F ST peaks that are associated with elevated d xy can help narrow down the potential causes of some islands of divergence (e.g. [18,[31][32][33][34]).…”

Incomplete Sterility of Chromosomal Hybrids: Implications for Karyotype Evolution and Homoploid Hybrid Speciation

“…Within this species, the diploid chromosome number gradually decreases from 2n = 106, 108 in north-eastern Spain to 2n = 56 in eastern Kazakhstan, and to 2n = 57, 58 in south-eastern Sweden (Lukhtanov et al, 2018). This cline was likely generated due to the secondary contact of two chromosomally diverged populations (Talla et al, 2019). The intraspecific nature of the extreme level of variability in chromosome number within this clade is supported by genetic and morphological data, as well as by mating experiments (Lukhtanov et al, 2011;Dincȃ et al, 2013).…”

“…Chromosomal Cline in Nature: On the Way to HHS The L. sinapis butterfly displays a chromosomal cline with diploid chromosomal numbers ranging from 2n = 106, 108 in Spain to 2n = 56 in Kazakhstan, and to 2n = 57, 58 in Sweden (Lukhtanov et al, 2018). This cline was most likely produced due to the secondary contact of two chromosomally diverged parental populations (Talla et al, 2019). The laboratory experimental data we obtained make it possible to advance hypotheses about how this cline originated and is maintained.…”