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Chromosomal rearrangements, such as inversions, have received considerable attention in the speciation literature due to their hampering effects on recombination. However, less is known about how other rearrangements, such as chromosome fissions and fusions, can affect the evolution of reproductive isolation. Here, we used crosses between populations of the wood white butterfly (Leptidea sinapis) with different karyotypes to identify genomic regions associated with hybrid inviability. We mapped candidate loci for hybrid inviability by contrasting allele frequencies between F2 hybrids that survived until the adult stage with individuals of the same cohort that succumbed to hybrid incompatibilities. Hybrid inviability factors were predominantly found in fast-evolving regions with reduced recombination rates, especially in regions where chromosome fusions have occurred. By analyzing sequencing coverage, we excluded aneuploidies as a direct link between hybrid inviability and chromosome fusions. Instead, our results point to an indirect relationship between hybrid inviability and chromosome fusions, possibly related to reductions in recombination rate caused by fusions. These results highlight that the extensive variation in chromosome numbers observed across the tree of life does not only distinguish species but can also be involved in speciation by being hotspots for the early evolution of postzygotic reproductive isolation.

Species frequently differ in the number and structure of chromosomes they harbor, but individuals that are heterozygous for chromosomal rearrangements may suffer from reduced fitness. Chromosomal rearrangements like fissions and fusions can hence serve as a mechanism for speciation between incipient lineages, but their evolution poses a paradox. How can rearrangements get fixed between populations if heterozygotes have reduced fitness? One solution is that this process predominantly occurs in small and isolated populations, where genetic drift can override natural selection. However, fixation is also more likely if a novel rearrangement is favored by a transmission bias, such as meiotic drive. Here, we investigate chromosomal transmission distortion in hybrids between two wood white (Leptidea sinapis) butterfly populations with extensive karyotype differences. Using data from two different crossing experiments, we uncover that there is a transmission bias favoring the ancestral chromosomal state for derived fusions, a result that shows that chromosome fusions actually can fix in populations despite being counteracted by meiotic drive. This means that meiotic drive not only can promote runaway chromosome number evolution and speciation, but also that it can be a conservative force acting against karyotypic change and the evolution of reproductive isolation. Based on our results, we suggest a mechanistic model for why chromosome fusion mutations may be opposed by meiotic drive and discuss factors contributing to karyotype evolution in Lepidoptera.

Background:  Regulation of transcription by DNA methylation in 5'-CpG-3' context is a widespread mechanism allowing differential expression of genetically identical cells to persist throughout development. Consequently, differences in DNA methylation can reinforce variation in gene expression among cells, tissues, populations, and species. Despite a surge in studies on DNA methylation, we know little about the importance of DNA methylation in population differentiation and speciation. Here we investigate the regulatory and evolutionary impact of DNA methylation in five tissues of two Ficedula flycatcher species and their naturally occurring F-1 hybrids.

Results: We show that the density of CpG in the promoters of genes determines the strength of the association between DNA methylation and gene expression. The impact of DNA methylation on gene expression varies among tissues with the brain showing unique patterns. Differentially expressed genes between parental species are predicted by genetic and methylation differentiation in CpG-rich promoters. However, both these factors fail to predict hybrid misexpression suggesting that promoter mismethylation is not a main determinant of hybrid misexpression in Ficedula flycatchers. Using allele-specific methylation estimates in hybrids, we also determine the genome-wide contribution of cis- and trans effects in DNA methylation differentiation. These distinct mechanisms are roughly balanced in all tissues except the brain, where trans differences predominate.

Conclusions:  Overall, this study provides insight on the regulatory and evolutionary impact of DNA methylation in songbirds.

Most species arise from the divergence of two populations within a species, but this is not only way speciation can occur. A new species can also evolve when diverging lineages hybridize and give rise to a persistent and ecologically differentiated species. Hybrid speciation in animals has been intensely debated, partly because hard evidence for the process have been difficult to gain. Recent access to large-scale, whole-genome sequencing data and development of novel analytical methods have made it more feasible to statistically test for hybrid origin of lineages. Here we report the discovery of a hybrid butterfly lineage. This lineage is mainly inhabiting an island in the Baltic Sea in Northern Europe and was previously described as a subspecies (horkei) of one of the parental species (Aricia artaxerxes). By analyzing whole-genome resequencing data, we conclude that horkei originated as a consequence of hybridization between A. artaxerxes and A. agestis. We show that this hybridization event occurred approximately 54,000 years ago, predating the last glaciation of the current distribution range. Horkei must therefore have persisted long enough to be able to colonize its current distribution range, despite that this range lies between the current ranges of the parental species. The hybrid origin, the maintenance of genomic integrity through time periods with dramatic climatic changes and the expression of a combination of parental traits - such as voltinism and host plant use - suggest that horkei can be considered a distinct species (Aricia horkei stat. nov.). Thus, we add to a growing list of hybrid speciation cases in animals.