Evolution of hybrid inviability associated with chromosome fusions

Abstract

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. By contrasting allele frequencies between F2hybrids that survived until the adult stage with individuals of the same cohort that succumbed to hybrid incompatibilities, we show that candidate loci for hybrid inviability mainly are situated in fast-evolving regions with reduced recombination rates, especially in regions where chromosome fusions have occurred. Our results show that the extensive variation in chromosome numbers observed across the tree of life can be involved in speciation by being hotspots for the early evolution of postzygotic reproductive isolation.

Meiotic drive against chromosome fusions in butterfly hybrids

“…In a previous study, we mapped the genomic architecture of F 2 intercross hybrid inviability between the SWE and CAT chromosomal races of L. sinapis and observed a two-fold enrichment of candidate loci for hybrid inviability in derived fusion regions (Boman et al 2023). This means that both transmission distortion and hybrid inviability are associated with the same chromosomes regions in this system, a pattern that has not been observed before as far as we know.…”

“…The F 1 offspring were used to establish both an intercross (F 1 x F 1 , n = 8) and a backcross F 2 -generation (F 1 female x male SWE, n = 2). For the intercross F 2 individuals, we monitored individual survival to determine the genomic architecture of hybrid inviability (see Boman et al (2023), for more details). Here, all offspring (n = 599) were sampled, i.e.…”

“…We inferred fixed differences between the parental populations using population re-sequencing data from 10 SWE and 10 CAT male L. sinapis (Talla et al 2019). In-depth information on variant calling can be found in Boman et al (2023). Briefly, reads were trimmed and filtered and mapped to the Darwin Tree of Life reference genome assembly of a male L. sinapis from Asturias in north-west Spain, which is inferred to have a diploid chromosome number of 96 (Lohse et al 2022).…”

“…Most of the interpopulation differences in karyotype spring from derived chromosome fissions and fusions in the CAT and SWE population, respectively (Höök et al 2023) and there is a cline in chromosome number between these two extremes across Europe (Lukhtanov et al 2011). In spite of the remarkable amount of rearrangements, hybrids between SWE and CAT are fertile and viable with hybrid breakdown of viability in F 2 and later generations indicative of recessive hybrid incompatibilities (Lukhtanov et al 2018; Boman et al 2023). These characteristics make L. sinapis an excellent model system for investigating the underlying evolutionary processes leading to karyotypic divergence.…”