Chromosome Fissions and Fusions Act as Barriers to Gene Flow betweenBrenthisFritillary Butterflies

Abstract

Chromosome rearrangements are thought to promote reproductive isolation between incipient species. However, it is unclear how often, and under what conditions, fission and fusion rearrangements act as barriers to gene flow. Here we investigate speciation between two largely sympatric fritillary butterflies, Brenthis daphne and B. ino. We use a composite likelihood approach to infer the demographic history of these species from whole genome sequence data. We then compare chromosome-level genome assemblies of individuals from each species and identify a total of nine chromosome fissions and fusions. Finally, we fit a demographic model where effective population sizes and effective migration rate vary across the genome, allowing us to quantify the effects of chromosome rearrangements on reproductive isolation. We show that chromosomes involved in rearrangements experienced less effective migration since the onset of species divergence and that genomic regions near rearrangement points have a further reduction in effective migration rate. Our results suggest that the evolution of multiple rearrangements in the B. daphne and B. ino populations, including alternative fusions of the same chromosomes, have resulted in a reduction in gene flow. While fission and fusion of chromosomes are unlikely to be the only processes that have led to speciation between these butterflies, this study shows that these rearrangements can directly promote reproductive isolation and may be involved in speciation when karyotypes evolve quickly.

Inferring inter-chromosomal rearrangements and ancestral linkage groups from synteny

“…Additionally, while the importance of fissions and fusions in speciation is becoming clearer (Yoshida et al . 2023; Mackintosh et al . 2023), we still have an incomplete understanding of exactly how such rearrangements prevent gene flow.…”

“…2023), we still have an incomplete understanding of exactly how such rearrangements prevent gene flow. Identifying inter-chromosomal rearrangements across species and populations will be the first step in answering these biological questions, and it is encouraging that our synteny-based method has already been used to generate new results about genome evolution (Mackintosh et al . 2023; Wright et al .…”

“…Additionally, while the importance of fissions and fusions in speciation is becoming clearer (Yoshida et al 2023;Mackintosh et al 2023), we still have an incomplete understanding of exactly how such rearrangements prevent gene flow. Identifying inter-chromosomal rearrangements across species and populations will be the first step in answering these biological questions, and it is encouraging that our synteny-based method has already been used to generate new results about genome evolution (Mackintosh et al 2023;Wright et al 2023). We anticipate that a variety of methods, focusing on different rearrangements types and relying on different inference procedures, will be required to investigate genome evolution across the tree of life and improve our understanding of the role of chromosome rearrangements in evolution.…”

“…2023), as well as broader processes like speciation (Yoshida et al . 2023; Mackintosh et al . 2023), so there is considerable interest in reconstructing how genomes have rearranged through time.…”

Genome architecture of an exceptionally invasive copepod crossing salinity boundaries

“…For instance, chromosome number variation in copepods is on par with the levels of variation found in vertebrates and insects [48,49,64]. The high variance in chromosome number in copepods suggests an evolutionary history of chromosomal fusions and fissions [65] and associated genomic rearrangements [66]. Such genomic rearrangements might explain the low levels of synteny we found among copepod genomes (Additional file 1: Fig.…”