The Dryas iulia Genome Supports Multiple Gains of a W Chromosome from a B Chromosome in Butterflies

Abstract

In butterflies and moths, which exhibit highly variable sex determination mechanisms, the homogametic Z chromosome is deeply conserved and is featured in many genome assemblies. The evolution and origin of the female W sex chromosome, however, remains mostly unknown. Previous studies have proposed that a ZZ/Z0 sex determination system is ancestral to Lepidoptera, and that W chromosomes may originate from sex-linked B chromosomes. Here, we sequence and assemble the female Dryas iulia genome into 32 highly contiguous ordered and oriented chromosomes, including the Z and W sex chromosomes. We then use sex-specific Hi-C, ATAC-seq, PRO-seq, and whole genome DNA sequence datasets to test if features of the D. iulia W chromosome are consistent with a hypothesized B chromosome origin. We show that the putative W chromosome displays female-associated DNA sequence, gene expression, and chromatin accessibility to confirm the sex-linked function of the W sequence. In contrast with expectations from studies of homologous sex chromosomes, highly repetitive DNA content on the W chromosome, the sole presence of domesticated repetitive elements in functional DNA, and lack of sequence homology with the Z chromosome or autosomes is most consistent with a B chromosome origin for the W, although it remains challenging to rule out extensive sequence divergence. Synteny analysis of the D. iulia W chromosome with other female lepidopteran genome assemblies shows no homology between W chromosomes and suggests multiple, independent origins of the W chromosome from a B chromosome likely occurred in butterflies.

Evolution of B Chromosomes: From Dispensable Parasitic Chromosomes to Essential Genomic Players

“…However, a possibility that at least in Tischeriidae W chromosome evolved from the fusion of a Z chromosome and an autosome has not been ruled out ( Dalíková et al, 2017 ; Hejníčková et al, 2019 ). Recent data from genome sequencing in another butterfly species Dryas iulia (tribe Heliconiini) support the origin of a W sex chromosome from a B chromosome and suggest that this event may have happened multiple times during the evolution of butterflies ( Lewis et al, 2021 ). It has also been proposed that the ancestral Y chromosome in Drosophila may have originated from a B chromosome ( Hackstein et al, 1996 ; Carvalho, 2002 ).…”

“…Based on these findings, it has been proposed that the effects of B chromosomes on their host may shift back and forth from parasitic or neutral to beneficial ( Camacho et al, 2000 ). In some species, it has been even hypothesised that B chromosomes may became an essential, stable part of the genome turning, for example, into new sex chromosomes or chromosomes restricted to germline that became essential for viability and fertility of their carriers ( Carvalho, 2002 ; Nokkala et al, 2003 ; Dalíková et al, 2017 ; Torgasheva et al, 2019 ; Imarazene et al, 2021 ; Lewis et al, 2021 ). In this review we describe mechanisms of B chromosome origin, strategies of their inheritance and give examples of the “cellular domestication” of B chromosomes, where these chromosomes provide some important functions for their hosts.…”

“…The second model (White, 1973) proposed that B chromosomes may be maintained in the population without drive mechanisms if they have a beneficial effect on their carriers in small numbers but start to be detrimental in high copy numbers. Empirical data reviewed in this paper supports both models providing evidence for the selfish spread of B chromosomes in populations through drive in many species ( Hasegawa, 1934 ; Nur, 1962 ; Nur, 1963 ; Rutishauser and Rӧthlisberger, 1966 ; Nur, 1969 ; Kayano, 1971 ; Jones and Rees, 1982 ; Gregg at al., 1984 ; Murray, 1984 ; Viseras et al, 1990 ; Jones, 1991 ; Pardo et al, 1995 ; Houben, 2017 ; Jones, 2018 ; Clark and Kocher, 2019 ; Blavet et al, 2021 ) as well as identifying beneficial effects of B chromosomes for their hosts ( Williams, 1970 ; Dherawattana and Sadanaga, 1973 ; Rees and Hutchinson, 1974 ; Holmes and Bougourd, 1989 ; Miao et al, 1991 ; Plowman and Bougourd, 1994 ; Enkerli et al, 1997 ; Hatta et al, 2002 ; Nokkala et al, 2003 ; Rodriguez-Carres et al, 2008 ; Akagi et al, 2009 ; Coleman et al, 2009 ; Ma et al, 2010 ; Balesdent et al, 2013 ; Thatcher et al, 2016 ; Williams et al, 2016 ; Dalíková et al, 2017 ; Pereira et al, 2017 ; van Dam et al, 2017 ; Armitage et al, 2018 ; Kinsella et al, 2019 ; Torgasheva et al, 2019 ; Imarazene et al, 2021 ; Lewis et al, 2021 ). From the example in rye where B chromosomes have beneficial function but are still driving ( Pereira et al, 2017 ) we see that there could be even co-occurrence of drive and beneficial function which indicates the rather extensive complexity of B chromosome evolution.…”

Linkage mapping and genome annotation give novel insights into gene family expansions and regional recombination rate variation in the painted lady (Vanessa cardui) butterfly

“…While having a size equal to an average autosome, the W-chromosome demonstrated very specific features; both a significantly higher overall proportion of TEs, a larger fraction of longer TEs, and a different distribution of repeat classes compared to other chromosomes. Similar to the silkmoth and julia heliconian (Dryas iulia), the W-chromosome in the painted lady had a significantly higher proportion of LTRs and LINEs (Lewis et al, 2021;Mita et al, 2004). The proportion of SINEs was however much smaller on the W-chromosome than on the autosomes and the Zchromosome.…”

Highlight—Epigenetics Virtual Issue: New Findings Amid Old Controversies

“…However, the authors found that these mobile elements were not restricted to the W chromosome and that they exhibited stage-, sex-, pairing-, gonad-, and strain-specific transcription. As explained in the Highlight feature on this article ( McGrath 2021a ), the authors hypothesize that W elements “not only influence the biology of S. mansoni , but they might represent one of the sources of heritable variability, thus shaping the evolution of the family Schistosomatidae.” In another study of W chromosome repeats, Stephen H. Montgomery and coauthors describe the W chromosome in the butterfly Dryas iulia , which exhibits female-specific gene expression and chromatin accessibility and is characterized by highly repetitive DNA content ( Lewis et al 2021 ). Their findings suggest that the evolution of the W chromosome in this species may have been heavily driven by repetitive elements and that these elements may have originated from a B chromosome, a nonessential chromosome with variable presence within populations.…”