The genome sequence of the lesser marbled fritillary, <i>Brenthis ino</i>, and evidence for a segregating neo-Z chromosome

Mackintosh, Alexander; Laetsch, Dominik R.; Baril, Tobias; Foster, Robert G.; Dincă, Vlad; Vila, Roger; Hayward, Alex; Lohse, Konrad

doi:10.1101/2021.12.16.472906

Cited by 4 publications

(13 citation statements)

References 57 publications

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“…While 34 chromosome pairs have been observed in Brenthis hecate spermatocytes (de Lesse 1961; Saitoh and Lukhtanov 1988), B. daphne and B. ino are reported to have only 12 -14 pairs of chromosomes (Maeki and Makino 1953;Saitoh et al 1989;Federley 1938;Saitoh 1987Saitoh , 1991. We recently assembled a B. ino reference genome (Mackintosh et al 2022) with 14 pairs of chromosomes. We found that a male individual was heterozygous for a neo-Z chromosome fusion and that the genome was highly rearranged compared to the ancestral nymphalid karyotype.…”

Section: Introductionmentioning

confidence: 99%

Chromosome fissions and fusions act as barriers to gene flow betweenBrenthisfritillary butterflies

Mackintosh

Vila

Laetsch

et al. 2022

Preprint

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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 daphneandB. 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 theB. daphneandB. inopopulations, 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.

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Section: Introductionmentioning

confidence: 99%

Chromosome fissions and fusions act as barriers to gene flow betweenBrenthisfritillary butterflies

Mackintosh

Vila

Laetsch

et al. 2022

Preprint

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“…The results of fusions between the ancestral sex chromosomes and autosomes are called neo-sex chromosomes (White, 1973; Hejníčková et al, 2021). Neo-Z chromosomes have been repeatedly described as occurring sporadically among different groups of Lepidoptera (Nguyen et al, 2013; Mongue et al, 2017; Mackintosh et al, 2021). More rarely, such sex chromosome – autosome fusions can be fixed in evolution and be the ancestors of entire phylogenetic lineages (Nguyen et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…The situation has changed quite recently due to the use of chromosome-level genome assemblies for karyotype analysis (Huang et al, 2022; Wang et al, 2022). This led to the first attempts to analyze rapid karyotypic evolution in different groups (Mudd et al, 2020; Yin et al, 2021), including Lepidoptera (Hill et al, 2019; Cicconardi et al, 2021; Mackintosh et al, 2021). However, to the best of our knowledge, no one has studied groups of organisms in which both evolutionary trends (chromosomal conservatism and chromosomal megaevolution) occur simultaneously.…”

Section: Introductionmentioning

confidence: 99%

Chromosomal conservatism vs chromosomal megaevolution: enigma of karyotypic evolution in Lepidoptera

Pazhenkova

Lukhtanov

2022

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In the evolution of many organisms, periods of very slow genome reorganization (=chromosomal conservatism) are interrupted by bursts of numerous chromosomal changes (=chromosomal megaevolution). However, the patterns, mechanisms, and consequences of conservative and rapid chromosomal evolution are still poorly understood and widely discussed. Here we show that in blue butterflies (Lepidoptera: Lycaenidae), the periods of chromosome number conservatism are characterized by the real stability of most autosomes and the highly dynamic evolution of the sex chromosome Z, which, due to autosome-sex chromosome fusions and fissions, is carried out according to the cycle Z=>NeoZ1=>Z=>NeoZ2=> Z=>NeoZ3. These fusions and fissions result in a fluctuation of chromosomal number around the ancestral value, a phenomenon previously observed (but not explained) in numerous groups of Lepidoptera. In the phase of chromosomal megaevolution, the explosive increase in the chromosome number occurs mainly due to simple chromosomal fissions, in some cases complicated by autosomal translocations. Interestingly, these translocations are not random and found to occur only between fragmented chromosomes originated from the same primary linkage group. We also found that the Z chromosomes of two closely related Lysandra species are differentiated by a large inversion. We argue that the special role of sex chromosomes in speciation can be reinforced via sex chromosome - autosome fusion. The cycles of fusions and fissions of sex chromosomes with autosomes, such as those found in the blue butterflies, indicate that the species divergence driven by neo-Z chromosome formation is widely distributed in Lepidoptera.

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“…Two male individuals (MO IP 500 and MO IP 504) were collected with a hand net at Le Moulin de Bertrand, Saint-Martin-de-Londres, Montpellier, France and flash frozen in liquid nitrogen. High-molecular-weight (HMW) DNA was extracted from the thorax of one of these individuals (MO IP 504) using a salting out extraction protocol as described in Mackintosh et al . (2021).…”

Section: Methodsmentioning

confidence: 99%

“…Transposable elements (TEs) were annotated using the Earl Grey TE annotation pipeline (https://github. com/TobyBaril/EarlGrey, Baril et al 2021;Platt et al 2016;Wong and Simakov 2018;Smit et al 2015;Xu and Wang 2007;Ou and Jiang 2019;Rubino and Creevey 2014;Jurka et al 2005;Hubley et al 2015;Flynn et al 2020) as in Mackintosh et al (2021).…”

Section: Genome Annotationmentioning

confidence: 99%

The genome sequence of the scarce swallowtail, Iphiclides podalirius

Mackintosh

Laetsch

Baril

et al. 2022

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The scarce swallowtail, Iphiclides podalirius (Linnaeus, 1758), is a species of butterfly in the family Papilionidae. Here we present a chromosome-level genome assembly for I. podalirius as well as gene and transposable element annotations. We estimate heterozygosity within different partitions of the genome and find a negative correlation between chromosome length and heterozygosity at fourfold-degenerate sites. This high quality genome assembly, the first for any species in the tribe Leptocircini, will be a valuable resource for population genomics in the genus Iphiclides and comparative genomics more generally.

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The genome sequence of the lesser marbled fritillary, Brenthis ino, and evidence for a segregating neo-Z chromosome

Cited by 4 publications

References 57 publications

Chromosome fissions and fusions act as barriers to gene flow betweenBrenthisfritillary butterflies

Chromosome fissions and fusions act as barriers to gene flow betweenBrenthisfritillary butterflies

Chromosomal conservatism vs chromosomal megaevolution: enigma of karyotypic evolution in Lepidoptera

The genome sequence of the scarce swallowtail, Iphiclides podalirius

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