Major improvements to the Heliconius melpomene genome assembly used to confirm 10 chromosome fusion events in 6 million years of butterfly evolution

Davey, John W.; Chouteau, Mathieu; Barker, Sarah L.; Maroja, Luana S.; Baxter, Simon W.; Simpson, Fraser; Joron, Mathieu; Mallet, James; Dasmahapatra, Kanchon K.; Jiggins, Chris D.

doi:10.1101/029199

Cited by 59 publications

(132 citation statements)

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“…We mapped a total of 109 Heliconius erato clade resequenced genomes to the Heliconius erato v1 reference genome (Van Belleghem et al., ) and 115 Heliconius melpomene clade genomes to the Heliconius melpomene v2 reference genome (Davey et al., ). These samples represent 20 H. erato clade and 16 H. melpomene clade populations covering nearly the entire geographic distribution of these species groups (Figure a and b).…”

Section: Resultsmentioning

confidence: 99%

“…Whole‐genome 100‐bp paired‐end Illumina resequencing data from H. erato and H. melpomene clade samples were aligned to the H. erato v1 (Van Belleghem et al., ) and H. melpomene v2 (Davey et al., ) reference genomes, respectively, using bwa v0.7 (Li, ). PCR duplicated reads were removed using picard v1.138 (http://picard.sourceforge.net) and sorted using samtools (Li et al., ).…”

Section: Methodsmentioning

confidence: 99%

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Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

et al. 2018

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Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a ‘large-X’ effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on the sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, i.e. ‘faster-X’, or barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply post-zygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of incompatibilities. Our work demonstrates the importance of taking demography into account in order to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

et al. 2018

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“…14,841 (73.8%) of the total number of genes in H. erato were assigned to an orthogroup, and 14,857 (68.6%) of the total number of genes in H. melpomene version Hmel2.5 were assigned to an orthogroup (Supporting Information Table S2). Conversely, the H. melpomene Hmel2 annotation has 13,019 predicted gene models (Davey et al., ). Using the Hmel2 annotation, OrthoFinder returned 9,320 clusters of genes, 6,846 of which included exactly one sequence per species (i.e., single‐copy orthogroups).…”

Section: Resultsmentioning

confidence: 99%

“…We established the linear model:

log (π_{italicnij}) \sim log (π_{italicnsj}) + chromosome_{type}_{j} + log (RPKM)

using r (v3.2.5). Chromosome type is either autosome or sex chromosome as assigned in Hmel2 reference genome (Davey et al., ). 477 genes with no polymorphism were removed from the analysis.…”

Section: Methodsmentioning

confidence: 99%

Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius

Pinharanda

Rousselle

Martin

et al. 2019

J of Evolutionary Biology

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Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution for a group of butterflies. First, we improve the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then, we analyse RNA from male and female whole abdomens and sequence female ovary and gut tissue to identify sex‐ and tissue‐specific gene expression profiles in H. melpomene. Using these expression profiles, we compare (a) sequence divergence and polymorphism; (b) the strength of positive and negative selection; and (c) rates of adaptive evolution, for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato. We show that the rate of adaptive substitutions is higher for Z than autosomal genes, but contrary to expectation, it is also higher for male‐biased than female‐biased genes. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic‐specific tissue. Our results contribute to a growing body of literature from other ZW systems that also provide mixed evidence for a fast‐Z effect where hemizygosity influences the rate of adaptive substitutions.

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“…The most recent review on the coevolution between passion vine butterflies and their host plants was written by Benson et al (1975), and the chemical basis of this process discussed by Spencer (1988). Since then, many new insights regarding the biology and phylogeny of Passiflora and heliconiines have been published, including genome sequencing of multiple Heliconius species (The Heliconius Consortium, 2012;Davey et al, 2016). This review covers both classical and recent findings concerning the arms race between Passiflora and heliconiines, describing the chemical and morphological defences of these plants against herbivory, and the butterflies' adaptations to counter these defences.…”

Section: Introductionmentioning

confidence: 99%

The arms race between heliconiine butterflies and Passiflora plants – new insights on an ancient subject

et al. 2017

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Heliconiines are called passion vine butterflies because they feed exclusively on Passiflora plants during the larval stage. Many features of Passiflora and heliconiines indicate that they have radiated and speciated in association with each other, and therefore this model system was one of the first examples used to exemplify coevolution theory. Three major adaptations of Passiflora plants supported arguments in favour of their coevolution with heliconiines: unusual variation of leaf shape within the genus; the occurrence of yellow structures mimicking heliconiine eggs; and their extensive diversity of defence compounds called cyanogenic glucosides. However, the protection systems of Passiflora plants go beyond these three features. Trichomes, mimicry of pathogen infection through variegation, and production of extrafloral nectar to attract ants and other predators of their herbivores, are morphological defences reported in this plant genus. Moreover, Passiflora plants are well protected chemically, not only by cyanogenic glucosides, but also by other compounds such as alkaloids, flavonoids, saponins, tannins and phenolics. Heliconiines can synthesize cyanogenic glucosides themselves, and their ability to handle these compounds was probably one of the most crucial adaptations that allowed the ancestor of these butterflies to feed on Passiflora plants. Indeed, it has been shown that Heliconius larvae can sequester cyanogenic glucosides and alkaloids from their host plants and utilize them for their own benefit. Recently, it was discovered that Heliconius adults have highly accurate visual and chemosensory systems, and the expansion of brain structures that can process such information allows them to memorize shapes and display elaborate pre-oviposition behaviour in order to defeat visual barriers evolved by Passiflora species. Even though the heliconiine-Passiflora model system has been intensively studied, the forces driving host-plant preference in these butterflies remain unclear. New studies have shown that host-plant preference seems to be genetically controlled, but in many species there is some plasticity in this choice and preferences can even be induced. Although much knowledge regarding the coevolution of Passiflora plants and heliconiine butterflies has accumulated in recent decades, there remain many exciting unanswered questions concerning this model system.

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Major improvements to the Heliconius melpomene genome assembly used to confirm 10 chromosome fusion events in 6 million years of butterfly evolution

Cited by 59 publications

References 53 publications

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius

The arms race between heliconiine butterflies and Passiflora plants – new insights on an ancient subject

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