Abstract
Heliconius butterflies (Lepidoptera: Nymphalidae) are a group of 48 neotropical species widely studied in evolutionary research. Despite the wealth of genomic data generated in past years, chromosomal level genome assemblies currently exist for only two species, Heliconius melpomene and Heliconius erato, each a representative of one of the two major clades of the genus. Here, we use these reference genomes to improve the contiguity of previously published draft genome assemblies of 16 Heliconius species. Using a reference-assisted scaffolding approach, we place and order the scaffolds of these genomes onto chromosomes, resulting in 95.7–99.9% of their genomes anchored to chromosomes. Genome sizes are somewhat variable among species (270–422 Mb) and in one small group of species (Heliconius hecale, Heliconius elevatus, and Heliconius pardalinus) expansions in genome size are driven mainly by repetitive sequences that map to four small regions in the H. melpomene reference genome. Genes from these repeat regions show an increase in exon copy number, an absence of internal stop codons, evidence of constraint on nonsynonymous changes, and increased expression, all of which suggest that at least some of the extra copies are functional. Finally, we conducted a systematic search for inversions and identified five moderately large inversions fixed between the two major Heliconius clades. We infer that one of these inversions was transferred by introgression between the lineages leading to the erato/sara and burneyi/doris clades. These reference-guided assemblies represent a major improvement in Heliconius genomic resources that enable further genetic and evolutionary discoveries in this genus.
Highlights
Advances in sequencing technology have revolutionized the field of evolutionary biology
We conducted a systematic search for inversions and identified five moderately large inversions fixed between the two major Heliconius clades
The proportion of reference-guided assembly length anchored to chromosomes was higher in assemblies guided by the genome of the phylogenetically closest species, H. doris being the only exception. This species is distant from both reference genomes, but has been inferred to be phylogenetically closer to H. melpomene (Edelman et al, 2019; Kozak et al, 2018; Kozak et al, 2015). It shows a 0.2% higher proportion of the assembly length included in scaffolds anchored to chromosomes using H. erato demophoon as the reference, likely because the larger genome of H. erato contains ancestral sequence that was lost by the smaller H. melpomene genome but retained in the early branching H. doris
Summary
Advances in sequencing technology have revolutionized the field of evolutionary biology. Generating short-read genomic datasets is common practice, enabling investigation of fundamental evolutionary processes including the genetic basis of adaptive traits, dynamics of selection on particular alleles, and demographic histories of populations. In order to exploit the power of low-cost short-read data, one must usually align reads to a reference genome. The availability of high-quality reference genomes can determine the breadth and power of comparative and population genomic analyses in evolutionary studies. Placing genome scaffolds on chromosomes allows one to contrast patterns between autosomes and sex chromosomes which has been important for understanding speciation (Coyne and Orr 1989; Coyne 2018; Prowell 1998; Masly and Presgraves 2007; Fontaine et al 2015; Ellegren et al 2012; Seixas et al 2018; Martin et al 2019). Chromosome-level assemblies have been shown to greatly improve the power and resolution of genome-wide association and QTL studies (Benevenuto et al 2019; Markelz et al 2017)
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