The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena

Edelman

Mallet

2020

Preprint

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 H. 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 (H. hecale, H. elevatus and H. pardalinus) differences in genome size are mainly driven by a few restricted repetitive regions. Genes within these repeat regions show an increase in exon copy number, an absence of internal stop codons, evidence of constraint on non-synonymous changes, and increased expression, all of which suggest that 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 should aid further genetic and evolutionary studies in this genus.

Section: Resultssupporting

confidence: 60%

Synteny-based genome assembly for 16 species ofHeliconiusbutterflies, and an assessment of structural variation across the genus

Edelman

Mallet

2020

Preprint

“…The de novo assembly of Heliconius mitochondrial genomes enables the recovery of near-complete mitochondrial sequences (∼15 kb, typical of Heliconius— see, e.g., Massardo et al 2020 ) for all 16 species, including part of the mitochondrial DNA control region. A genealogy based on these mitochondrial genomes ( fig.…”

Section: Resultsmentioning

confidence: 99%

Synteny-Based Genome Assembly for 16 Species ofHeliconiusButterflies, and an Assessment of Structural Variation across the Genus

Genome Biology and Evolution

Edelman

Mallet

2021

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 H. 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 (H. hecale, H. elevatus and H. 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 non-synonymous 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.

“…However, the range of H. hecalesia does overlap with that of H. clysonymus and its sister species H. hortense in West Ecuador, the Colombian Andes, and Central America (Rosser et al 2012), and there are documented natural hybrids between H. hecalesia and both H. clysonymus and H. hortense (Mallet et al 2007). Previous phylogenetic studies showed that H. telesiphe forms a well-supported clade with H. clysonymus and H. hortense, nested within the erato clade (Kozak et al 2015;Massardo et al 2020). Therefore, it is likely that the signal from introgression loci in H. hecalesia might come from H. clysonymus, H. hortense, or any ancestral population of these three species.…”

Section: Evidence Of Introgression In the Wildmentioning

confidence: 99%

“…In this case, it did not seem to produce reliable inference of the species tree and introgression events, with considerable uncertainty surrounding the tree topology and the timing and direction of introgression events. Finally, Massardo et al (2020) analyzed the genome data from Edelman et al (2019) together with three additional genomes in both erato-sara and melpomene -silvaniform clades and inferred species trees using the same approach as in Edelman et al (2019).…”

Section: Introductionmentioning

confidence: 99%

Full-likelihood genomic analysis clarifies a complex history of species divergence and introgression: the example of theerato-saragroup ofHeliconiusbutterflies

Thawornwattana

Yang

et al. 2021

Preprint

Introgression plays a key role in adaptive evolution and species diversification in many groups of species including Heliconius butterflies. However, frequent hybridization and subsequent gene flow between species makes estimation of the species phylogeny challenging. Here, we infer species phylogeny and introgression events from whole-genome sequence data of six members of the erato-sara clade of Heliconius using a multispecies coalescent model with introgression (MSci) and an isolation-with-migration (IM) model. These approaches probabilistically capture the genealogical heterogeneity across the genome due to introgression and incomplete lineage sorting in a full likelihood framework. We detect robust signals of introgression across the genome, and estimate the direction, timing and magnitude of each introgression event. The results clarify several processes of speciation and introgression in the erato-sara group. In particular, we confirm ancestral gene flow between the sara clade and an ancestral population of H. telesiphe, a hybrid origin of H. hecalesia, and gene flow between the sister species H. erato and H. himera. The ability to confidently infer the presence, timing and magnitude of introgression events using genomic sequence data is helpful for understanding speciation in the presence of gene flow and will be useful for understanding the adaptive consequences of introgressed regions of the genome. Our analysis serves to highlight the power of full likelihood methods under the MSci model to the history of species divergence and cross-species introgression from genome-scale data.