Haplotype tagging reveals parallel formation of hybrid races in two butterfly species

Abstract

One-sentence summary:Haplotagging, a novel linked-read sequencing technique that enables whole genome haplotyping in large populations, reveals the formation of a novel hybrid race in parallel hybrid zones of two co-mimicking Heliconius butterfly species through strikingly parallel divergences in their genomes. Short title:Haplotagging reveals parallel formation of hybrid races Abstract Genetic variation segregates as linked sets of variants, or haplotypes. Haplotypes and linkage are central to genetics and underpin virtually all genetic and selection analysis. And yet, genomic data often lack haplotype information, due to constraints in sequencing technologies. Here we present "haplotagging", a simple, low-cost linked-read sequencing technique that allows sequencing of hundreds of individuals while retaining linkage information. We apply haplotagging to construct megabasesize haplotypes for over 600 individual butterflies (Heliconius erato and H. melpomene), which form overlapping hybrid zones across an elevational gradient in Ecuador. Haplotagging identifies loci controlling distinctive high-and lowland wing color patterns. Divergent haplotypes are found at the same major loci in both species, while chromosome rearrangements show no parallelism. Remarkably, in both species the geographic clines for the major wing pattern loci are displaced by 18 km, leading to the rise of a novel hybrid morph in the centre of the hybrid zone.We propose that shared warning signalling (Müllerian mimicry) may couple the cline shifts seen in both species, and facilitate the parallel co-emergence of a novel hybrid morph in both co-mimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations.

Genomics of altitude-associated wing shape in two tropical butterflies

“…1B, orange triangles). For the genomic analyses we used a large dataset from a nearby hybrid zone (Meier et al, 2020) (Fig. 1C).…”

“…We used 666 whole-genomes of H. erato (n=479) and H. melpomene (n=187) from a recent study (Meier et al, 2020), sequenced with 'haplotagging'. This linked-read sequencing technique retains long-range information via barcoding of DNA molecules before sequencing, which permits megabase-size haplotypes to be reconstructed computationally (Meier et al, 2020…”

“…To identify the genomic regions potentially controlling quantitative wing shape variation in these two Heliconius species, we performed genome-wide association mapping (GWAS, doAsso ANGSD). VCF files from Meier et al (2020) containing genotype likelihoods were used as input (-vcf-pl). We performed the GWAS with a generalized linear framework and a dosage model (-doAsso 6), which calculates the expected genotype from the input and implements a normal linear regression with the dosages as the predictor variable.…”

“…Decades of careful lab crosses described the inheritance of the colour pattern elements and identified the genes controlling them (Martin et al, 2012;Nadeau et al, 2016;Reed et al, 2011;Westerman et al, 2018). In the last decade, whole-genome sequencing in elevationally structured colour-morph hybrid zones has confirmed the role of these loci, which repeatedly diverge across highland and lowland colour pattern races (reverse genetics, Meier et al, 2020;Nadeau et al, 2014). Genome-wide association studies demonstrated that these diverging parts of the genome were associated with specific colour pattern elements.…”

“…Here we present the first study to examine the heritability and genomic basis of wing shape of two butterfly species in the wild. (Meier et al, 2020). B) Common-garden rearing protocol.…”