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

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. Yet, genomic data often omit 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 megabase-size 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 center of the hybrid zone. We propose that shared warning signaling (Müllerian mimicry) may couple the cline shifts seen in both species and facilitate the parallel coemergence of a novel hybrid morph in both comimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations.

A beginner's guide to low‐coverage whole genome sequencing for population genomics

“…Despite major technological advances, long-read sequencing that can recover haplotype information remains too costly for typical population genomic studies. However, the recent development of an affordable linked-read low-coverage sequencing approach (haplotagging; Meier et al, 2021) promises to open many new opportunities for haplotype-based inference on a population scale by enabling efficient phasing and imputation of low-coverage linked-read data without a reference panel. Phased haplotype data will provide substantial improvement in imputation performance compared to the short-insert lcWGS data explored in Box 4, and make completely new types of analysis possible with lcWGS data.…”

Supergene formation: evidence for recombination suppression among multiple functional loci within inversions

“…Because of this oligogenic control of mimetic colour pattern, crosses between different mimetic forms often result in the formation of recombinant, non-mimetic phenotypes. This is notably observed in the transition zones between the geographic ranges of distinct mimetic forms (22,26) and the recurrent formation of these poorly protected individuals is expected to favor the evolution of clusters of wing pattern loci (2,27). Consistent with this prediction, two independent inversions have been observed around cortex -a gene involved in wing patterning-in H. numata and H. pardalinus (28) and in H. sara, H. demeter, H. hecalesia and H. telesiphe, respectively (29).…”

Insights into invasive species from whole‐genome resequencing

“…Though linked-read sequencing approaches show great promise in population genomics (e.g., Lutgen et al, 2020), many platforms are currently prohibitively expensive. One notable exception is haplotagging, a recent low-cost linked-read sequencing method (Meier et al, 2021).…”