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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.

SUBMITTER: Meier JI

PROVIDER: S-EPMC8237668 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Recent studies on insect interactions on plants have revealed that herbivorous insects indirectly interact with each other through changes in plant traits following herbivory. However, less attention has been given to plant biomass relative to plant quality in relation to indirect interactions among herbivores. We explored the extent to which the larval food demand of two specialist butterflies (Sericinus montela and Atrophaneura alcinous) explains their interaction on a host plant, Aristolochia debilis. A laboratory experiment showed that plant mass consumption by A. alcinous larvae was 2.6 times greater than that by S. montela. We predicted that A. alcinous, which requires more food, is more vulnerable to food shortages than S. montela. In a cage experiment, an asymmetric interspecific interaction was detected between the two specialist butterflies; S. montela larval density significantly decreased the survival and prolonged the development time of A. alcinous, but A. alcinous density affected neither the survival nor the development time of S. montela. The prediction based on the food requirement was partly supported by the fact that increasing A. alcinous density likely caused a food shortage, which more negatively affected A. alcinous survival than S. montela survival. Conversely, increasing the density of S. montela did not reduce the remaining food quantity, suggesting that the negative effect of S. montela density on A. alcinous was unlikely to be due to food shortage. Although aristolochic acid I, a defensive chemical specific to Aristolochia plants, did not influence the food consumption or growth of either butterfly larva, unmeasured attributes of plant quality may have mediated an indirect interaction between the two butterflies. Consequently, our study suggests that not only the quality but also the quantity of plants should be considered to fully understand the characteristics, such as symmetry, of interspecific interactions among herbivorous insects on the same host plant.

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

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