Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies

Abstract

Heliconius butterflies, a speciose genus of Müllerian mimics, represent a classic example of an adaptive radiation that includes a range of derived dietary, life history, physiological and neural traits. However, key lineages within the genus, and across the broader Heliconiini tribe, lack genomic resources, limiting our understanding of how adaptive and neutral processes shaped genome evolution during their radiation. Here, we generate highly contiguous genome assemblies for nine Heliconiini, 29 additional reference-assembled genomes, and improve 10 existing assemblies. Altogether, we provide a dataset of annotated genomes for a total of 63 species, including 58 species within the Heliconiini tribe. We use this extensive dataset to generate a robust and dated heliconiine phylogeny, describe major patterns of introgression, explore the evolution of genome architecture, and the genomic basis of key innovations in this enigmatic group, including an assessment of the evolution of putative regulatory regions at the Heliconius stem. Our work illustrates how the increased resolution provided by such dense genomic sampling improves our power to generate and test gene-phenotype hypotheses, and precisely characterize how genomes evolve.

Evolution of larval gregariousness is associated with host plant specialisation, but not host morphology, in Heliconiini butterflies

“…We obtained two lists of 52 and 75 butterfly species within the Heliconiini tribe from phylogenies used in Cicconardi et al (2023) and Kozak et al (2015), respectively. Kozak et al's phylogeny was used for the primary analyses, as this incorporates a larger total number of species (Figure 1a).…”

“…We performed all our main analyses on an additional, separate Heliconiini phylogeny (Cicconardi et al, 2023). Overall, we recorded 19 gregarious species, out of 57 included in Cicconardi et al (2023).…”

“…We performed all our main analyses on an additional, separate Heliconiini phylogeny (Cicconardi et al, 2023). Overall, we recorded 19 gregarious species, out of 57 included in Cicconardi et al (2023). Our model estimated eight independent transitions to gregariousness, and the phylogenetic signal of social behaviour is estimated to be very strong (λ = 1.0).…”

“…Although little is known about the behavioural mechanisms supporting these aggregations, at least some gregarious Heliconiini are trail followers (Pescador-Rubio et al, 2011), suggesting these transitions reflect behavioural adaptations in larvae rather than simple variation in female egg laying. This variation, coupled with tribe-wide estimates of the phylogenetic structure of the Heliconiini (Cicconardi et al, 2023;Kozak et al, 2015), positions these butterflies as a highly useful system with which to study behavioural evolution in response to host plant ecology.…”

Ecological diversification in an adaptive radiation of plants: the role of de novo mutation and introgression

“…Given that introgressed genetic material may confer fitness effects and can be subject to strong selection, particularly in functionally important genomic regions (Moran et al 2021), signatures of introgression are expected to be distributed heterogeneously across the genome (Harrison and Larson 2016;Martin and Jiggins 2017). Introgression may provide a source of genetic diversity in adaptive radiations (Edelman and Mallet 2021), and although its importance in this context has historically been somewhat controversial (Seehausen 2004), many recent efforts have highlighted the myriad ways in which introgression may effectively broaden the genomic substrate for adaptation through novel combinations of haplotypes (e.g., McGee et al 2020;Ferreira et al 2021;Ronco et al 2021;De-Kayne et al 2022;Suvorov et al 2022;Cicconardi et al 2023;Marcionetti and Salamin 2023). In addition to widespread ILS and introgression, radiations also often feature patterns of repeated evolution, which may be either the result of the adaptive introgression of beneficial alleles or independent (convergent) adaptation in disparate lineages to similar ecological conditions.…”