Neil Rosser

Sequencing of the genome of the butterfly Heliconius melpomene shows that closely related Heliconius species exchange protective colour-pattern genes promiscuously. Heliconius butterflies are an excellent system in which to study ecology, behaviour, mimicry and speciation. The genome of the postman butterfly Heliconius melpomene has now been sequenced. Using genomic resequencing of individuals from distinct lineages, the authors document heterogenous patterns of genomic diversity associated with adaptively divergent wing-colour patterns. As the second lepidopteran genome to be sequenced, Heliconius offers novel opportunities for comparative genomics within this economically significant insect order, which includes many pest species, as well as the only domesticated insect, the silkmoth Bombyx mori. The evolutionary importance of hybridization and introgression has long been debated1. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation2,3,4,5. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

Research into Heliconius butterflies has made a significant contribution to evolutionary biology. Here, we review our understanding of the diversification of these butterflies, covering recent advances and a vast foundation of earlier work. Whereas no single group of organisms can be sufficient for understanding life's diversity, after years of intensive study, research into Heliconius has addressed a wide variety of evolutionary questions. We first discuss evidence for widespread gene flow between Heliconius species and what this reveals about the nature of species. We then address the evolution and diversity of warning patterns, both as the target of selection and with respect to their underlying genetic basis. The identification of major genes involved in mimetic shifts, and homology at these loci between distantly related taxa, has revealed a surprising predictability in the genetic basis of evolution. In the final sections, we consider the evolution of warning patterns, and Heliconius diversity more generally, within a broader context of ecological and sexual selection. We consider how different traits and modes of selection can interact and influence the evolution of reproductive isolation.

Animals that cooperate with nonrelatives represent a challenge to inclusive fitness theory, unless cooperative behavior is shown to provide direct fitness benefits. Inheritance of breeding resources could provide such benefits, but this route to cooperation has been little investigated in the social insects. We show that nest inheritance can explain the presence of unrelated helpers in a classic social insect model, the primitively eusocial wasp Polistes dominulus. We found that subordinate helpers produced more direct offspring than lone breeders, some while still subordinate but most after inheriting the dominant position. Thus, while indirect fitness obtained through helping relatives has been the dominant paradigm for understanding eusociality in insects, direct fitness is vital to explain cooperation in P. dominulus.

We compiled a large database of 58 059 point locality records for 70 species and 434 subspecies of heliconiine butterflies and used these data to test evolutionary hypotheses for their diversification. To study geographical patterns of diversity and contact zones, we mapped: (1) species richness; (2) mean molecular phylogenetic terminal branch length; (3) subspecies richness and the proportion of specimens that were subspecific hybrids, and (4) museum sampling effort. Heliconiine species richness is high throughout the Amazon region and peaks near the equator in the foothills and middle elevations of the eastern Andes. Mean phylogenetic terminal branch length is lowest in the eastern Andes and tends to be low in species-rich areas. By contrast, areas of high subspecies richness, where subspecies overlap in range and/or hybridize, are concentrated along the course of the Amazon River, with the eastern Andes slopes and foothills relatively depauperate in terms of local intraspecific phenotypic diversity. Spatial gradients in heliconiine species richness in the Neotropics are consistent with the hypothesis that species richness gradients are driven at least in part by variation in speciation and/or extinction rates, resulting in observed gradients in mean phylogenetic branch length, rather than via evolutionary age or niche conservatism alone. The data obtained in the present study, coupled with individual case studies of recently evolved Heliconius species, suggest that the radiation of heliconiine butterflies occurred predominantly on the eastern slopes of the Andes in Colombia, Ecuador, and Peru, as well as in the upper/middle Amazon basin.

Abstract Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species 1,2 . However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation 3 . Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus , which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene , and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus . These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.