The genomic basis of species barriers in Heliconius butterflies

Understanding the genetics underlying the speciation process has been a long-standing goal of evolutionary biology. Studying inter-population crosses can elucidate the genetic architecture of reproductive isolation and, ultimately, the process of speciation. Hybridization between two species is often maladaptive and results in offspring with decreased fitness compared to the parental forms. Recently, with the development of molecular and genomic tools, it has become possible to understand how and when reproductive isolation arises and what are the underlying mechanisms in the evolution of genetic incompatibilities. Heliconius is a genus of neotropical butterfly best know for their Müllerian mimicry. Here I focus on Heliconius cydno and Heliconius melpomene, two hybridising sympatric species with low levels of inter-specific hybridisation that nonetheless results in genome-wide signatures of admixture. I show that hybrids develop ovarian tissue and, occasionally, oocytes; and use genomic approaches to examine several potential mechanisms underlying post-zygotic isolation between H. cydno and H. melpomene. Firstly, I investigate evolution by gene duplication and identify loci putatively under divergent selection that may play a role in species divergence and speciation. Secondly, I quantify sexually dimorphic expression in H. melpomene, and calculate rates of molecular evolution between H. melpomene and H. erato. Thirdly, I identify differentially expressed genes in the H. cydno x H. melpomene F1 hybrids that may be involved in the species barrier. Finally, investigate whether epigenetic silencing mechanisms could underlie post-zygotic isolation between H. cydno and H. melpomene by quantifying transposable element expression and small RNAs. Overall, I identify loci that merit further investigation for their potential in maintaining reproductive barriers between these two species. I show that different regions of the genome evolve at different molecular rates but there is no faster-Z effect, and consider how might this affect evolution of reproductive isolation. Finally, I show that aberrant epigenetic silencing, a mechanism behind hybrid sterility that is common in other species, is not correlated with post-zygotic isolation between H. cydno and H. melpomene.National Environment Research Council (PFZE/063); St John’s College 10th Term Funding; a grant from the Cambridge Philosophical Society and a grant for financial hardship from the Elliot and Leathersellers’ Company Funds

A novel terpene synthase controls differences in anti-aphrodisiac pheromone production between closely related Heliconius butterflies.

Plants and insects often use the same compounds for chemical communication, but not much is known about the genetics of convergent evolution of chemical signals. The terpene (E)-β-ocimene is a common component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-aphrodisiac pheromone. While the biosynthesis of terpenes has been described in plants and microorganisms, few terpene synthases (TPSs) have been identified in insects. Here, we study the recent divergence of 2 species, H. melpomene and Heliconius cydno, which differ in the presence of (E)-β-ocimene; combining linkage mapping, gene expression, and functional analyses, we identify 2 novel TPSs. Furthermore, we demonstrate that one, HmelOS, is able to synthesise (E)-β-ocimene in vitro. We find no evidence for TPS activity in HcydOS (HmelOS ortholog of H. cydno), suggesting that the loss of (E)-β-ocimene in this species is the result of coding, not regulatory, differences. The TPS enzymes we discovered are unrelated to previously described plant and insect TPSs, demonstrating that chemical convergence has independent evolutionary origins

A novel terpene synthase controls differences in anti-aphrodisiac pheromone production between closely related Heliconius butterflies

Plants and insects often use the same compounds for chemical communication, but not much is known about the genetics of convergent evolution of chemical signals. The terpene (E)-beta-ocimene is a common component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-aphrodisiac pheromone. While the biosynthesis of terpenes has been described in plants and microorganisms, few terpene synthases (TPSs) have been identified in insects. Here, we study the recent divergence of 2 species, H. melpomene and Heliconius cydno, which differ in the presence of (E)-beta-ocimene; combining linkage mapping, gene expression, and functional analyses, we identify 2 novel TPSs. Furthermore, we demonstrate that one, HmelOS, is able to synthesise (E)-beta-ocimene in vitro. We find no evidence for TPS activity in HcydOS (HmelOS ortholog of H. cydno), suggesting that the loss of (E)-beta-ocimene in this species is the result of coding, not regulatory, differences. The TPS enzymes we discovered are unrelated to previously described plant and insect TPSs, demonstrating that chemical convergence has independent evolutionary origins.Peer reviewe

Estimation of the spontaneous mutation rate in Heliconius melpomene

This is the final published version. It first appeared at mbe.oxfordjournals.org/content/early/2014/11/03/molbev.msu302.abstract.We estimated the spontaneous mutation rate in Heliconius melpomene by genome sequencing of\ud a pair of parents and 30 of their offspring, based on the ratio of number of de novo heterozygotes\ud to the number of callable site-individuals. We detected nine new mutations, each one affecting a\ud single site in a single offspring. This yields an estimated mutation rate of 2.9 x 10-9 (95%\ud confidence interval, 1.3 x 10-9 - 5.5 x 10-9), which is similar to recent estimates in Drosophila\ud melanogaster, the only other insect species in which the mutation rate has been directly estimated.\ud We infer that recent effective population size of H. melpomene is about 2 million, a substantially\ud lower value than its census size, suggesting a role for natural selection reducing diversity. We\ud estimate that H. melpomene diverged from its M?llerian co-mimic H. erato about 6 MYA, a\ud somewhat later date than estimates based on a local molecular clock.CJ was funded by BBSRC [H01439X/1], JWD was funded by the Herchel Smith Fund and PDK and\ud RWN were funded by the BBSRC

No evidence for maintenance of a sympatric Heliconius species barrier by chromosomal inversions.

Mechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of coadapted gene combinations. The sympatric butterfly species Heliconius melpomene and Heliconius cydno are separated by many strong barriers, but the species still hybridize infrequently in the wild, and around 40% of the genome is influenced by introgression. We tested the hypothesis that genetic barriers between the species are maintained by inversions or other mechanisms that reduce between-species recombination rate. We constructed fine-scale recombination maps for Panamanian populations of both species and their hybrids to directly measure recombination rate within and between species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno

A novel terpene synthase controls differences in anti-aphrodisiac pheromone production between closely related Heliconius butterflies

Funder: Deutsche Forschungsgemeinschaft; Grant(s): Emmy Noether Fellowship GZ:ME4845/1-1Funder: Jane ja Aatos Erkon Säätiö; funder-id: http://dx.doi.org/10.13039/501100004012Funder: Smithsonian Tropical Research Institute; funder-id: http://dx.doi.org/10.13039/100009201Plants and insects often use the same compounds for chemical communication, but not much is known about the genetics of convergent evolution of chemical signals. The terpene (E)-β-ocimene is a common component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-aphrodisiac pheromone. While the biosynthesis of terpenes has been described in plants and microorganisms, few terpene synthases (TPSs) have been identified in insects. Here, we study the recent divergence of 2 species, H. melpomene and Heliconius cydno, which differ in the presence of (E)-β-ocimene; combining linkage mapping, gene expression, and functional analyses, we identify 2 novel TPSs. Furthermore, we demonstrate that one, HmelOS, is able to synthesise (E)-β-ocimene in vitro. We find no evidence for TPS activity in HcydOS (HmelOS ortholog of H. cydno), suggesting that the loss of (E)-β-ocimene in this species is the result of coding, not regulatory, differences. The TPS enzymes we discovered are unrelated to previously described plant and insect TPSs, demonstrating that chemical convergence has independent evolutionary origins

Estimation of the spontaneous nutation rate in Heliconius melpomene

This is the final published version. It first appeared at mbe.oxfordjournals.org/content/early/2014/11/03/molbev.msu302.abstract.We estimated the spontaneous mutation rate in Heliconius melpomene by genome sequencing of\ud a pair of parents and 30 of their offspring, based on the ratio of number of de novo heterozygotes\ud to the number of callable site-individuals. We detected nine new mutations, each one affecting a\ud single site in a single offspring. This yields an estimated mutation rate of 2.9 x 10-9 (95%\ud confidence interval, 1.3 x 10-9 - 5.5 x 10-9), which is similar to recent estimates in Drosophila\ud melanogaster, the only other insect species in which the mutation rate has been directly estimated.\ud We infer that recent effective population size of H. melpomene is about 2 million, a substantially\ud lower value than its census size, suggesting a role for natural selection reducing diversity. We\ud estimate that H. melpomene diverged from its M?llerian co-mimic H. erato about 6 MYA, a\ud somewhat later date than estimates based on a local molecular clock.CJ was funded by BBSRC [H01439X/1], JWD was funded by the Herchel Smith Fund and PDK and\ud RWN were funded by the BBSRC

merged_by_tool_trio_melpomene

chromosome 2 merged by tool on the trio H. melpomene sample

Data from: The comparative landscape of duplications in Heliconius melpomene and Heliconius cydno

Gene duplications can facilitate adaptation and may lead to inter-population divergence, causing reproductive isolation. We used whole-genome re-sequencing data from 34 butterflies to detect duplications in two Heliconius species, H. cydno and H. melpomene. Taking advantage of three distinctive signals of duplication in short-read sequencing data, we identified 744 duplicated loci in H. cydno and H. melpomene, 96% of which were validated with single molecule sequencing. We have found that duplications overlap genes significantly less than expected at random in H. melpomene, consistent with the action of background selection against duplicates in functional regions of the genome. Duplicate loci that are highly differentiated between H. melpomene and H. cydno map to four different chromosomes. Four duplications were identified with a strong signal of divergent selection, including an odorant binding protein and another in close proximity with a known wing colour pattern locus that differs between the two species