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Abstract Neotropical Heliconius butterflies are well known for their intricate behaviors and multiple instances of incipient speciation. Chemosensing plays a fundamental role in the life history of these groups of butterflies and in the establishment of reproductive isolation. However, chemical communication involves synergistic sensory and accessory functions, and it remains challenging to investigate the molecular mechanisms underlying behavioral differences. Here, we examine the gene expression profiles and genomic divergence of three sensory tissues (antennae, legs, and mouthparts) between sexes (females and males) and life stages (different adult stages) in two hybridizing butterflies, Heliconius melpomene and Heliconius cydno. By integrating comparative transcriptomic and population genomic approaches, we found evidence of widespread gene expression divergence, supporting a crucial role of sensory tissues in the establishment of species barriers. We also show that sensory diversification increases in a manner consistent with evolutionary divergence based on comparison with the more distantly related species Heliconius charithonia. The findings of our study strongly support the unique chemosensory function of antennae in all three species, the importance of the Z chromosome in interspecific divergence, and the nonnegligible role of nonchemosensory genes in the divergence of chemosensory tissues. Collectively, our results provide a genome-wide illustration of diversification in the chemosensory system under incomplete reproductive isolation, revealing strong molecular separation in the early stage of speciation. Here, we provide a unique perspective and relevant view of the genetic architecture (sensory and accessory functions) of chemosensing beyond the classic chemosensory gene families, leading to a better understanding of the magnitude and complexity of molecular changes in sensory tissues that contribute to the establishment of reproductive isolation and speciation. 

Chemosensory communication is essential to insect biology, playing indispensable roles during mate-finding, foraging, and oviposition behaviors. These traits are particularly important during speciation, where chemical perception may serve to establish species barriers. However, identifying genes associated with such complex behavioral traits remains a significant challenge. Through a combination of transcriptomic and genomic approaches, we characterize the genetic architecture of chemoperception and the role of chemosensing during speciation for a young species pair of Heliconius butterflies, Heliconius melpomene and Heliconius cydno . We provide a detailed description of chemosensory gene-expression profiles as they relate to sensory tissue (antennae, legs, and mouthparts), sex (male and female), and life stage (unmated and mated female butterflies). Our results untangle the potential role of chemical communication in establishing barriers during speciation and identify strong candidate genes for mate and host plant choice behaviors. Of the 252 chemosensory genes, HmOBP20 (involved in volatile detection) and HmGr56 (a putative synephrine-related receptor) emerge as strong candidates for divergence in pheromone detection and host plant discrimination, respectively. These two genes are not physically linked to wing-color pattern loci or other genomic regions associated with visual mate preference. Altogether, our results provide evidence for chemosensory divergence between H. melpomene and H. cydno , two rarely hybridizing butterflies with distinct mate and host plant preferences, a finding that supports a polygenic architecture of species boundaries. 

Abstract Butterfly eyes are complex organs that are composed of a diversity of proteins and they play a central role in visual signaling and ultimately, speciation, and adaptation. Here, we utilized the whole eye transcriptome to obtain a more holistic view of the evolution of the butterfly eye while accounting for speciation events that co-occur with ancient hybridization. We sequenced and assembled transcriptomes from adult female eyes of eight species representing all major clades of the Heliconius genus and an additional outgroup species, Dryas iulia. We identified 4,042 orthologous genes shared across all transcriptome data sets and constructed a transcriptome-wide phylogeny, which revealed topological discordance with the mitochondrial phylogenetic tree in the Heliconius pupal mating clade. We then estimated introgression among lineages using additional genome data and found evidence for ancient hybridization leading to the common ancestor of Heliconius hortense and Heliconius clysonymus. We estimated the Ka/Ks ratio for each orthologous cluster and performed further tests to demonstrate genes showing evidence of adaptive protein evolution. Furthermore, we characterized patterns of expression for a subset of these positively selected orthologs using qRT-PCR. Taken together, we identified candidate eye genes that show signatures of adaptive molecular evolution and provide evidence of their expression divergence between species, tissues, and sexes. Our results demonstrate: 1) greater evolutionary changes in younger Heliconius lineages, that is, more positively selected genes in the cydno–melpomene–hecale group as opposed to the sara–hortense–erato group, and 2) suggest an ancient hybridization leading to speciation among Heliconius pupal-mating species. 

Background Insects are the most diverse group of animals which have established intricate evolutionary interactions with bacteria. However, the importance of these interactions is still poorly understood. Few studies have focused on a closely related group of insect species, to test the similarities and differences between their microbiota. Heliconius butterflies are a charismatic recent insect radiation that evolved the unique ability to use pollen as a protein source, which affected life history traits and resulted in an elevated speciation rates. We hypothesize that different Heliconius butterflies sharing a similar trophic pollen niche, harbor a similar gut flora within species, population and sexes. Methods To test our hypothesis, we characterized the microbiota of 38 adult male and female butterflies representing six species of Heliconius butterflies and 2 populations of the same species. We sequenced the V4 region of the 16S rRNA gene with the Roche 454 system and analyzed the data with standard tools for microbiome analysis. Results Overall, we found a low microbial diversity with only 10 OTUs dominating across all individuals, mostly Proteobacteria and Firmicutes, which accounted for  99.5% of the bacterial reads. When rare reads were considered, we identified a total of 406 OTUs across our samples. We identified reads within Phyla Chlamydiae , found in 5 butterflies of four species. Interestingly, only three OTUs were shared among all 38 individuals ( Bacillus, Enterococcus and Enterobacteriaceae ). Altogether, the high individual variation overshadowed species and sex differences. Thus, bacterial communities were not structured randomly with 13% of beta-diversity explained by species, and 40 rare OTUs being significantly different across species. Finally, 13 OTUs, including the intercellular symbiont Spiroplasma, varied significantly in relative abundance between males and females. Discussion The Heliconius microbial communities in these 38 individuals show a low diversity with few differences in the rare microbes between females, males, species or populations. Indeed, Heliconius butterflies, similarly to other insects, are dominated by few OTUs, mainly from Proteobacteria and Firmicutes. The overall low microbial diversity observed contrasts with the high intra-species variation in microbiome composition. This could indicate that much of the microbiome maybe acquired from their surroundings. The significant differences between species and sexes were restricted to rare taxa, which could be important for microbial community stability under changing conditions as seen in other host-microbiome systems. The presence of symbionts like Spiroplasma or Chlamydiae , identified in this study for the first time in Heliconius , could play a vital role in their behavior and evolution by vertical transmission. Altogether, our study represents a step forward into the description of the microbial diversity in a charismatic group of closely related butterflies.