874 research outputs found
Butterfly learning and the diversification of plant leaf shape
Visual cues are important for insects to find flowers and host plants. It has been proposed that the diversity of leaf shape in Passiflora vines could be a result of negative frequency dependent selection driven by visual searching behavior among their butterfly herbivores. Here we tested the hypothesis that Heliconius butterflies use leaf shape as a cue to initiate approach toward a host plant. We first tested for the ability to recognize shapes using a food reward conditioning experiment. Butterflies showed an innate preference for flowers with three and five petals. However, they could be trained to increase the frequency of visits to a non-preferred flower with two petals, indicating an ability to learn to associate shape with a reward. Next we investigated shape learning specifically in the context of oviposition by conditioning females to lay eggs on two shoots associated with different artificial leaf shapes: their own host plant, Passiflora biflora, and a lanceolate non-biflora leaf shape. The conditioning treatment had a significant effect on the approach of butterflies to the two leaf shapes, consistent with a role for shape learning in oviposition behavior. This study is the first to show that Heliconius butterflies use shape as a cue for feeding and oviposition, and can learn shape preference for both flowers and leaves. This demonstrates the potential for Heliconius to drive negative frequency dependent selection on the leaf shape of their Passiflora host plants
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Sexually dimorphic gene expression and transcriptome evolution provides mixed evidence for a fast-Z effect in Heliconius
Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution for a group of butterflies. First, we improve the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then, we analyse RNA from male and female whole abdomens and sequence female ovary and gut tissue to identify sex and tissue specific gene expression profiles in H. melpomene. Using these expression profiles we compare: 1) sequence divergence and polymorphism; 2) the strength of positive and negative selection; and 3) rates of adaptive evolution, for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato.
We show that the rate of adaptive substitutions is higher for Z than autosomal genes, but contrary to expectation, it is also higher for male biased than female biased genes. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic specific tissue. Our results contribute to a growing body of literature from other ZW systems that also provide mixed evidence for a fastâZ effect where hemizygosity influences the rate of adaptive substitutions
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Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?
A major challenge is to understand how conserved gene regulatory networks control the wonderful diversity of form that we see among animals and plants. Butterfly wing patterns are an excellent example of this diversity. Butterfly wings form as imaginal discs in the caterpillar and are constructed by a gene regulatory network, much of which is conserved across the holometabolous insects. Recent work in butterflies takes advantage of genomic approaches and offers insights into how the diversification of wing patterns is overlaid onto this conserved network. WntA is a patterning morphogen that alters spatial information in the wing. Optix is a transcription factor that acts later in development to paint specific wing regions red. Both of these loci fit the paradigm of conserved protein-coding loci with diverse regulatory elements and developmental roles that have taken on novel derived functions in patterning wings. These discoveries offer insights into the 'Nymphalid Ground Plan', which offers a unifying hypothesis for pattern formation across nymphalid butterflies. These loci also represent 'hotspots' for morphological change that have been targeted repeatedly during evolution. Both convergent and divergent evolution of a great diversity of patterns is controlled by complex alleles at just a few genes. We suggest that evolutionary change has become focused on one or a few genetic loci for two reasons. First, pre-existing complex -regulatory loci that already interact with potentially relevant transcription factors are more likely to acquire novel functions in wing patterning. Second, the shape of wing regulatory networks may constrain evolutionary change to one or a few loci. Overall, genomic approaches that have identified wing patterning loci in these butterflies offer broad insight into how gene regulatory networks evolve to produce diversity.
This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.Wellcome Trus
Deep Convergence, Shared Ancestry, and Evolutionary Novelty in the Genetic Architecture of Heliconius Mimicry
Convergent evolution can occur through different genetic mechanisms in different species. It is now clear that convergence at the genetic level is also widespread, and can be caused by either (i) parallel genetic evolution, where independently evolved convergent mutations arise in different populations or species, or (ii) collateral evolution in which shared ancestry results from either ancestral polymorphism or introgression among taxa. The adaptive radiation of Heliconius butterflies shows color pattern variation within species, as well as mimetic convergence between species. Using comparisons from across multiple hybrid zones, we use signals of shared ancestry to identify and refine multiple putative regulatory elements in Heliconius melpomene and its comimics, Heliconius elevatus and Heliconius besckei, around three known major color patterning genes: optix, WntA, and cortex. While we find that convergence between H. melpomene and H. elevatus is caused by a complex history of collateral evolution via introgression in the Amazon, convergence between these species in the Guianas appears to have evolved independently. Thus, we find adaptive convergent genetic evolution to be a key driver of regulatory changes that lead to rapid phenotypic changes. Furthermore, we uncover evidence of parallel genetic evolution at some loci around optix and WntA in H. melpomene and its distant comimic Heliconius erato. Ultimately, we show that all three of convergence, conservation, and novelty underlie the modular architecture of Heliconius color pattern mimicry
The evolution of sex ratio distorter suppression affects a 25 cM genomic region in the butterfly Hypolimnas bolina
Open Access ArticleSymbionts that distort their host's sex ratio by favouring the production and survival of females are common in arthropods. Their presence produces intense Fisherian selection to return the sex ratio to parity, typified by the rapid spread of host 'suppressor' loci that restore male survival/development. In this study, we investigated the genomic impact of a selective event of this kind in the butterfly Hypolimnas bolina. Through linkage mapping, we first identified a genomic region that was necessary for males to survive Wolbachia-induced male-killing. We then investigated the genomic impact of the rapid spread of suppression, which converted the Samoan population of this butterfly from a 100:1 female-biased sex ratio in 2001 to a 1:1 sex ratio by 2006. Models of this process revealed the potential for a chromosome-wide effect. To measure the impact of this episode of selection directly, the pattern of genetic variation before and after the spread of suppression was compared. Changes in allele frequencies were observed over a 25 cM region surrounding the suppressor locus, with a reduction in overall diversity observed at loci that co-segregate with the suppressor. These changes exceeded those expected from drift and occurred alongside the generation of linkage disequilibrium. The presence of novel allelic variants in 2006 suggests that the suppressor was likely to have been introduced via immigration rather than through de novo mutation. In addition, further sampling in 2010 indicated that many of the introduced variants were lost or had declined in frequency since 2006. We hypothesize that this loss may have resulted from a period of purifying selection, removing deleterious material that introgressed during the initial sweep. Our observations of the impact of suppression of sex ratio distorting activity reveal a very wide genomic imprint, reflecting its status as one of the strongest selective forces in nature.Natural Environment Research Council (NERC
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Maintaining mimicry diversity: optimal warning colour patterns differ among microhabitats in Amazonian clearwing butterflies
Mimicry is one of the best-studied examples of adaptation, and recent studies have provided new insights into the role of mimicry in speciation and diversification. Classical MĂŒllerian mimicry theory predicts convergence in warning signal among protected species, yet tropical butterflies are exuberantly diverse in warning colour patterns, even within communities. We tested the hypothesis that microhabitat partitioning in aposematic butterflies and insectivorous birds can lead to selection for different colour patterns in different microhabitats and thus help maintain mimicry diversity. We measured distribution across flight height and topography for 64 species of clearwing butterflies (Ithomiini) and their co-mimics, and 127 species of insectivorous birds, in an Amazon rainforest community. For the majority of bird species, estimated encounter rates were non-random for the two most abundant mimicry rings. Furthermore, most butterfly species in these two mimicry rings displayed the warning colour pattern predicted to be optimal for anti-predator defence in their preferred microhabitats. These conclusions were supported by a field trial using butterfly specimens, which showed significantly different predation rates on colour patterns in two microhabitats. We therefore provide the first direct evidence to support the hypothesis that different mimicry patterns can represent stable, community-level adaptations to differing biotic environments.This work was funded by the Leverhulme Trust F/00158/AK, F/09 364F (UK) and additionally supported by the Centre National de la Recherche Scientifique (ATIP grant to M. Elias), the MusĂ©um National d'Histoire Naturelle and the University of Florid
What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies
The process by which species evolve can be illuminated by investigating barriers that limit gene flow between taxa. Recent radiations, such as Heliconius butterflies, offer the opportunity to compare isolation between pairs of taxa at different stages of ecological, geographical, and phylogenetic divergence. Here, we report a comparative analysis of existing and novel data in order to quantify the strength and direction of isolating barriers within a well-studied clade of Heliconius Our results highlight that increased divergence is associated with the accumulation of stronger and more numerous barriers to gene flow. Wing pattern is both under natural selection for MĂŒllerian mimicry and involved in mate choice, and therefore underlies several isolating barriers. However, pairs which share a similar wing pattern also display strong reproductive isolation mediated by traits other than wing pattern. This suggests that, while wing pattern is a key factor for early stages of divergence, it may become facultative at later stages of divergence. Additional factors including habitat partitioning, hybrid sterility, and chemically mediated mate choice are associated with complete speciation. Therefore, although most previous work has emphasized the role of wing pattern, our comparative results highlight that speciation is a multi-dimensional process, whose completion is stabilized by many factors.This work was supported by ERC Starting Grant Stg-243179 (MimEvol) and French Research Agency grant ANR-12-JSV7-0005 (HybEvol) to M.J. C.S. was funded by the Universidad del Rosario FIUR grant QDN-DG001 and COLCIENCIAS (Grant FP44842-5-2017). R.M.M. was funded by a Research Fellowship at King's College, Cambridge, UK. R.M.M. and C.D.J. were funded by an ERC grant (Speciation Genetics 339873)
The comparative landscape of duplications in Heliconius melpomene and Heliconius cydno
Gene duplications can facilitate adaptation and may lead to interpopulation divergence, causing reproductive isolation. We used whole-genome resequencing data from 34 butterflies to detect duplications in two Heliconius species, Heliconius cydno and Heliconius 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 and evaluated the accuracy of our approach using 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.AP is funded by a NERC studentship (PFZE/063). CDJ, SLB, JWD and SHM are funded by ERC grant SpeciationGenetics (Grant Number 339873). Pacific Biosciences sequencing was carried out by Karen Oliver in collaboration with Richard Durbin at the Sanger Institute, supported by European Research Council (ERC) Grant Number 339873, Wellcome Trust Grant Number 098051. We thank Jenny Barna and Stuart Rankin for computing support. Analyses were carried out using the Darwin Supercomputer of the University of Cambridge High Performance Computing Service (http://www.hpc.cam.ac.uk/), provided by Dell Inc. using Strategic Research Infrastructure Funding from the Higher Education Funding Council for England, and funding from the Science and Technology Facilities Council. We thank the editor and three anonymous reviewers for their comments that helped us to improve this manuscript
Male pheromone composition depends on larval but not adult diet in Heliconius melpomene
1. Condition-dependent traits can act as honest signals of mate quality, with fitter individuals able to display preferred phenotypes. Nutrition is known to be an important determinant of individual condition, with diet known to affect many secondary sexual traits.
2. In Heliconius butterflies, male chemical signalling plays an important role in female mate choice. Potential male sex pheromone components have been previously identified, but it is unclear what information they convey to the female.
3. Here, we test the effect of diet on androconial and genital compound production in male Heliconius melpomene rosina. To manipulate larval diet, we rear larvae on three different Passiflora host plants: P. menispermifolia, the preferred host plant, P. vitifolia, and P. platyloba. To manipulate adult diet, we rear adult butterflies with and without access to pollen, a key component of their diet.
4. We find no evidence that adult pollen consumption affects compound production in the first ten days after eclosion. We also find strong overlap in the chemical profiles of individuals reared on different larval host plants. The most abundant compounds produced by the butterflies do not differ between host plant groups. However, some compounds found in small amounts differ both qualitatively and quantitatively. We predict some of these compounds to be of plant origin and the others synthesized by the butterfly. Further electrophysiological and behavioural experiments will be needed to determine the biological significance of these differences.KD was supported by a Natural Research Council Doctoral Training Partnership and a Smithsonian Tropical Research Institute Short Term Fellowship. KJRPB and CDJ were supported by a European Research Council grant number 339873 SpeciationGenetics. WOM was supported by the Smithsonian Tropical Research Institute and NSF grant DEB 1257689. SS thanks the Deutsche Forschungsgemeinschaft (DFG) for support through grant Schu984/12-1
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A new subspecies in a Heliconius butterfly adaptive radiation (Lepidoptera: Nymphalidae)
A fundamental goal in evolutionary biology is to understand how evolutionary patterns and processes shape natural diversity. This, however, requires a complete characterization of the phenotypic and genetic variation between and within species. Here, we used molecular, morphological and behavioural data to describe a new and stable subspecies of Heliconius timareta, named Heliconius timareta linaresisubsp.nov. This race differs phenotypically from other red-coloured H. timareta and instead exhibits a black and yellow wing pattern more similar to Heliconius cydno. However, mtDNA, microsatellite and amplified-fragment length polymorphism data indicate a closer relationship with H. timareta than H. cydno and Heliconius melpomene. Larval morphology and host plant preferences are similar to other H. timareta and H. cydno races. Thus, our combined data indicate that this taxon is a novel subspecies of H. timareta, clearly differentiated from H. cydno and H. melpomene.We acknowledge the Smithsonian Tropical Research Institute (STRI), where part of the laboratory work was carried out and funded. C.F. Arias and N. Giraldo were supported by fellowships from the Smithsonian Tropical Research Institute. C. F. Arias was also supported by Convocatoria âEs tiempo de volverâ (COLCINECIAS)-2014, contract No. 656-2014. W.O. McMillan received support from NSF grant (DEB 1257689). C. Salazar was funded by Convocatoria para proyectos de investigaciĂłn en Ciencias BĂĄsicas (COLCINECIAS)-2014, contract No. FP44842-103-2015
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