We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation.
We here pioneer a low-cost assembly strategy for 20 Heliconiini genomes to characterize the evolutionary history of the rapidly radiating genus Heliconius. A bifurcating tree provides a poor fit to the data, and we therefore explore a reticulate phylogeny for Heliconius. We probe the genomic architecture of gene flow, and develop a new method to distinguish incomplete lineage sorting from introgression. We find that most loci with non-canonical histories arose through introgression, and are strongly underrepresented in regions of low recombination and high gene density. This is expected if introgressed alleles are more likely to be purged in such regions due to tighter linkage with incompatibility loci. Finally, we identify a hitherto unrecognized inversion, and show it is a convergent structural rearrangement that captures a known color pattern switch locus within the genus. Our multi-genome assembly approach enables an improved understanding of adaptive radiation.
Recent adaptive radiations provide excellent model systems for understanding speciation, but rapid diversification can cause problems for phylogenetic inference. Here we use gene genealogies to investigate the phylogeny of recent speciation in the heliconiine butterflies. We sequenced three gene regions, intron 3 ( approximately 550 bp) of sex-linked triose-phosphate isomerase (Tpi), intron 3 ( approximately 450 bp) of autosomal mannose-phosphate isomerase (Mpi), and 1,603 bp of mitochondrial cytochrome oxidase subunits I and II (COI and COII), for 37 individuals from 25 species of Heliconius and related genera. The nuclear intron sequences evolved at rates similar to those of mitochondrial coding sequences, but the phylogenetic utility of introns was restricted to closely related geographic populations and species due to high levels of indel variation. For two sister species pairs, Heliconius erato-Heliconius himera and Heliconius melpomene-Heliconius cydno, there was highly significant discordance between the three genes. At mtDNA and Tpi, the hypotheses of reciprocal monophyly and paraphyly of at least one species with respect to its sister could not be distinguished. In contrast alleles sampled from the third locus, Mpi, showed polyphyletic relationships between both species pairs. In all cases, recent coalescence of mtDNA lineages within species suggests that polyphyly of nuclear genes is not unexpected. In addition, very similar alleles were shared between melpomene and cydno, implying recent gene flow. Our finding of discordant genealogies between genes is consistent with models of adaptive speciation with ongoing gene flow and highlights the need for multiple locus comparisons to resolve phylogeny among closely related species.
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.
Sex-specific pheromones are known to play an important role in butterfly courtship, and may influence both individual reproductive success and reproductive isolation between species. Extensive ecological, behavioural and genetic studies of Heliconius butterflies have made a substantial contribution to our understanding of speciation. Male pheromones, although long suspected to play an important role, have received relatively little attention in this genus. Here, we combine morphological, chemical and behavioural analyses of male pheromones in the Neotropical butterfly Heliconius melpomene. First, we identify putative androconia that are specialized brush-like scales that lie within the shiny grey region of the male hindwing. We then describe putative male sex pheromone compounds, which are largely confined to the androconial region of the hindwing of mature males, but are absent in immature males and females. Finally, behavioural choice experiments reveal that females of H. melpomene, H. erato and H. timareta strongly discriminate against conspecific males which have their androconial region experimentally blocked. As well as demonstrating the importance of chemical signalling for female mate choice in Heliconius butterflies, the results describe structures involved in release of the pheromone and a list of potential male sex pheromone compounds.
Abstract1. The use of image data to quantify, study and compare variation in the colours and patterns of organisms requires the alignment of images to establish homology, followed by colour-based segmentation of images. Here, we describe an R package for image alignment and segmentation that has applications to quantify colour patterns in a wide range of organisms.2. patternize is an R package that quantifies variation in colour patterns obtained from image data. patternize first defines homology between pattern positions across specimens either through manually placed homologous landmarks or automated image registration. Pattern identification is performed by categorizing the distribution of colours using an RGB threshold, k-means clustering or watershed transformation.3. We demonstrate that patternize can be used for quantification of the colour patterns in a variety of organisms by analysing image data for butterflies, guppies, spiders and salamanders. Image data can be compared between sets of specimens, visualized as heatmaps and analysed using principal component analysis.4. patternize has potential applications for fine scale quantification of colour pattern phenotypes in population comparisons, genetic association studies and investigating the basis of colour pattern variation across a wide range of organisms. K E Y W O R D Scolour patterns, heatmap, image registration, image segmentation, landmarks | INTRODUCTIONNatural populations often harbour great phenotypic diversity. Variation in colour and pattern are of the more vivid examples of morphological variability in nature. Taxa as diverse as spiders (Cotoras et al., 2016;De Busschere, Baert, Van Belleghem, Dekoninck, & Hendrickx, 2012), insects (Katakura, Saitoh, Nakamura, & Abbas, 1994;Williams, 2007), fish (Endler, 1983;Houde, 1987), amphibians and reptiles (Allen, Baddeley, Scott-samuel, & Cuthill, 2013;Balogová & Uhrin, 2015;Calsbeek, Bonneaud, & Smith, 2008;Rabbani, Zacharczenko, Green, Abbani, & Acharczenko, 2015), mammals (Hoekstra, Hirschmann, Bundey, Insel, & Crossland, 2006;Nekaris & Jaffe, 2007) and plants (Clegg & Durbin, 2000;Mascó, Noy-Meir, & Sérsic, 2004) | ALIGNMENTSuperimposing colour patterns to quantify variation in their expression requires the homologous alignment of the anatomical structures they occur in. Image transformations for this alignment can be obtained from landmark based transformations or image registration techniques. | Landmark based transformationsLandmark based transformations use discrete anatomical points that are homologous among individuals in the analysis. Non-rigid, but uniform transformations from one set of "source" landmarks to a set of "target" landmarks such as affine transformations include translation, rotation, scaling and skewing (Hazewinkel, 2001). Additionally, nonuniform changes in shape between the source and target landmarks can be accounted for by storing the transformation as if it were "the bending of a thin sheet of metal," the so-called thin plate spline (TPS) transformation (Duchon, 1...
In butterflyfishes (Chaetodontidae), color pattern evolves rapidly and is often the only morphological trait separating closely related species. Vivid coloration is frequently assumed to provide critical signals for mate recognition and mate choice, but few direct experimental tests are available. Here we analyze the relationship between color pattern change, mate choice, and genetic differentiation in a group of three very closely related allopatric butterflyfishes. We found that in only one member of this group, Chaetodon multicinctus, is color pattern evolution associated with mate preference and genetic divergence. For its two sister species, C. punctatofasciatus and C. pelewensis, color pattern change has not resulted in assortative mating (based on laboratory pairing experiments and field observations) or in significant mtDNA or allozyme differentiation. In a contact zone on reefs in the Solomon Islands and Papua New Guinea, hybridization between the two forms has nearly homogenized color pattern differences. Outside these areas, however, color pattern remains distinct. Genetic variation is homogeneous over a much larger geographic scale. Sequence variation in the tRNA-proline end of the mitochondrial control region and allozyme variation was distributed widely within C. punctatofasciatus and C. pelewensis, which suggests few constraints to mitochondrial or nuclear gene flow across the color pattern boundary. These contrasting patterns strongly suggest that selection is maintaining color pattern differences in allopatry in the face of potentially homogenizing levels of gene flow. The mating pattern data show that this selection is not operating on mate recognition in the strictest sense, but probably on some other aspect of the social system of these territorial fish. In this case, divergence in mating preference can follow color pattern evolution, but is not contemporaneous with it.
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