RESUMO
Sex chromosomes are evolutionarily labile in many animals and sometimes fuse with autosomes, creating so-called neo-sex chromosomes. Fusions between sex chromosomes and autosomes have been proposed to reduce sexual conflict and to promote adaptation and reproductive isolation among species. Recently, advances in genomics have fuelled the discovery of such fusions across the tree of life. Here, we discovered multiple fusions leading to neo-sex chromosomes in the sapho subclade of the classical adaptive radiation of Heliconius butterflies. Heliconius butterflies generally have 21 chromosomes with very high synteny. However, the five Heliconius species in the sapho subclade show large variation in chromosome number ranging from 21 to 60. We find that the W chromosome is fused with chromosome 4 in all of them. Two sister species pairs show subsequent fusions between the W and chromosomes 9 or 14, respectively. These fusions between autosomes and sex chromosomes make Heliconius butterflies an ideal system for studying the role of neo-sex chromosomes in adaptive radiations and the degeneration of sex chromosomes over time. Our findings emphasize the capability of short-read resequencing to detect genomic signatures of fusion events between sex chromosomes and autosomes even when sex chromosomes are not explicitly assembled.
Assuntos
Borboletas , Evolução Molecular , Cromossomos Sexuais , Animais , Borboletas/genética , Cromossomos Sexuais/genética , Feminino , Masculino , Filogenia , Genômica/métodos , Sintenia , Cromossomos de Insetos/genética , Genoma de InsetoRESUMO
When populations experience different sensory conditions, natural selection may favor sensory system divergence, affecting peripheral structures and/or downstream neural pathways. We characterized the outer eye morphology of sympatric Heliconius butterflies from different forest types and their first-generation reciprocal hybrids to test for adaptive visual system divergence and hybrid disruption. In Panama, Heliconius cydno occurs in closed forests, whereas Heliconius melpomene resides at the forest edge. Among wild individuals, H. cydno has larger eyes than H. melpomene, and there are heritable, habitat-associated differences in the visual brain structures that exceed neutral divergence expectations. Notably, hybrids have intermediate neural phenotypes, suggesting disruption. To test for similar effects in the visual periphery, we reared both species and their hybrids in common garden conditions. We confirm that H. cydno has larger eyes and provide new evidence that this is driven by selection. Hybrid eye morphology is more H. melpomene-like despite body size being intermediate, contrasting with neural trait intermediacy. Overall, our results suggest that eye morphology differences between H. cydno and H. melpomene are adaptive and that hybrids may suffer fitness costs due to a mismatch between the peripheral visual structures and previously described neural traits that could affect visual performance.
Assuntos
Borboletas , Seleção Genética , Simpatria , Animais , Borboletas/anatomia & histologia , Borboletas/genética , Borboletas/fisiologia , Olho/anatomia & histologia , Panamá , Feminino , Masculino , Hibridização GenéticaRESUMO
Little is known about the extent to which species use homologous regulatory architectures to achieve phenotypic convergence. By characterizing chromatin accessibility and gene expression in developing wing tissues, we compared the regulatory architecture of convergence between a pair of mimetic butterfly species. Although a handful of color pattern genes are known to be involved in their convergence, our data suggest that different mutational paths underlie the integration of these genes into wing pattern development. This is supported by a large fraction of accessible chromatin being exclusive to each species, including the de novo lineage-specific evolution of a modular optix enhancer. These findings may be explained by a high level of developmental drift and evolutionary contingency that occurs during the independent evolution of mimicry.
Assuntos
Evolução Biológica , Mimetismo Biológico , Borboletas , Montagem e Desmontagem da Cromatina , Asas de Animais , Animais , Mimetismo Biológico/genética , Borboletas/anatomia & histologia , Borboletas/genética , Borboletas/crescimento & desenvolvimento , Pigmentação/genética , Asas de Animais/anatomia & histologia , Asas de Animais/crescimento & desenvolvimento , Regulação da Expressão Gênica no Desenvolvimento , Elementos Facilitadores GenéticosRESUMO
Despite insertions and deletions being the most common structural variants (SVs) found across genomes, not much is known about how much these SVs vary within populations and between closely related species, nor their significance in evolution. To address these questions, we characterized the evolution of indel SVs using genome assemblies of three closely related Heliconius butterfly species. Over the relatively short evolutionary timescales investigated, up to 18.0% of the genome was composed of indels between two haplotypes of an individual Heliconius charithonia butterfly and up to 62.7% included lineage-specific SVs between the genomes of the most distant species (11 Mya). Lineage-specific sequences were mostly characterized as transposable elements (TEs) inserted at random throughout the genome and their overall distribution was similarly affected by linked selection as single nucleotide substitutions. Using chromatin accessibility profiles (i.e., ATAC-seq) of head tissue in caterpillars to identify sequences with potential cis-regulatory function, we found that out of the 31,066 identified differences in chromatin accessibility between species, 30.4% were within lineage-specific SVs and 9.4% were characterized as TE insertions. These TE insertions were localized closer to gene transcription start sites than expected at random and were enriched for sites with significant resemblance to several transcription factor binding sites with known function in neuron development in Drosophila We also identified 24 TE insertions with head-specific chromatin accessibility. Our results show high rates of structural genome evolution that were previously overlooked in comparative genomic studies and suggest a high potential for structural variation to serve as raw material for adaptive evolution.
Assuntos
Borboletas , Animais , Borboletas/genética , Cromatina/genética , Elementos de DNA Transponíveis/genética , Genômica , Mutação INDEL , Drosophila/genética , Evolução MolecularRESUMO
Genetic variation segregates as linked sets of variants or haplotypes. Haplotypes and linkage are central to genetics and underpin virtually all genetic and selection analysis. Yet, genomic data often omit haplotype information due to constraints in sequencing technologies. Here, we present "haplotagging," a simple, low-cost linked-read sequencing technique that allows sequencing of hundreds of individuals while retaining linkage information. We apply haplotagging to construct megabase-size haplotypes for over 600 individual butterflies (Heliconius erato and H. melpomene), which form overlapping hybrid zones across an elevational gradient in Ecuador. Haplotagging identifies loci controlling distinctive high- and lowland wing color patterns. Divergent haplotypes are found at the same major loci in both species, while chromosome rearrangements show no parallelism. Remarkably, in both species, the geographic clines for the major wing-pattern loci are displaced by 18 km, leading to the rise of a novel hybrid morph in the center of the hybrid zone. We propose that shared warning signaling (Müllerian mimicry) may couple the cline shifts seen in both species and facilitate the parallel coemergence of a novel hybrid morph in both comimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations.
Assuntos
Borboletas/genética , Haplótipos/genética , Hibridização Genética , Animais , Mimetismo Biológico , Inversão Cromossômica/genética , Equador , Rearranjo Gênico/genética , Variação Genética , Genoma , Característica Quantitativa Herdável , Seleção Genética , Especificidade da EspécieRESUMO
Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a "large-X" effect, genome scans between recently diverged populations and species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on the sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, that is "faster-X", barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole-genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply postzygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of incompatibilities. Our work demonstrates the importance of taking demography into account to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.
Assuntos
Borboletas/genética , Fluxo Gênico , Especiação Genética , Genética Populacional , Cromossomos Sexuais/genética , Animais , América Central , Feminino , Masculino , Modelos Genéticos , América do SulRESUMO
Understanding the genetic basis of phenotypic variation and the mechanisms involved in the evolution of adaptive novelty, especially in adaptive radiations, is a major goal in evolutionary biology. Here, we used whole-genome sequence data to investigate the origin of the yellow hindwing bar in the Heliconius cydno radiation. We found modular variation associated with hindwing phenotype in two narrow noncoding regions upstream and downstream of the cortex gene, which was recently identified as a pigmentation pattern controller in multiple species of Heliconius. Genetic variation at each of these modules suggests an independent control of the dorsal and ventral hindwing patterning, with the upstream module associated with the ventral phenotype and the downstream module with the dorsal one. Furthermore, we detected introgression between H. cydno and its closely related species Heliconius melpomene in these modules, likely allowing both species to participate in novel mimicry rings. In sum, our findings support the role of regulatory modularity coupled with adaptive introgression as an elegant mechanism by which novel phenotypic combinations can evolve and fuel an adaptive radiation.
Assuntos
Evolução Biológica , Mimetismo Biológico/genética , Borboletas/genética , Pigmentação/genética , Animais , Variação Genética , Genética Populacional , Genótipo , Fenótipo , Filogenia , Asas de AnimaisRESUMO
Identifying the genomic changes that control morphological variation and understanding how they generate diversity is a major goal of evolutionary biology. In Heliconius butterflies, a small number of genes control the development of diverse wing color patterns. Here, we used full genome sequencing of individuals across the Heliconius erato radiation and closely related species to characterize genomic variation associated with wing pattern diversity. We show that variation around color pattern genes is highly modular, with narrow genomic intervals associated with specific differences in color and pattern. This modular architecture explains the diversity of color patterns and provides a flexible mechanism for rapid morphological diversification.
RESUMO
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 Müllerian 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.
Assuntos
Mimetismo Biológico , Borboletas , Ecossistema , Pigmentação , Adaptação Fisiológica , Animais , Aves , Cor , Equador , Comportamento PredatórioRESUMO
Understanding why species richness peaks along the Andes is a fundamental question in the study of Neotropical biodiversity. Several biogeographic and diversification scenarios have been proposed in the literature, but there is confusion about the processes underlying each scenario, and assessing their relative contribution is not straightforward. Here, we propose to refine these scenarios into a framework which evaluates four evolutionary mechanisms: higher speciation rate in the Andes, lower extinction rates in the Andes, older colonization times and higher colonization rates of the Andes from adjacent areas. We apply this framework to a species-rich subtribe of Neotropical butterflies whose diversity peaks in the Andes, the Godyridina (Nymphalidae: Ithomiini). We generated a time-calibrated phylogeny of the Godyridina and fitted time-dependent diversification models. Using trait-dependent diversification models and ancestral state reconstruction methods we then compared different biogeographic scenarios. We found strong evidence that the rates of colonization into the Andes were higher than the other way round. Those colonizations and the subsequent local diversification at equal rates in the Andes and in non-Andean regions mechanically increased the species richness of Andean regions compared to that of non-Andean regions ('species-attractor' hypothesis). We also found support for increasing speciation rates associated with Andean lineages. Our work highlights the importance of the Andean slopes in repeatedly attracting non-Andean lineages, most likely as a result of the diversity of habitats and/or host plants. Applying this analytical framework to other clades will bring important insights into the evolutionary mechanisms underlying the most species-rich biodiversity hotspot on the planet.