RESUMO
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
Heliconius butterflies provide good examples of both homoploid hybrid speciation and ecological speciation. In particular, examples of adaptive introgression have been detected among the subspecies of Heliconius timareta, which acquired red color pattern elements from H. melpomene. We tested whether the introgression of red wing pattern elements into H. timareta florencia might also be associated with incipient reproductive isolation (RI) from its close relative, H. timareta subsp. nov., found in the eastern Andes. No choice experiments show a 50% reduction in mating between females of H. t. subsp. nov. and males of H .t. florencia, but not in the reciprocal direction. In choice experiments using wing models, males of H. timareta subsp. nov. approach and court red phenotypes less than their own, whereas males of H. t. florencia prefer models with a red phenotype. Intrinsic postzygotic isolation was not detected in crosses between these H. timareta races. These results suggest that a color pattern trait gained by introgression is triggering RI between H. timareta subsp. nov. and H. t. florencia.
Assuntos
Borboletas/anatomia & histologia , Borboletas/genética , Preferência de Acasalamento Animal , Animais , Cor , Sinais (Psicologia) , Feminino , Especiação Genética , Masculino , Pigmentação/genética , Isolamento Reprodutivo , Asas de Animais/anatomia & histologiaRESUMO
The origins of the extraordinary diversity within the Neotropics have long fascinated biologists and naturalists. Yet, the underlying factors that have given rise to this diversity remain controversial. To test the relative importance of Quaternary climatic change and Neogene tectonic and paleogeographic reorganizations in the generation of biodiversity, we examine intraspecific variation across the Heliconius cydno radiation and compare this variation to that within the closely related Heliconius melpomene and Heliconius timareta radiations. Our data, which consist of both mtDNA and genome-scan data from nearly 2250 amplified fragment length polymorphism (AFLP) loci, reveal a complex history of differentiation and admixture at different geographic scales. Both mtDNA and AFLP phylogenies suggest that H. timareta and H. cydno are probably geographic extremes of the same radiation that probably diverged from H. melpomene prior to the Pliocene-Pleistocene boundary, consistent with hypotheses of diversification that rely on geological events in the Pliocene. The mtDNA suggests that this radiation originated in Central America or the northwestern region of South America, with a subsequent colonization of the eastern and western slopes of the Andes. Our genome-scan data indicate significant admixture among sympatric H. cydno/H. timareta and H. melpomene populations across the extensive geographic ranges of the two radiations. Within H. cydno, both mtDNA and AFLP data indicate significant population structure at local scales, with strong genetic differences even among adjacent H. cydno colour pattern races. These genetic patterns highlight the importance of past geoclimatic events, intraspecific gene flow, and local population differentiation in the origin and establishment of new adaptive forms.
Assuntos
Evolução Biológica , Borboletas/genética , Variação Genética , Genética Populacional , Filogenia , Análise do Polimorfismo de Comprimento de Fragmentos Amplificados , Animais , Borboletas/classificação , América Central , DNA Mitocondrial/genética , Filogeografia , Pigmentação , Análise de Sequência de DNA , América do SulRESUMO
Hybrid zones are powerful natural systems to study evolutionary processes to gain an understanding of adaptation and speciation. In the Cauca Valley (Colombia), two butterfly races, Heliconius cydno cydnides and Heliconius cydno weymeri, meet and hybridize. We characterized this hybrid zone using a combination of mitochondrial DNA (mtDNA) sequences, amplified fragment length polymorphisms (AFLPs), microsatellites and sequences for nuclear loci within and outside of the genomic regions that cause differences in wing colour pattern. The hybrid zone is largely composed of individuals of mixed ancestry. However, there is strong genetic discontinuity between the hybridizing races in mtDNA and, to a lesser extent, in all nuclear markers surveyed. The mtDNA clustering of H. c. cydnides with the H. cydno race from the Magdalena Valley and H. c. weymeri with the H. cydno race from the pacific coast suggests that H. c. cydnides colonized the Cauca Valley from the north, whereas H. c. weymeri did so by crossing the Andes in the southern part, implying a secondary contact origin. Colonization of the valley by H. cydno was accompanied by mimicry shift. Strong ecological isolation, driven by locally adaptive differences in mimetic wing patterns, is playing an important role in maintaining the hybrid zone. However, selection on wing pattern alone is not sufficient to explain the genetic discontinuity observed. There is evidence for differences in male mating preference, but the contribution of additional barriers needs further investigation. Overall, our results support the idea that speciation is a cumulative process, where the combination of multiple isolation barriers, combined with major phenotypic differences, facilitates population divergence in face of gene flow.
Assuntos
Borboletas/genética , Quimera , Genética Populacional , Análise do Polimorfismo de Comprimento de Fragmentos Amplificados , Animais , Colômbia , DNA Mitocondrial , Feminino , Especiação Genética , Variação Genética , Masculino , Repetições de Microssatélites , Pigmentação/genética , Seleção Genética , Comportamento Sexual Animal , Asas de AnimaisRESUMO
BACKGROUND: Cryptic population structure can be an indicator of incipient speciation or historical processes. We investigated a previously documented deep break in the mitochondrial haplotypes of Heliconius erato chestertonii to explore the possibility of cryptic speciation, and also the possible presence of endosymbiont bacteria that might drive mitochondrial population structure. RESULTS: Among a sample of 315 individuals from 16 populations of western Colombia, two principal mtDNA clades were detected with 2.15% divergence and we confirmed this structure was weakly associated with geography. The first mtDNA clade included 87% of individuals from northern populations and was the sister group of H. erato members of Andes western, while the second clade contained most individuals from southern populations (78%), which shared haplotypes with an Ecuadorian race of H. erato. In contrast, analysis using AFLP markers showed H. e. chestertonii to be a genetically homogeneous species with no association between mitochondrial divergence and AFLP structure. The lack of congruence between molecular markers suggests that cryptic speciation is not a plausible explanation for the deep mitochondrial divergence in H. e chestertonii. We also carried out the first tests for the presence of endosymbiontic bacteria in Heliconius, and identified two distinct lineages of Wolbachia within H. e. chestertonii. However, neither of the principal mitochondrial clades of H. e. chestertonii was directly associated with the patterns of infection. CONCLUSIONS: We conclude that historical demographic processes are the most likely explanation for the high mitochondrial differentiation in H. e. chestertonii, perhaps due to gene flow between Cauca valley H. e. chestertonii and west Pacific slope populations of H. erato.
Assuntos
Borboletas/genética , DNA Mitocondrial/genética , Evolução Molecular , Especiação Genética , Simbiose , Análise do Polimorfismo de Comprimento de Fragmentos Amplificados , Animais , Bactérias , Borboletas/classificação , Borboletas/microbiologia , Análise por Conglomerados , Colômbia , Genética Populacional , Haplótipos , Filogenia , Polimorfismo Genético , Análise de Sequência de DNARESUMO
The mimetic butterflies Heliconius erato and Heliconius melpomene have undergone parallel radiations to form a near-identical patchwork of over 20 different wing-pattern races across the Neotropics. Previous molecular phylogenetic work on these radiations has suggested that similar but geographically disjunct color patterns arose multiple times independently in each species. The neutral markers used in these studies, however, can move freely across color pattern boundaries, and therefore might not represent the history of the adaptive traits as accurately as markers linked to color pattern genes. To assess the evolutionary histories across different loci, we compared relationships among races within H. erato and within H. melpomene using a series of unlinked genes, genes linked to color pattern loci, and optix, a gene recently shown to control red color-pattern variation. We found that although unlinked genes partition populations by geographic region, optix had a different history, structuring lineages by red color patterns and supporting a single origin of red-rayed patterns within each species. Genes closely linked (80-250 kb) to optix exhibited only weak associations with color pattern. This study empirically demonstrates the necessity of examining phenotype-determining genomic regions to understand the history of adaptive change in rapidly radiating lineages. With these refined relationships, we resolve a long-standing debate about the origins of the races within each species, supporting the hypothesis that the red-rayed Amazonian pattern evolved recently and expanded, causing disjunctions of more ancestral patterns.
Assuntos
Borboletas/genética , Variação Genética , Filogenia , Asas de Animais/metabolismo , Animais , Borboletas/classificação , Região do Caribe , Núcleo Celular/genética , Análise por Conglomerados , DNA Mitocondrial/química , DNA Mitocondrial/genética , Genes de Insetos/genética , Geografia , Haplótipos , Dados de Sequência Molecular , Fenótipo , Pigmentação/genética , Análise de Sequência de DNA , América do Sul , Especificidade da EspécieRESUMO
Homoploid speciation generates species without a change in chromosome number via introgressive hybridization and has been considered rare in animals. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has a color pattern that can be recreated by introgression of the H. melpomene red band into an H. cydno genetic background. Wild H. heurippa males show assortative mating based on color pattern and we here investigate the origin of this preference by studying first-generation backcross hybrids between H. melpomene and H. cydno that resemble H. heurippa. These hybrids show assortative mating preferences, showing a strong preference for their own color pattern over that of either parental species. This is consistent with a genetic basis to wing pattern preference and implies, first, that assortative mating preferences would facilitate the initial establishment of a homozygous hybrid color pattern by increasing the likelihood that early generation hybrids mate among themselves. Second, once established such a lineage would inherit assortative mating preferences that would lead to partial reproductive isolation from parental lineages.
Assuntos
Borboletas , Quimera/genética , Especiação Genética , Preferência de Acasalamento Animal , Animais , Borboletas/anatomia & histologia , Borboletas/genética , Borboletas/fisiologia , Cruzamentos Genéticos , Feminino , Masculino , Pigmentação/genéticaRESUMO
BACKGROUND: Sister species divergence and reproductive isolation commonly results from ecological adaptation. In mimetic Heliconius butterflies, shifts in colour pattern contribute to pre- and post-mating reproductive isolation and are commonly correlated with speciation. Closely related mimetic species are therefore not expected, as they should lack several important sources of reproductive isolation. RESULTS: Here we present phenotypic, behavioral and genetic evidence for the coexistence of two sympatric 'cryptic' species near Florencia in the eastern Andes of Colombia that share the same orange rayed colour pattern. These represent H. melpomene malleti and a novel taxon in the H. cydno group, here designated as novel race of Heliconius timareta, Heliconius timareta florencia. No-choice mating experiments show that these sympatric forms have strong assortative mating ( approximately 96%) despite great similarity in colour pattern, implying enhanced divergence in pheromonal signals. CONCLUSION: We hypothesize that these species might have resulted from recent convergence in colour pattern, perhaps facilitated by hybrid introgression of wing pattern genes.