ABSTRACT
Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species1,2. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation3. Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus, which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture.
Subject(s)
Butterflies , Genetic Introgression , Genetic Speciation , Hybridization, Genetic , Quantitative Trait Loci , Animals , Female , Male , Butterflies/anatomy & histology , Butterflies/classification , Butterflies/genetics , Gene Flow , Genetic Introgression/genetics , Genome, Insect/genetics , Mating Preference, Animal , Phenotype , Pigmentation/genetics , Quantitative Trait Loci/genetics , Reproductive Isolation , Selection, Genetic/genetics , Species Specificity , Sympatry/genetics , Wings, Animal/anatomy & histology , Wings, Animal/metabolismABSTRACT
BACKGROUND: Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri. RESULTS: We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathena is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato, of a small genomic region upstream of the color patterning gene cortex. CONCLUSIONS: Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution.
Subject(s)
Biological Evolution , Butterflies/genetics , Ecosystem , Genome , Hybridization, Genetic , Animals , Brazil , Female , Male , Whole Genome SequencingABSTRACT
The recent publication of a time-tree for the plant family Solanaceae (nightshades) provides the opportunity to use independent calibrations to test divergence times previously inferred for the diverse Neotropical butterfly tribe Ithomiini. Ithomiini includes clades that are obligate herbivores of Solanaceae, with some genera feeding on only one genus. We used 8 calibrations extracted from the plant tree in a new relaxed molecular-clock analysis to produce an alternative temporal framework for the diversification of ithomiines. We compared the resulting age estimates to: (i) a time-tree obtained using 7 secondary calibrations from the Nymphalidae tree of Wahlberg et al. (2009), and (ii) Wahlberg et al.'s (2009) original age estimates for the same clades. We found that Bayesian clock estimates were rather sensitive to a variety of analytical parameters, including taxon sampling. Regardless of this sensitivity however, ithomiine divergence times calibrated with the ages of nightshades were always on average half the age of previous estimates. Younger dates for ithomiine clades appear to fit better with factors long suggested to have promoted diversification of the group such as the uplifting of the Andes, in the case of montane genera. Alternatively, if ithomiines are as old as previous estimates suggest, the recent ages inferred for the diversification of Solanaceae seem likely to be seriously underestimated. Our study exemplifies the difficulty of testing hypotheses of divergence times and of choosing between alternative dating scenarios, and shows that age estimates based on seemingly plausible calibrations may be grossly incongruent.
Subject(s)
Butterflies/classification , Classification/methods , Phylogeny , Animals , Fossils , Solanaceae/classification , TimeABSTRACT
The sugarcane borer, Diatraea saccharalis (F.), is the main pest of sugarcane in Brazil. Genetic variability and gene flow among 13 Brazilian populations of the species were evaluated based on mitochondrial DNA sequences to estimate the exchange of genetic information within and among populations. We found high genetic structure among sampled localities (ΦST=0.50923), and pairwise genetic distances were significantly correlated to geographic distances. Demographic analysis and genealogical network of mitochondrial sequences indicate population growth and admixture of D. saccharalis populations, events likely related to the sequential expansion of the corn and sugarcane crops in Brazil. The implications of these findings for pest management are discussed.
Subject(s)
Genetic Variation , Moths/genetics , Animals , Brazil , Insect Control , PhylogeographyABSTRACT
BACKGROUND: The temporal and geographical diversification of Neotropical insects remains poorly understood because of the complex changes in geological and climatic conditions that occurred during the Cenozoic. To better understand extant patterns in Neotropical biodiversity, we investigated the evolutionary history of three Neotropical swallowtail Troidini genera (Papilionidae). First, DNA-based species delimitation analyses were conducted to assess species boundaries within Neotropical Troidini using an enlarged fragment of the standard barcode gene. Molecularly delineated species were then used to infer a time-calibrated species-level phylogeny based on a three-gene dataset and Bayesian dating analyses. The corresponding chronogram was used to explore their temporal and geographical diversification through distinct likelihood-based methods. RESULTS: The phylogeny for Neotropical Troidini was well resolved and strongly supported. Molecular dating and biogeographic analyses indicate that the extant lineages of Neotropical Troidini have a late Eocene (33-42 Ma) origin in North America. Two independent lineages (Battus and Euryades+Parides) reached South America via the GAARlandia temporary connection, and later became extinct in North America. They only began substantive diversification during the early Miocene in Amazonia. Macroevolutionary analysis supports the "museum model" of diversification, rather than Pleistocene refugia, as the best explanation for the diversification of these lineages. CONCLUSIONS: This study demonstrates that: (i) current Neotropical biodiversity may have originated ex situ; (ii) the GAARlandia bridge was important in facilitating invasions of South America; (iii) colonization of Amazonia initiated the crown diversification of these swallowtails; and (iv) Amazonia is not only a species-rich region but also acted as a sanctuary for the dynamics of this diversity. In particular, Amazonia probably allowed the persistence of old lineages and contributed to the steady accumulation of diversity over time with constant net diversification rates, a result that contrasts with previous studies on other South American butterflies.
Subject(s)
Butterflies/classification , Butterflies/genetics , Phylogeography , Animals , Aristolochia , Bayes Theorem , Biodiversity , Genetic Speciation , South AmericaABSTRACT
Population genetic studies are essential to the better application of pest management strategies, including the monitoring of the evolution of resistance to insecticides and genetically modified plants. Bacillus thuringiensis Berliner (Bt) crops have been instrumental in controlling tobacco budworm, Heliothis virescens (F.) (Lepidoptera: Noctuidae), a pest that has developed resistance to many common insecticides once used for its management. In our study, microsatellite markers were applied to investigate the genetic structure and patterns of gene flow among Brazilian populations of H. virescens from cotton, Gossypium hirsutum L., and soybean, Glycine max (L.) Merr., fields, aiming to propose means to improve its management in the field. In total, 127 alleles were found across nine microsatellites loci for 205 individuals from 12 localities. Low levels of gene flow and moderate to great genetic structure were found for these populations. Host plant association, crop growing season, and geographic origin were not responsible for the genetic structuring among Brazilian populations of H. virescens. Other factors, such as demographic history and seasonal variability of intrapopulation genetic variation, were suggested to be molding the current pattern of genetic variability distribution.
Subject(s)
Gene Flow , Moths/genetics , Animals , Brazil , Genetic Variation , Gossypium , Microsatellite Repeats , Glycine maxABSTRACT
The interdisciplinary field of Chemical Ecology in Brazil is currently composed of groups that emerged through the pioneering studies of Keith Spalding Brown Jr. and José Tércio Barbosa Ferreira. Following Keith Brown 's steps, José Roberto Trigo continued investigating the role of plant natural products in mediating the association among insects and their host plants, mainly in the Order Lepidoptera. The role of pyrrolizidine alkaloids in those associations was investigated extensively by Brown and Trigo, and most of what is currently known on this subject is based on their studies. The present work acknowledges their contribution to the Brazilian chemical ecology field and on insect-plant communication studies mediated by different chemical compounds.
Subject(s)
Lepidoptera , Pyrrolizidine Alkaloids , Animals , Brazil , Ecology , PlantsABSTRACT
The global increase in species richness toward the tropics across continents and taxonomic groups, referred to as the latitudinal diversity gradient, stimulated the formulation of many hypotheses to explain the underlying mechanisms of this pattern. We evaluate several of these hypotheses to explain spatial diversity patterns in a butterfly family, the Nymphalidae, by assessing the contributions of speciation, extinction, and dispersal, and also the extent to which these processes differ among regions at the same latitude. We generate a time-calibrated phylogeny containing 2,866 nymphalid species (~45% of extant diversity). Neither speciation nor extinction rate variations consistently explain the latitudinal diversity gradient among regions because temporal diversification dynamics differ greatly across longitude. The Neotropical diversity results from low extinction rates, not high speciation rates, and biotic interchanges with other regions are rare. Southeast Asia is also characterized by a low speciation rate but, unlike the Neotropics, is the main source of dispersal events through time. Our results suggest that global climate change throughout the Cenozoic, combined with tropical niche conservatism, played a major role in generating the modern latitudinal diversity gradient of nymphalid butterflies.
Subject(s)
Animal Distribution , Biodiversity , Butterflies/physiology , Tropical Climate , Animals , Extinction, Biological , Genes, Insect , Genetic Speciation , Geography , Phylogeny , Spatio-Temporal AnalysisABSTRACT
The Neotropics harbour the most diverse flora and fauna on Earth. The Andes are a major centre of diversification and source of diversity for adjacent areas in plants and vertebrates, but studies on insects remain scarce, even though they constitute the largest fraction of terrestrial biodiversity. Here, we combine molecular and morphological characters to generate a dated phylogeny of the butterfly genus Pteronymia (Nymphalidae: Danainae), which we use to infer spatial, elevational and temporal diversification patterns. We first propose six taxonomic changes that raise the generic species total to 53, making Pteronymia the most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows that Pteronymia originated in the Northern Andes, where it diversified extensively. Some lineages colonized lowlands and adjacent montane areas, but diversification in those areas remained scarce. The recent colonization of lowland areas was reflected by an increase in the rate of evolution of species' elevational ranges towards present. By contrast, speciation rate decelerated with time, with no extinction. The geological history of the Andes and adjacent regions have likely contributed to Pteronymia diversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others.
Subject(s)
Biodiversity , Butterflies/physiology , Animals , Butterflies/anatomy & histology , Butterflies/classification , Calibration , Genetic Speciation , Likelihood Functions , Phylogeny , Phylogeography , Species Specificity , Time FactorsABSTRACT
Proteins containing an Rho GTPase-activating protein (RhoGAP) domain work as molecular switches involved in the regulation of diverse cellular functions. The ability of these GTPases to regulate a wide number of cellular processes conies from their interactions with multiple effectors and inhibitors, including the RhoGAP family, which stimulates their intrinsic GTPase activity. Here, a phylogenetic approach was applied to study the evolutionary relationship among 59 RhoGAP domain-containing proteins. The sequences were aligned by their RhoGAP domains and the phylogenetic hypotheses were generated using Maximum Parsimony and Bayesian analyses. The character tracing of two traits, GTPase activity and presence of other domains, indicated a significant phylogenetic signal for both of them.
Subject(s)
GTPase-Activating Proteins/chemistry , Phylogeny , Algorithms , Animals , Bayes Theorem , Computational Biology , Databases, Protein , Evolution, Molecular , GTP Phosphohydrolases/chemistry , Genetic Techniques , Humans , Internet , Protein Structure, Tertiary , Proteomics , SoftwareABSTRACT
The applicability of mitochondrial nad6 sequences to studies of DNA and population variability in Lepidoptera was tested in four species of economically important moths and one of wild butterflies. The genetic information so obtained was compared to that of cox1 sequences for two species of Lepidoptera. nad6 primers appropriately amplified all the tested DNA targets, the generated data proving to be as informative and suitable in recovering population structures as that of cox1. The proposal is that, to obtain more robust results, this mitochondrial region can be complementarily used with other molecular sequences in studies of low level phylogeny and population genetics in Lepidoptera.
ABSTRACT
Faced by a growing need of identification and delimitation of new and established cryptic species that are being lost at an increasing rate, taxonomists can now more than ever take advantage of an enormous variety of new molecular and computational tools. At this moment they should be open to all new available technologies in the so called 'technology-driven revolution' in systematics. The use of the 'DNA barcode' has been discussed by those applying successfully this approach to identify and diagnose species and by those who believe that the flaws in the use of this molecular marker are as many as to negate the worth of its employment. For insects of the order Lepidoptera neither side seems totally correct or wrong, and although many groups of lepidopterans have been taxonomically resolved by using exclusively or additionally this marker for diagnoses, for others the 'barcode' helped little to resolve taxonomic issues. Here we briefly present some pros and cons of using DNA barcode as a tool in taxonomic studies, with special attention to studies with groups of Lepidoptera developed in the last few years.
Subject(s)
Lepidoptera/classification , Lepidoptera/genetics , Animals , Classification/methodsABSTRACT
The applicability of mitochondrial nad6 sequences to studies of DNA and population variability in Lepidoptera was tested in four species of economically important moths and one of wild butterflies. The genetic information so obtained was compared to that of cox1 sequences for two species of Lepidoptera. nad6 primers appropriately amplified all the tested DNA targets, the generated data proving to be as informative and suitable in recovering population structures as that of cox1. The proposal is that, to obtain more robust results, this mitochondrial region can be complementarily used with other molecular sequences in studies of low level phylogeny and population genetics in Lepidoptera.
Subject(s)
Animals , DNA, Mitochondrial , Genetic Variation , Lepidoptera/genetics , Butterflies , Electron Transport Complex IV , Genetics, Population , Sequence Analysis, DNAABSTRACT
Faced by a growing need of identification and delimitation of new and established cryptic species that are being lost at an increasing rate, taxonomists can now more than ever take advantage of an enormous variety of new molecular and computational tools. At this moment they should be open to all new available technologies in the so called "technology-driven revolution" in systematics. The use of the "DNA barcode" has been discussed by those applying successfully this approach to identify and diagnose species and by those who believe that the flaws in the use of this molecular marker are as many as to negate the worth of its employment. For insects of the order Lepidoptera neither side seems totally correct orwrong, and although many groups of lepidopterans have been taxonomically resolved by using exclusively or additionally this marker for diagnoses, for others the "barcode" helped little to resolve taxonomic issues. Here we briefly present some pros and cons of using DNA barcode as a tool in taxonomic studies, with special attention to studies with groups of Lepidoptera developed in the last few years.
A necessida de crescente de identificação e delimitação de novas espécies, ou de espécies crípticas já estabelecidas, que estão sendo perdidas a uma taxa também crescente, tem levado diversos especialistas a utilizar em uma variedade de ferramentas moleculares e computacionais. Neste momento, taxonomistas devem estar atentos a toda nova tecnologia disponível na chamada "revolução dirigida pela tecnologia"na sistemática, que tem entre as novas ferramentas moleculares a utilização de"DNA barcodes". O uso de "DNA barcode" tem sido amplamente discutido por aqueles que aplicam essa abordagem com sucesso para identificar e diagnosticar espécies, e por aqueles que acreditam que são tantos os problemas no uso desse marcador molecular que não se justifica seu emprego. Para insetos da ordem Lepidoptera nenhum lado parece estar totalmente certo ou errado e, embora alguns grupos de lepidópteros tenham sido resolvidos taxonomicamente pelo uso exclusivo ou adicional desse marcador, para outros o "barcode" ajudou pouco a resolver problemas taxonômicos. Aqui nós apresentamos brevemente prós e contras do uso de "DNA barcode" como ferramenta em estudos taxonômicos, com atenção especial para estudos com grupos de Lepidoptera desenvolvidos nos últimos anos.