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ABSTRACT: Adaptation to divergent ecological niches can result in speciation. Traits subject to disruptive selection that also contribute to non-random mating will facilitate speciation with gene flow. Such 'magic' or 'multiple-effect' traits may be widespread and important for generating biodiversity, but strong empirical evidence is still lacking. Although there is evidence that putative ecological traits are indeed involved in assortative mating, evidence that these same traits are under divergent selection is considerably weaker. Heliconius butterfly wing patterns are subject to positive frequency-dependent selection by predators, owing to aposematism and Müllerian mimicry, and divergent colour patterns are used by closely related species to recognize potential mates. The amenability of colour patterns to experimental manipulation, independent of other traits, presents an excellent opportunity to test their role during speciation. We conducted field experiments with artificial butterflies, designed to match natural butterflies with respect to avian vision. These were complemented with enclosure trials with live birds and real butterflies. Our experiments showed that hybrid colour-pattern phenotypes are attacked more frequently than parental forms. For the first time, we demonstrate disruptive ecological selection on a trait that also acts as a mating cue.
Proceedings of the Royal Society B: Biological Sciences 10/2012; · 5.41 Impact Factor
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ABSTRACT: The Heliconius butterflies are a diverse recent radiation comprising multiple levels of divergence with ongoing gene flow between species. The recently sequenced genome of Heliconius melpomene allowed us to investigate the genomic evolution of this group using dense RAD marker sequencing. Phylogenetic analysis of 54 individuals robustly supported reciprocal monophyly of H. melpomene and Heliconius cydno and refuted previous phylogenetic hypotheses that H. melpomene may be paraphylectic with respect to H. cydno. Heliconius timareta also formed a monophyletic clade closely related but distinct from H. cydno with Heliconius heurippa falling within this clade. We find evidence for genetic admixture between sympatric populations of the sister clades H. melpomene and H. cydno/timareta, particularly between H. cydno and H. melpomene from Central America and between H. timareta and H. melpomene from the eastern slopes of the Andes. Between races, divergence is primarily explained by isolation by distance and there is no detectable genetic population structure between parapatric races, suggesting that hybrid zones between races are not zones of secondary contact. Our results also support previous findings that colour pattern loci are shared between populations and species with similar colour pattern elements. Furthermore, this pattern is almost unique to these genomic regions, with only a very small number of other loci showing significant similarity between populations and species with similar colour patterns.
Molecular Ecology 08/2012; · 5.52 Impact Factor
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Arnaud Martin,
Riccardo Papa,
Nicola J Nadeau,
Ryan I Hill,
Brian A Counterman,
Georg Halder, Chris D Jiggins,
Marcus R Kronforst,
Anthony D Long,
W Owen McMillan,
Robert D Reed
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ABSTRACT: Although animals display a rich variety of shapes and patterns, the genetic changes that explain how complex forms arise are still unclear. Here we take advantage of the extensive diversity of Heliconius butterflies to identify a gene that causes adaptive variation of black wing patterns within and between species. Linkage mapping in two species groups, gene-expression analysis in seven species, and pharmacological treatments all indicate that cis-regulatory evolution of the WntA ligand underpins discrete changes in color pattern features across the Heliconius genus. These results illustrate how the direct modulation of morphogen sources can generate a wide array of unique morphologies, thus providing a link between natural genetic variation, pattern formation, and adaptation.
Proceedings of the National Academy of Sciences 07/2012; 109(31):12632-7. · 9.68 Impact Factor
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ABSTRACT: It is widely documented that hybridisation occurs between many closely related species, but the importance of introgression in adaptive evolution remains unclear, especially in animals. Here, we have examined the role of introgressive hybridisation in transferring adaptations between mimetic Heliconius butterflies, taking advantage of the recent identification of a gene regulating red wing patterns in this genus. By sequencing regions both linked and unlinked to the red colour locus, we found a region that displays an almost perfect genotype by phenotype association across four species, H. melpomene, H. cydno, H. timareta, and H. heurippa. This particular segment is located 70 kb downstream of the red colour specification gene optix, and coalescent analysis indicates repeated introgression of adaptive alleles from H. melpomene into the H. cydno species clade. Our analytical methods complement recent genome scale data for the same region and suggest adaptive introgression has a crucial role in generating adaptive wing colour diversity in this group of butterflies.
PLoS Genetics 06/2012; 8(6):e1002752. · 8.69 Impact Factor
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Kanchon K Dasmahapatra,
James R Walters,
Adriana D Briscoe,
John W Davey,
Annabel Whibley,
Nicola J Nadeau,
Aleksey V Zimin,
Daniel S T Hughes,
Laura C Ferguson,
Simon H Martin, [......],
Richard H Ffrench-Constant,
Mathieu Joron,
Marcus R Kronforst,
Sean P Mullen,
Robert D Reed,
Steven E Scherer,
Stephen Richards,
James Mallet,
W Owen McMillan, Chris D Jiggins
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ABSTRACT: The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.
Nature 05/2012; · 36.28 Impact Factor
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Nicola J Nadeau,
Annabel Whibley,
Robert T Jones,
John W Davey,
Kanchon K Dasmahapatra,
Simon W Baxter,
Michael A Quail,
Mathieu Joron,
Richard H ffrench-Constant,
Mark L Blaxter,
James Mallet, Chris D Jiggins
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ABSTRACT: Heliconius butterflies represent a recent radiation of species, in which wing pattern divergence has been implicated in speciation. Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across the whole Heliconius radiation. Previous studies of population genetic patterns at these regions have sequenced small amplicons. Here, we use targeted next-generation sequence capture to survey patterns of divergence across these entire regions in divergent geographical races and species of Heliconius. This technique was successful both within and between species for obtaining high coverage of almost all coding regions and sufficient coverage of non-coding regions to perform population genetic analyses. We find major peaks of elevated population differentiation between races across hybrid zones, which indicate regions under strong divergent selection. These 'islands' of divergence appear to be more extensive between closely related species, but there is less clear evidence for such islands between more distantly related species at two further points along the 'speciation continuum'. We also sequence fosmid clones across these regions in different Heliconius melpomene races. We find no major structural rearrangements but many relatively large (greater than 1 kb) insertion/deletion events (including gain/loss of transposable elements) that are variable between races.
Philosophical Transactions of The Royal Society B Biological Sciences 02/2012; 367(1587):343-53. · 6.40 Impact Factor
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ABSTRACT: Heliconius butterflies are an excellent system for understanding the genetic basis of phenotypic change. Here we document surprising diversity in the genetic control of a common phenotype. Two disjunct H. erato populations have each recruited the Cr and/or Sd loci that control similar yellow hindwing patterns, but the alleles involved partially complement one another indicating either multiple origins for the patterning alleles or developmental drift in genetic control of similar patterns. We show that in these H. erato populations cr and sd are epistatically interacting and that the parental origin of alleles can explain phenotypes of backcross individuals. In contrast, mimetic H. melpomene populations with identical phenotypes (H. m. rosina and H. m. amaryllis) do not show genetic complementation (F(1)s and F(2)s are phenotypically identical to parentals). Finally, we report hybrid female inviability in H. m. melpomene × H. m. rosina crosses (previously only female infertility had been reported) and presence of standing genetic variation for alternative color alleles at the Yb locus in true breeding H. melpomene melpomene populations (expressed when in a different genomic background) that could be an important source of variation for the evolution of novel phenotypes or a result of developmental drift. Although recent work has emphasized the simple genetic control of wing pattern in Heliconius, we show there is underlying complexity in the allelic variation and epistatic interactions between major patterning loci.
PLoS ONE 01/2012; 7(10):e48627. · 4.09 Impact Factor
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ABSTRACT: 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.
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.
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.
BMC Evolutionary Biology 12/2011; 11:358. · 3.52 Impact Factor
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ABSTRACT: The evolution of pigmentation in vertebrates and flies has involved repeated divergence at a small number of genes related to melanin synthesis. Here, we study insect melanin synthesis genes in Heliconius butterflies, a group characterised by its diversity of wing patterns consisting of black (melanin), and yellow and red (ommochrome) pigmented scales. Consistent with their respective biochemical roles in Drosophila melanogaster, ebony is upregulated in non-melanic wing regions destined to be pigmented red whilst tan is upregulated in melanic regions. Wing regions destined to be pigmented yellow, however, are downregulated for both genes. This pattern is conserved across multiple divergent and convergent phenotypes within the Heliconii, suggesting a conserved mechanism for the development of black, red and yellow pattern elements across the genus. Linkage mapping of five melanin biosynthesis genes showed that, in contrast to other organisms, these genes do not control pattern polymorphism. Thus, the pigmentation genes themselves are not the locus of evolutionary change but lie downstream of a wing pattern regulatory factor. The results suggest a modular system in which particular combinations of genes are switched on whenever red, yellow or black pattern elements are favoured by natural selection for diverse and mimetic wing patterns.
Archiv für Entwickelungsmechanik der Organismen 12/2011; 221(5-6):297-308. · 1.77 Impact Factor
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Heather M Hines,
Brian A Counterman,
Riccardo Papa,
Priscila Albuquerque de Moura,
Marcio Z Cardoso,
Mauricio Linares,
James Mallet,
Robert D Reed, Chris D Jiggins,
Marcus R Kronforst,
W Owen McMillan
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ABSTRACT: 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.
Proceedings of the National Academy of Sciences 11/2011; 108(49):19666-71. · 9.68 Impact Factor
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Mathieu Joron,
Lise Frezal,
Robert T Jones,
Nicola L Chamberlain,
Siu F Lee,
Christoph R Haag,
Annabel Whibley,
Michel Becuwe,
Simon W Baxter,
Laura Ferguson, [......],
Richard Clark,
Michael A Quail,
Helen Beasley,
Rebecca Glithero,
Christine Lloyd,
Sarah Sims,
Matthew C Jones,
Jane Rogers, Chris D Jiggins,
Richard H ffrench-Constant
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ABSTRACT: Supergenes are tight clusters of loci that facilitate the co-segregation of adaptive variation, providing integrated control of complex adaptive phenotypes. Polymorphic supergenes, in which specific combinations of traits are maintained within a single population, were first described for 'pin' and 'thrum' floral types in Primula and Fagopyrum, but classic examples are also found in insect mimicry and snail morphology. Understanding the evolutionary mechanisms that generate these co-adapted gene sets, as well as the mode of limiting the production of unfit recombinant forms, remains a substantial challenge. Here we show that individual wing-pattern morphs in the polymorphic mimetic butterfly Heliconius numata are associated with different genomic rearrangements at the supergene locus P. These rearrangements tighten the genetic linkage between at least two colour-pattern loci that are known to recombine in closely related species, with complete suppression of recombination being observed in experimental crosses across a 400-kilobase interval containing at least 18 genes. In natural populations, notable patterns of linkage disequilibrium (LD) are observed across the entire P region. The resulting divergent haplotype clades and inversion breakpoints are found in complete association with wing-pattern morphs. Our results indicate that allelic combinations at known wing-patterning loci have become locked together in a polymorphic rearrangement at the P locus, forming a supergene that acts as a simple switch between complex adaptive phenotypes found in sympatry. These findings highlight how genomic rearrangements can have a central role in the coexistence of adaptive phenotypes involving several genes acting in concert, by locally limiting recombination and gene flow.
Nature 08/2011; 477(7363):203-6. · 36.28 Impact Factor
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ABSTRACT: Despite the prominent and worldwide use of Bacillus thuringiensis (Bt) insecticidal toxins in agriculture, knowledge of the mechanism by which they kill pests remains incomplete. Here we report genetic mapping of a membrane transporter (ABCC2) to a locus controlling Bt Cry1Ac toxin resistance in two lepidopterans, implying that this protein plays a critical role in Bt function.
Genetics 08/2011; 189(2):675-9. · 4.01 Impact Factor
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Robert D Reed,
Riccardo Papa,
Arnaud Martin,
Heather M Hines,
Brian A Counterman,
Carolina Pardo-Diaz, Chris D Jiggins,
Nicola L Chamberlain,
Marcus R Kronforst,
Rui Chen,
Georg Halder,
H Frederik Nijhout,
W Owen McMillan
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ABSTRACT: Mimicry--whereby warning signals in different species evolve to look similar--has long served as a paradigm of convergent evolution. Little is known, however, about the genes that underlie the evolution of mimetic phenotypes or to what extent the same or different genes drive such convergence. Here, we characterize one of the major genes responsible for mimetic wing pattern evolution in Heliconius butterflies. Mapping, gene expression, and population genetic work all identify a single gene, optix, that controls extreme red wing pattern variation across multiple species of Heliconius. Our results show that the cis-regulatory evolution of a single transcription factor can repeatedly drive the convergent evolution of complex color patterns in distantly related species, thus blurring the distinction between convergence and homology.
Science 07/2011; 333(6046):1137-41. · 31.20 Impact Factor
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ABSTRACT: The origin and evolution of supergenes have long fascinated evolutionary biologists. In the polymorphic butterfly Heliconius numata, a supergene controls the switch between multiple different forms, and results in near-perfect mimicry of model species. Here, we use a morphometric analysis to quantify the variation in wing pattern observed in two broods of H. numata with different alleles at the supergene locus, 'P'. Further, we genotype the broods to associate the variation we capture with genetic differences. This allows us to begin mapping the quantitative trait loci that have minor effects on wing pattern. In addition to finding loci on novel chromosomes, our data, to our knowledge, suggest for the first time that ancestral colour-pattern loci, known to have major effects in closely related species, may contribute to the wing patterns displayed by H. numata, despite the large transfer of effects to the supergene.
Proceedings of the Royal Society B: Biological Sciences 06/2011; 279(1727):316-25. · 5.41 Impact Factor
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ABSTRACT: Premating behavioral isolation is increasingly recognized as an important part of ecological speciation, where divergent natural selection causes the evolution of reproductive barriers. A number of studies have now demonstrated that traits under divergent natural selection also affect mate preferences. However, studies of single species pairs only capture a snapshot of the speciation process, making it difficult to assess the role of mate preferences throughout the entire process. Heliconius butterflies are well known for their brightly colored mimetic warning patterns, and previous studies have shown that these patterns are also used as mate recognition cues. Here, we present mate preference data for four pairs of sister taxa, representing different stages of divergence, which together allow us to compare diverging mate preferences across the continuum of Heliconius speciation. Using a novel Bayesian approach, our results support a model of ecological speciation in which strong premating isolation arises early, but continues to increase throughout the continuum from polymorphic populations through to "good," sympatric ecologically divergent species.
Evolution 05/2011; 65(5):1489-500. · 5.15 Impact Factor
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ABSTRACT: Ecological speciation proceeds through the accumulation of divergent traits that contribute to reproductive isolation, but in the face of gene flow traits that characterize incipient species may become disassociated through recombination. Heliconius butterflies are well known for bright mimetic warning patterns that are also used in mate recognition and cause both pre- and post-mating isolation between divergent taxa. Sympatric sister taxa representing the final stages of speciation, such as Heliconius cydno and Heliconius melpomene, also differ in ecology and hybrid fertility. We examine mate preference and sterility among offspring of crosses between these species and demonstrate the clustering of Mendelian colour pattern loci and behavioural loci that contribute to reproductive isolation. In particular, male preference for red patterns is associated with the locus responsible for the red forewing band. Two further colour pattern loci are associated, respectively, with female mating outcome and hybrid sterility. This genetic architecture in which 'speciation genes' are clustered in the genome can facilitate two controversial models of speciation, namely divergence in the face of gene flow and hybrid speciation.
Proceedings of the Royal Society B: Biological Sciences 02/2011; 278(1705):511-8. · 5.41 Impact Factor
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ABSTRACT: Heliconius butterflies are an excellent system for studies of adaptive convergent and divergent phenotypic traits. Wing colour patterns are used as signals to both predators and potential mates and are inherited in a Mendelian manner. The underlying genetic mechanisms of pattern formation have been studied for many years and shed light on broad issues, such as the repeatability of evolution. In Heliconius melpomene, the yellow hindwing bar is controlled by the HmYb locus. MicroRNAs (miRNAs) are important post-transcriptional regulators of gene expression that have key roles in many biological processes, including development. miRNAs could act as regulators of genes involved in wing development, patterning and pigmentation. For this reason we characterised miRNAs in developing butterfly wings and examined differences in their expression between colour pattern races.
We sequenced small RNA libraries from two colour pattern races and detected 142 Heliconius miRNAs with homology to others found in miRBase. Several highly abundant miRNAs were differentially represented in the libraries between colour pattern races. These candidates were tested further using Northern blots, showing that differences in expression were primarily due to developmental stage rather than colour pattern. Assembly of sequenced reads to the HmYb region identified hme-miR-193 and hme-miR-2788; located 2380 bp apart in an intergenic region. These two miRNAs are expressed in wings and show an upregulation between 24 and 72 hours post-pupation, indicating a potential role in butterfly wing development. A search for miRNAs in all available H. melpomene BAC sequences (~2.5 Mb) did not reveal any other miRNAs and no novel miRNAs were predicted.
Here we describe the first butterfly miRNAs and characterise their expression in developing wings. Some show differences in expression across developing pupal stages and may have important functions in butterfly wing development. Two miRNAs were located in the HmYb region and were expressed in developing pupal wings. Future work will examine the expression of these miRNAs in different colour pattern races and identify miRNA targets among wing patterning genes.
BMC Genomics 01/2011; 12:62. · 4.07 Impact Factor
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ABSTRACT: The yellow gene family is intriguing for a number of reasons. To date, yellow-like genes have only been identified in insect species and a number of bacteria. The function of the yellows is largely unknown, although a few have been associated with melanization and behavior in Drosophila, and a unique clade of genes from Apis mellifera may be involved in caste specification. Here, we show that yellow-like sequences are present in bacteria, insects, and fungi but absent from other eukaryotes apart from isolated putative sequences in Amphioxus, the Salmon Louse, and Naegleria. The yellow-like family forms a discrete gene class characterized by the presence of a major royal jelly protein domain, but eukaryote yellow-like proteins are not monophyletic. The unusual phylogenetic distribution of yellow-like sequences suggests either multiple horizontal transfer from bacteria into eukaryotes or extensive gene loss in eukaryote lineages. Comparative analysis of yellow family synteny and gene order demonstrates that a highly conserved block of three to five genes has been maintained throughout insect diversification despite extensive genome rearrangements. We show strong purifying selection on seven yellow genes over approximately 100 My separating the silkmoth and Heliconius butterflies and an association between spatial regulation of gene expression and distribution of melanic pigment in the developing butterfly wing. A single ancestral yellow-like gene has therefore undergone multiple rounds of duplication within the insects accompanied by functional constraint on both genomic location and protein evolution.
Molecular Biology and Evolution 01/2011; 28(1):257-72. · 5.55 Impact Factor
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ABSTRACT: Restriction-site associated DNA (RAD) sequencing is a powerful new method for targeted sequencing across the genomes of many individuals. This approach has broad potential for genetic analysis of non-model organisms including genotype-phenotype association mapping, phylogeography, population genetics and scaffolding genome assemblies through linkage mapping. We constructed a RAD library using genomic DNA from a Plutella xylostella (diamondback moth) backcross that segregated for resistance to the insecticide spinosad. Sequencing of 24 individuals was performed on a single Illumina GAIIx lane (51 base paired-end reads). Taking advantage of the lack of crossing over in homologous chromosomes in female Lepidoptera, 3,177 maternally inherited RAD alleles were assigned to the 31 chromosomes, enabling identification of the spinosad resistance and W/Z sex chromosomes. Paired-end reads for each RAD allele were assembled into contigs and compared to the genome of Bombyx mori (n = 28) using BLAST, revealing 28 homologous matches plus 3 expected fusion/breakage events which account for the difference in chromosome number. A genome-wide linkage map (1292 cM) was inferred with 2,878 segregating RAD alleles inherited from the backcross father, producing chromosome and location specific sequenced RAD markers. Here we have used RAD sequencing to construct a genetic linkage map de novo for an organism that has no previous genome data. Comparative analysis of P. xyloxtella linkage groups with B. mori chromosomes shows for the first time, genetic synteny appears common beyond the Macrolepidoptera. RAD sequencing is a powerful system capable of rapidly generating chromosome specific data for non-model organisms.
PLoS ONE 01/2011; 6(4):e19315. · 4.09 Impact Factor
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ABSTRACT: Studies of the genetic basis of adaptive changes in natural populations are now addressing questions that date back to the beginning of evolutionary biology, such as whether evolution proceeds in a gradual or discontinuous manner, and whether convergent evolution involves convergent genetic changes. Studies that combine quantitative genetics and population genomics provide a powerful tool for identifying genes controlling recent adaptive change. Accumulating evidence shows that single loci, and in some cases single mutations, often have major effects on phenotype. This implies that discontinuous evolution, with rapid changes in phenotype, could occur frequently in natural populations. Furthermore, convergent evolution commonly involves the same genes. This implies a surprising predictability underlying the genetic basis of evolutionary changes. Nonetheless, most studies of recent evolution involve the loss of traits, and we still understand little of the genetic changes needed in the origin of novel traits.
Trends in Genetics 11/2010; 26(11):484-92. · 10.06 Impact Factor
