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The Male Sex Pheromone of the Butterfly Bicyclus anynana: Towards an Evolutionary Analysis  [PDF]
Caroline M. Nieberding, Helene de Vos, Maria V. Schneider, Jean-Marc Lassance, Natalia Estramil, Jimmy Andersson, Joakim B?ng, Erik Hedenstr?m, Christer L?fstedt, Paul M. Brakefield
PLOS ONE , 2008, DOI: 10.1371/journal.pone.0002751
Abstract: Background Female sex pheromones attracting mating partners over long distances are a major determinant of reproductive isolation and speciation in Lepidoptera. Males can also produce sex pheromones but their study, particularly in butterflies, has received little attention. A detailed comparison of sex pheromones in male butterflies with those of female moths would reveal patterns of conservation versus novelty in the associated behaviours, biosynthetic pathways, compounds, scent-releasing structures and receiving systems. Here we assess whether the African butterfly Bicyclus anynana, for which genetic, genomic, phylogenetic, ecological and ethological tools are available, represents a relevant model to contribute to such comparative studies. Methodology/Principal Findings Using a multidisciplinary approach, we determined the chemical composition of the male sex pheromone (MSP) in the African butterfly B. anynana, and demonstrated its behavioural activity. First, we identified three compounds forming the presumptive MSP, namely (Z)-9-tetradecenol (Z9-14:OH), hexadecanal (16:Ald ) and 6,10,14-trimethylpentadecan-2-ol (6,10,14-trime-15-2-ol), and produced by the male secondary sexual structures, the androconia. Second, we described the male courtship sequence and found that males with artificially reduced amounts of MSP have a reduced mating success in semi-field conditions. Finally, we could restore the mating success of these males by perfuming them with the synthetic MSP. Conclusions/Significance This study provides one of the first integrative analyses of a MSP in butterflies. The toolkit it has developed will enable the investigation of the type of information about male quality that is conveyed by the MSP in intraspecific communication. Interestingly, the chemical structure of B. anynana MSP is similar to some sex pheromones of female moths making a direct comparison of pheromone biosynthesis between male butterflies and female moths relevant to future research. Such a comparison will in turn contribute to understanding the evolution of sex pheromone production and reception in butterflies.
Temporal Gene Expression Variation Associated with Eyespot Size Plasticity in Bicyclus anynana  [PDF]
Jeffrey C. Oliver, Diane Ramos, Kathleen L. Prudic, Antónia Monteiro
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0065830
Abstract: Seasonal polyphenism demonstrates an organism's ability to respond to predictable environmental variation with alternative phenotypes, each presumably better suited to its respective environment. However, the molecular mechanisms linking environmental variation to alternative phenotypes via shifts in development remain relatively unknown. Here we investigate temporal gene expression variation in the seasonally polyphenic butterfly Bicyclus anynana. This species shows drastic changes in eyespot size depending on the temperature experienced during larval development. The wet season form (larvae reared over 24°C) has large ventral wing eyespots while the dry season form (larvae reared under 19°C) has much smaller eyespots. We compared the expression of three proteins, Notch, Engrailed, and Distal-less, in the future eyespot centers of the two forms to determine if eyespot size variation is associated with heterochronic shifts in the onset of their expression. For two of these proteins, Notch and Engrailed, expression in eyespot centers occurred earlier in dry season than in wet season larvae, while Distal-less showed no temporal difference between the two forms. These results suggest that differences between dry and wet season adult wings could be due to a delay in the onset of expression of these eyespot-associated genes. Early in eyespot development, Notch and Engrailed may be functioning as repressors rather than activators of the eyespot gene network. Alternatively, temporal variation in the onset of early expressed genes between forms may have no functional consequences to eyespot size regulation and may indicate the presence of an 'hourglass' model of development in butterfly eyespots.
Cytogenetic Characterization and AFLP-Based Genetic Linkage Mapping for the Butterfly Bicyclus anynana, Covering All 28 Karyotyped Chromosomes  [PDF]
Arjen E. Van't Hof, Franti?ek Marec, Ilik J. Saccheri, Paul M. Brakefield, Bas J. Zwaan
PLOS ONE , 2008, DOI: 10.1371/journal.pone.0003882
Abstract: Background The chromosome characteristics of the butterfly Bicyclus anynana, have received little attention, despite the scientific importance of this species. This study presents the characterization of chromosomes in this species by means of cytogenetic analysis and linkage mapping. Methodology/Principal Findings Physical genomic features in the butterfly B. anynana were examined by karyotype analysis and construction of a linkage map. Lepidoptera possess a female heterogametic W-Z sex chromosome system. The WZ-bivalent in pachytene oocytes of B. anynana consists of an abnormally small, heterochromatic W-chromosome with the Z-chromosome wrapped around it. Accordingly, the W-body in interphase nuclei is much smaller than usual in Lepidoptera. This suggests an intermediate stage in the process of secondary loss of the W-chromosome to a ZZ/Z sex determination system. Two nucleoli are present in the pachytene stage associated with an autosome and the WZ-bivalent respectively. Chromosome counts confirmed a haploid number of n = 28. Linkage mapping had to take account of absence of crossing-over in females, and of our use of a full-sib crossing design. We developed a new method to determine and exclude the non-recombinant uninformative female inherited component in offspring. The linkage map was constructed using a novel approach that uses exclusively JOINMAP-software for Lepidoptera linkage mapping. This approach simplifies the mapping procedure, avoids over-estimation of mapping distance and increases the reliability of relative marker positions. A total of 347 AFLP markers, 9 microsatellites and one single-copy nuclear gene covered all 28 chromosomes, with a mapping distance of 1354 cM. Conserved synteny of Tpi on the Z-chromosome in Lepidoptera was confirmed for B. anynana. The results are discussed in relation to other mapping studies in Lepidoptera. Conclusions/Significance This study adds to the knowledge of chromosome structure and evolution of an intensively studied organism. On a broader scale it provides an insight in Lepidoptera sex chromosome evolution and it proposes a simpler and more reliable method of linkage mapping than used for Lepidoptera to date.
Male Courtship Rate Plasticity in the Butterfly Bicyclus anynana Is Controlled by Temperature Experienced during the Pupal and Adult Stages  [PDF]
Ashley Bear, Antónia Monteiro
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0064061
Abstract: Environmental cues can act to initiate alternative developmental trajectories that result in different adult phenotypes, including behavioral phenotypes. The developmental period when an organism is sensitive to the cue is often described as a critical period. Here we investigated the critical period for temperature-sensitive courtship rate plasticity in the butterfly Bicyclus anynana. We performed a series of temperature-shift experiments in which larvae, pupae, or adults were shifted for blocks of time from one temperature to an alternative temperature, and then we quantified the courtship rate exhibited by adult males. We discovered that the critical period begins during pupal development and extends into adulthood, but temperature experienced during larval development does not affect male courtship rate. This finding allows us to develop hypotheses that address how developmental and physiological factors may have influenced the evolution of behavioral plasticity in this species.
The composition of cuticular compounds indicates body parts, sex and age in the model butterfly Bicyclus anynana (Lepidoptera)  [PDF]
Stéphanie Heuskin,Maryse Vanderplanck,Marie-Jeanne Holveck,Tobias Engl,Cédric Taverne,Georges Lognay,Caroline M. Nieberding
Frontiers in Ecology and Evolution , 2014, DOI: 10.3389/fevo.2014.00037
Abstract: Chemical communication in insects' sexual interactions is well-known to involve olfaction of volatile compounds called sex pheromones. In theory, sexual chemical communication may also involve chemicals with low or no volatility exchanged during precopulatory gustatory contacts. Yet, knowledge on this latter type of chemicals is so far mostly restricted to the Drosophila fly model. Here we provide the most comprehensive characterization to date of the cuticular chemical profile, including both volatile and non-volatile compounds, of a model butterfly, Bicyclus anynana. First, we characterized the body distribution of 103 cuticular lipids, mostly alkanes and methyl-branched alkanes, by gas chromatography coupled to mass spectrometry (GC-MS). Second, we developed a multivariate statistical approach to cope with such complex chemical profiles and showed that variation in the presence or abundance of a subset of the cuticular lipids indicated body parts, and traits involved in B. anynana mate choice, namely sex and age. Third, we identified the chemical structure of the 20 most indicative compounds, which were on average more abundant (1346.4 ± 1994.6 ng; mean ± SD) than other, likely less indicative, compounds (225.9 ± 507.2 ng; mean ± SD). Fourth, we showed that wings and legs displayed most of the chemical information found on the entire body of the butterflies. Fifth, we showed that non-random gustatory contacts occurred between specific male and female body parts during courtship. The body parts mostly touched by the conspecific displayed the largest between-sex differentiation in cuticular composition. Altogether, the large diversity of cuticular lipids in B. anynana, which exceeds the one of Drosophila flies, and its non-random distribution and evaluation across individuals, together suggest that gustatory information is likely exchanged during sexual interactions in Lepidoptera.
The Genetic, Morphological, and Physiological Characterization of a Dark Larval Cuticle Mutation in the Butterfly, Bicyclus anynana  [PDF]
Ashley Bear,Ariel Simons,Erica Westerman,Antónia Monteiro
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0011563
Abstract: Studies on insect melanism have greatly contributed to our understanding of natural selection and the ultimate factors influencing the evolution of darkly pigmented phenotypes. Research on several species of melanic lepidopteran larvae have found that low levels of circulating juvenile hormone (JH) titers are associated with a melanic phenotype, suggesting that genetic changes in the JH biosynthetic pathway give rise to increased deposition of melanin granules in the cuticle in this group. But does melanism arise through different molecular mechanisms in different species? The present study reports on a Bicyclus anynana (Lepidoptera: Nymphalidae) dark larvae single locus mutation, in which larvae exhibit a darker cuticle relative to wild type. Unlike other lepidopteran melanic larvae mutations, this one is autosomal recessive and does not appear to involve a deficiency in JH titers. Unlike JH deficiency mutants, dark larvae mutants display similar growth rates and sexual behaviors as wild type, and topical application of a JH analogue failed to rescue the wild type cuticular coloration. Finally, transmission electron microscopy showed that sclerotization or deposition of diffuse melanin, rather than deposition of melanin granules, produces the dark coloration found in the cuticle of this species. We conclude that different molecular mechanisms underlie larval melanism in different species of Lepidoptera.
A Gene-Based Linkage Map for Bicyclus anynana Butterflies Allows for a Comprehensive Analysis of Synteny with the Lepidopteran Reference Genome  [PDF]
Patrícia Beldade ,Suzanne V. Saenko,Nicolien Pul,Anthony D. Long
PLOS Genetics , 2009, DOI: 10.1371/journal.pgen.1000366
Abstract: Lepidopterans (butterflies and moths) are a rich and diverse order of insects, which, despite their economic impact and unusual biological properties, are relatively underrepresented in terms of genomic resources. The genome of the silkworm Bombyx mori has been fully sequenced, but comparative lepidopteran genomics has been hampered by the scarcity of information for other species. This is especially striking for butterflies, even though they have diverse and derived phenotypes (such as color vision and wing color patterns) and are considered prime models for the evolutionary and developmental analysis of ecologically relevant, complex traits. We focus on Bicyclus anynana butterflies, a laboratory system for studying the diversification of novelties and serially repeated traits. With a panel of 12 small families and a biphasic mapping approach, we first assigned 508 expressed genes to segregation groups and then ordered 297 of them within individual linkage groups. We also coarsely mapped seven color pattern loci. This is the richest gene-based map available for any butterfly species and allowed for a broad-coverage analysis of synteny with the lepidopteran reference genome. Based on 462 pairs of mapped orthologous markers in Bi. anynana and Bo. mori, we observed strong conservation of gene assignment to chromosomes, but also evidence for numerous large- and small-scale chromosomal rearrangements. With gene collections growing for a variety of target organisms, the ability to place those genes in their proper genomic context is paramount. Methods to map expressed genes and to compare maps with relevant model systems are crucial to extend genomic-level analysis outside classical model species. Maps with gene-based markers are useful for comparative genomics and to resolve mapped genomic regions to a tractable number of candidate genes, especially if there is synteny with related model species. This is discussed in relation to the identification of the loci contributing to color pattern evolution in butterflies.
A wing expressed sequence tag resource for Bicyclus anynana butterflies, an evo-devo model
Patrícia Beldade, Stephen Rudd, Jonathan D Gruber, Anthony D Long
BMC Genomics , 2006, DOI: 10.1186/1471-2164-7-130
Abstract: By targeting cDNAs from developing wings at the stages when pattern is specified, we biased gene discovery towards genes potentially involved in pattern formation. Assembly of 9,903 ESTs from a subtracted library allowed us to identify 4,251 genes of which 2,461 were annotated based on BLAST analyses against relevant gene collections. Gene prediction software identified 2,202 peptides, of which 215 longer than 100 amino acids had no homology to any known proteins and, thus, potentially represent novel or highly diverged butterfly genes. We combined gene and Single Nucleotide Polymorphism (SNP) identification by constructing cDNA libraries from pools of outbred individuals, and by sequencing clones from the 3' end to maximize alignment depth. Alignments of multi-member contigs allowed us to identify over 14,000 putative SNPs, with 316 genes having at least one high confidence double-hit SNP. We furthermore identified 320 microsatellites in transcribed genes that can potentially be used as genetic markers.Our project was designed to combine gene and sequence polymorphism discovery and has generated the largest gene collection available for any butterfly and many potential markers in expressed genes. These resources will be invaluable for exploring the potential of B. anynana in particular, and butterflies in general, as models in ecological, evolutionary, and developmental genetics.The last decade has witnessed an increased effort at bringing together methods and ideas from evolutionary and developmental biology (evo-devo) to explore the genetic basis of morphological diversity [1-7]. Understanding the genetic bases of phenotypic variation is a fundamental challenge for evo-devo and for contemporary biology in general [8]. The color patterns on butterfly wings are a spectacular example of morphological variation, and have been established as an important system in the study of evolution and development [9-11]. These patterns, which vary both across and within species,
Environmental Effects on Temperature Stress Resistance in the Tropical Butterfly Bicyclus Anynana  [PDF]
Klaus Fischer,Anneke Dierks,Kristin Franke,Thorin L. Geister,Magdalena Liszka,Sarah Winter,Claudia Pflicke
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0015284
Abstract: The ability to withstand thermal stress is considered to be of crucial importance for individual fitness and species' survival. Thus, organisms need to employ effective mechanisms to ensure survival under stressful thermal conditions, among which phenotypic plasticity is considered a particularly quick and effective one.
Metabolic Signature of Sun Exposed Skin Suggests Catabolic Pathway Overweighs Anabolic Pathway  [PDF]
Manpreet Randhawa, Vineet Sangar, Samantha Tucker-Samaras, Michael Southall
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0090367
Abstract: Skin chronically exposed to sun results in phenotypic changes referred as photoaging. This aspect of aging has been studied extensively through genomic and proteomic tools. Metabolites, the end product are generated as a result of biochemical reactions are often studied as a culmination of complex interplay of gene and protein expression. In this study, we focused exclusively on the metabolome to study effects from sun-exposed and sun-protected skin sites from 25 human subjects. We generated a highly accurate metabolomic signature for the skin that is exposed to sun. Biochemical pathway analysis from this data set showed that sun-exposed skin resides under high oxidative stress and the chains of reactions to produce these metabolites are inclined toward catabolism rather than anabolism. These catabolic activities persuade the skin cells to generate metabolites through the salvage pathway instead of de novo synthesis pathways. Metabolomic profile suggests catabolic pathways and reactive oxygen species operate in a feed forward fashion to alter the biology of sun exposed skin.
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