[Show abstract][Hide abstract] ABSTRACT: Coevolutionary interactions are thought to have spurred the evolution of key innovations and driven the diversification of much of life on Earth. However, the genetic and evolutionary basis of the innovations that facilitate such interactions remains poorly understood. We examined the coevolutionary interactions between plants (Brassicales) and butterflies (Pieridae), and uncovered evidence for an escalating evolutionary arms-race. Although gradual changes in trait complexity appear to have been facilitated by allelic turnover, key innovations are associated with gene and genome duplications. Furthermore, we show that the origins of both chemical defenses and of molecular counter adaptations were associated with shifts in diversification rates during the arms-race. These findings provide an important connection between the origins of biodiversity, coevolution, and the role of gene and genome duplications as a substrate for novel traits.
Proceedings of the National Academy of Sciences 06/2015; 112(27). DOI:10.1073/pnas.1503926112 · 9.67 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Numerous studies have found amino acid variation at the phosphoglucose isomerase (PGI) gene associated with organismal performance and fitness. Here we focus upon recent advances in the study of this gene, highlighting novel species being studied, new tools being used, and emerging insights into the evolutionary dynamics acting on this gene. Our synthesis highlights questions that are coming into focus, as well as the need for attention in specific areas, such as manipulative experiments to establish mechanistic insights and a causative role of allelic variation.
[Show abstract][Hide abstract] ABSTRACT: Previous studies have reported that chromosome synteny in Lepidoptera has been well conserved, yet the number of haploid chromosomes varies widely from 5 to 223. Here we report the genome (393 Mb) of the Glanville fritillary butterfly (Melitaea cinxia; Nymphalidae), a widely recognized model species in metapopulation biology and eco-evolutionary research, which has the putative ancestral karyotype of n=31. Using a phylogenetic analyses of Nymphalidae and of other Lepidoptera, combined with orthologue-level comparisons of chromosomes, we conclude that the ancestral lepidopteran karyotype has been n=31 for at least 140 My. We show that fusion chromosomes have retained the ancestral chromosome segments and very few rearrangements have occurred across the fusion sites. The same, shortest ancestral chromosomes have independently participated in fusion events in species with smaller karyotypes. The short chromosomes have higher rearrangement rate than long ones. These characteristics highlight distinctive features of the evolutionary dynamics of butterflies and moths.
[Show abstract][Hide abstract] ABSTRACT: The butterfly family Pieridae comprises approximately 1000 described species placed in 85 genera, but the higher classification has not yet been settled. We used molecular data from eight gene regions (one mitochondrial and seven nuclear protein-coding genes) comprising a total of ~6700 bp from 96 taxa to infer a well-supported phylogenetic hypothesis for the family. Based on this hypothesis, we revise the higher classification for all pierid genera. We resurrect the tribe Teracolini stat. rev. in the subfamily Pierinae to include the genera Teracolus, Pinacopteryx, Gideona, Ixias, Eronia, Colotis and most likely Calopieris. We transfer Hebomoia to the tribe Anthocharidini and assign the previously unplaced genera Belenois and Dixeia to the subtribe Aporiina. Three lineages near the base of Pierinae (Leptosia, Elodina and Nepheronia + Pareronia) remain unplaced. For each of these, we describe and delineate new tribes: Elodinini Braby tribus nova, Leptosiaini Braby tribus nova and Nepheroniini Braby tribus nova. The proposed higher classification is based on well-supported monophyletic groups and is likely to remain stable even with the addition of more data.
Zoologica Scripta 08/2014; 43(6). DOI:10.1111/zsc.12075 · 3.22 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The macroevolutionary history of the megadiverse insect order Lepidoptera remains little-known, yet coevolutionary dynamics with their angiospermous host plants are thought to have influenced their diversification significantly. We estimate the divergence times of all higher-level lineages of Lepidoptera, including most extant families. We find that the diversification of major lineages in Lepidoptera are approximately equal in age to the crown group of angiosperms and that there appear to have been three significant increases in diversification rates among Lepidoptera over evolutionary time: 1) at the origin of the crown group of Ditrysia about 150 million years ago (mya), 2) at the origin of the stem group of Apoditrysia about 120 mya and finally 3) a spectacular increase at the origin of the stem group of the quadrifid noctuoids about 70 mya. In addition, there appears to be a significant increase in diversification rate in multiple lineages around 90 mya, which is concordant with the radiation of angiosperms. Almost all extant families appear to have begun diversifying soon after the Cretaceous/Paleogene event 65.51 mya.
PLoS ONE 11/2013; 8(11):e80875. DOI:10.1371/journal.pone.0080875 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Phylogenomic advances provide more rigorous estimates for the timing of evolutionary divergences than previously available (e.g., Bayesian relaxed-clock estimates with soft fossil constraints). However, because many family-level clades and higher, as well as model species within those clades, have not been included in phylogenomic studies, the literature presents temporal estimates likely harboring substantial errors. Blindly using such dates can substantially retard scientific advancement. We suggest a way forward by conducting analyses that minimize prior assumptions and use large datasets, and demonstrate how using such a phylogenomic approach can lead to significantly more parsimonious conclusions without a good fossil record. We suggest that such an approach calls for research into the biological causes of conflict between molecular and fossil signatures.
[Show abstract][Hide abstract] ABSTRACT: Transcriptome studies of insect herbivory are still rare, yet studies in model systems have uncovered patterns of transcript regulation that appear to provide insights into how insect herbivores attain polyphagy, such as a general increase in expression breadth and regulation of ribosomal, digestion- and detoxification-related genes. We investigated the potential generality of these emerging patterns, in the Swedish comma, Polygonia c-album, which is a polyphagous, widely-distributed butterfly. Urtica dioica and Ribes uva-crispa are hosts of P. c-album, but Ribes represents a recent evolutionary shift onto a very divergent host. Utilizing the assembled transcriptome for read mapping, we assessed gene expression finding that caterpillar life-history (i.e. 2nd vs. 4th-instar regulation) had a limited influence on gene expression plasticity. In contrast, differential expression in response to host-plant identified genes encoding serine-type endopeptidases, membrane-associated proteins and transporters. Differential regulation of genes involved in nucleic acid binding was also observed suggesting that polyphagy involves large scale transcriptional changes. Additionally, transcripts coding for structural constituents of the cuticle were differentially expressed in caterpillars in response to their diet indicating that the insect cuticle may be a target for plant defence. Our results state that emerging patterns of transcript regulation from model species appear relevant in species when placed in an evolutionary context.
[Show abstract][Hide abstract] ABSTRACT: Oxygen conductance to the tissues determines aerobic metabolic performance in most eukaryotes but has cost/benefit tradeoffs. Here we examine in lowland populations of a butterfly a genetic polymorphism affecting oxygen conductance via the hypoxia-inducible factor (HIF) pathway, which senses intracellular oxygen and controls the development of oxygen delivery networks. Genetically distinct clades of Glanville fritillary (Melitaea cinxia) across a continental scale maintain, at intermediate frequencies, alleles in a metabolic enzyme (succinate dehydrogenase, SDH) that regulates HIF-1α. One Sdhd allele was associated with reduced SDH activity rate, twofold greater cross-sectional area of tracheoles in flight muscle, and better flight performance. Butterflies with less tracheal development had greater post-flight hypoxia signaling, swollen & disrupted mitochondria, and accelerated aging of flight metabolic performance. Allelic associations with metabolic and aging phenotypes were replicated in samples from different clades. Experimentally elevated succinate in pupae increased the abundance of HIF-1α and expression of genes responsive to HIF activation, including tracheal morphogenesis genes. These results indicate that the hypoxia inducible pathway, even in lowland populations, can be an important axis for genetic variation underlying intraspecific differences in oxygen delivery, physiological performance, and life history.
[Show abstract][Hide abstract] ABSTRACT: Exon structure is relatively well conserved among orthologs in several large clades of species (e.g. Mammalia, Diptera,
Lepidoptera) across evolutionary distances of up to 80 million years. Thus, it should be straightforward to predict the exon
structures in novel species based upon the known exon structures of species that have had their genomes sequenced and well
assembled. Being able to predict the exon boundaries in the genes of novel species is important given the quickly growing numbers
of transcriptome sequencing projects. CEPiNS is a new pipeline for mining exon boundaries of predicted gene sets from model
species and then using this information to identify the exon boundaries in a novel species through codon based alignment. The
pipeline uses the freeware SPIDEY, an exon boundary prediction tool, and BLAST (BLASTN, BLASTP, TBLASTX), both of which
are part of NCBI’s toolkit. CEPiNS provides an important tool to analyze the transcriptome of novel species.
[Show abstract][Hide abstract] ABSTRACT: Background
Marine fish, such as the Atlantic herring (Clupea harengus), often show a low degree of differentiation over large geographical regions. Despite strong environmental gradients (salinity and temperature) in the Baltic Sea, population genetic studies have shown little genetic differentiation among herring in this area, but some evidence for environmentally-induced selection has been uncovered. The mitochondrial genome is a likely target for selection in this system due to its functional role in metabolism.
We sequenced whole mitochondrial genomes for herring from throughout the Baltic region (n=98) in order to investigate evidence for geographical structuring, selection, and associations between genetic and environmental variation. Three well-supported clades that predate the formation of the Baltic Sea were identified, but geographic structuring of this variation was weak (ΦST = 0.036). There was evidence for significant positive selection, particularly in the ND2, ND4 and ND5 genes, and amino acids under significant selection in these genes explained some of the clade formation. Despite uncovering evidence for selection, correlations between genetic diversity or differentiation with environmental factors (temperature, salinity, latitude) were weak.
The results indicate that most of the current mtDNA diversity in herring predates the formation of the Baltic Sea, and that little structuring has evolved since. Thus, fisheries management units in this region cannot be determined on the basis of mtDNA variability. Preliminary evidence for selection underlying clade formation indicates that the NADH complex may be useful for examining adaptation and population structuring at a broader geographical scale.
[Show abstract][Hide abstract] ABSTRACT: The timing of the origin of arthropods in relation to the Cambrian explosion is still controversial, as are the timing of other arthropod macroevolutionary events such as the colonization of land and the evolution of flight. Here we assess the power of a phylogenomic approach to shed light on these major events in the evolutionary history of life on Earth. Analyzing a large phylogenomic dataset (122 taxa, 62 genes) with a Bayesian relaxed molecular clock, we simultaneously reconstructed the phylogenetic relationships and the absolute times of divergences among the arthropods. Simulations were used to test whether our analysis could distinguish between alternative Cambrian explosion scenarios with increasing levels of autocorrelated rate variation. Our analyses support previous phylogenomic hypotheses and simulations indicate a Precambrian origin of the arthropods. Our results provide insights into the three independent colonizations of land by arthropods and suggest that evolution of insect wings happened much earlier than the fossil record indicates, with flight evolving during a period of increasing oxygen levels and impressively large forests. These and other findings provide a foundation for macroevolutionary and comparative genomic study of Arthropoda.
[Show abstract][Hide abstract] ABSTRACT: How well does RNA-Seq data perform for quantitative whole gene expression analysis in the absence of a genome? This is one unanswered question facing the rapidly growing number of researchers studying non-model species. Using Homo sapiens data and resources, we compared the direct mapping of sequencing reads to predicted genes from the genome with mapping to de novo transcriptomes assembled from RNA-Seq data. Gene coverage and expression analysis was further investigated in the non-model context by using increasingly divergent genomic reference species to group assembled contigs by unique genes.
Eight transcriptome sets, composed of varying amounts of Illumina and 454 data, were assembled and assessed. Hybrid 454/Illumina assemblies had the highest transcriptome and individual gene coverage. Quantitative whole gene expression levels were highly similar between using a de novo hybrid assembly and the predicted genes as a scaffold, although mapping to the de novo transcriptome assembly provided data on fewer genes. Using non-target species as reference scaffolds does result in some loss of sequence and expression data, and bias and error increase with evolutionary distance. However, within a 100 million year window these effect sizes are relatively small.
Predicted gene sets from sequenced genomes of related species can provide a powerful method for grouping RNA-Seq reads and annotating contigs. Gene expression results can be produced that are similar to results obtained using gene models derived from a high quality genome, though biased towards conserved genes. Our results demonstrate the power and limitations of conducting RNA-Seq in non-model species.
[Show abstract][Hide abstract] ABSTRACT: Roche 454 sequencing of the transcriptome has become a standard approach for efficiently obtaining single nucleotide polymorphisms (SNPs) in non-model species. In this chapter, the primary issues facing the development of SNPs from the transcriptome in non-model species are presented: tissue and sampling choices, mRNA preparation, considerations of normalization, pooling and barcoding, how much to sequence, how to assemble the data and assess the assembly, calling transcriptome SNPs, developing these into genomic SNPs, and publishing the work. Discussion also covers the comparison of this approach to RAD-tag sequencing and the potential of using other sequencing platforms for SNP development.
[Show abstract][Hide abstract] ABSTRACT: Aim Our study provides a description of the mitogenetic structure of alpine butterflies of the Parnassius phoebus complex throughout their Holarctic distribution. Our analyses extend and reassess population history models for alpine butterflies under an explicit calibration of their mitochondrial DNA (mtDNA) substitution rate.
Location Mountain ranges of the Holarctic region.
Methods A fragment (824 bp) of the mitochondrial cytochrome c oxidase subunit I (COI) gene was sequenced in 203 samples (72 locations), and combined with previously available COI sequences (499 samples), to obtain full coverage of the Holarctic distribution of the P. phoebus complex. A global species distribution model (SDM) was calculated by the maximum entropy (Maxent) approach, allowing assignment of samples into geographically consistent ‘operational’ units. Phylogenetic and coalescent methods were applied to describe the global mitogenetic structure and estimate population genetics parameters. Geological and palaeoecological evidence was used for internal calibration and validation of a COI substitution rate.
Results Eurasian (including Alaskan) and North American populations form two distinct mitochondrial clades. The mitochondrial time to most recent common ancestor (TMRCA) of the North American clade was estimated at less than 125 ka, and the TMRCA of the Eurasian–Alaskan clade at less than 80 ka, except for a single divergent sequence from Mongolia. Pairwise divergence times between all geographical units within each continent date well within the last 100 ka, and most likely, the last 50–10 ka.
Main conclusions In contrast with its currently scattered distribution within each of Eurasia and North America, the mitogenetic structure of the P. phoebus complex in both continents is shallow and weak, and shows no evidence of geographical structure dating back earlier than the last glacial cycle. We argue that mtDNA data are consistent with recent (Würm/Wisconsin) range expansion across each of the two continents and with persistent glacial long-range gene flow which ceased during the Holocene. We propose that P. phoebus may represent a model for Holarctic alpine invertebrates with moderate dispersal abilities in that its genetic structure at a continental scale reflects extensive connectivity during the most recent glacial phases.
[Show abstract][Hide abstract] ABSTRACT: Little is known about variation in gene expression that affects life history traits in wild populations of outcrossing species. Here, we analyse heritability of larval development traits and associated variation in gene expression in the Glanville fritillary butterfly (Melitaea cinxia) across three ecologically relevant temperatures. We studied the development of final-instar larvae, which is greatly affected by temperature, and during which stage larvae build up most of the resources for adult life. Larval development time and weight gain varied significantly among families sampled from hundreds of local populations, indicating substantial heritable variation segregating in the large metapopulation. Global gene expression analysis using common garden-reared F2 families revealed that 42% of the >8000 genes surveyed exhibited significant variation among families, 39% of the genes showed significant variation between the temperature treatments, and 18% showed a significant genotype-by-environment interaction. Genes with large family and temperature effects included larval serum protein and cuticle-binding protein genes, and the expression of these genes was closely correlated with the rate of larval development. Significant expression variation in these same categories of genes has previously been reported among adult butterflies originating from newly established versus old local populations, supporting the notion of a life history syndrome put forward based on ecological studies and involving larval development and adult dispersal capacity. These findings suggest that metapopulation dynamics in heterogeneous environments maintain heritable gene expression variation that affects the regulation of life history traits.