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Meier, J. I.

Publications and source records attributed to Meier, J. I..

14 recordsLinked to original sources

338 coleopteran genomes reveal exceptional rearrangement variation compared to other insect orders

Chromosomal rearrangements reshape genome architecture, but rate variation across the tree of life remains poorly understood. Analysing 338 beetle (Coleoptera) genomes, we inferred eight ancestral linkage groups. No species retained these linkage groups, whereas the most frequent karyotypes of 10 or 11 chromosomes evolved at least 65 times through independent rearrangements. Rearrangement rates vary widely across lineages, with exceptionally high rates associated with major species radiations. Comparisons to 340 fly and 210 butterfly and moth genomes reveal the highest rates of long-term persistent rearrangements in beetles and that the beetle X chromosome traces back to the ancestor of Holometabola. We identified frequent X chromosome changes, mostly representing recent autosomal-X fusions, but no fissions. For autosomes, key rearrangement predictors include chromosome size, repeats and centromere position.

evolutionary biology↗

Highly modular genomic architecture underlies combinatorial mechanism of speciation and adaptive radiation

Hybridisation can fuel rapid adaptive radiation, but how it enables the formation of phenotypically highly dimensional species-rich radiations remains unclear. We investigated this by analysing genotype-phenotype associations for 14 ecological (trophic, body patterns) and mating traits (nuptial colour) across 107 species of Lake Victoria cichlid fishes. We find weak trait covariance across the radiation, with many different trait combinations constituting different species. Across the radiation, polygenic, redundant, and lowly pleiotropic genomic architectures of hybrid origin underlie the repeated evolution of key traits. Such independent genomic modules can be reshuffled and recombined like Lego bricks, generating diverse trait combinations from a finite number of elements. During speciation, dispersed oligogenic trait modules become coupled through long-range linkage disequilibrium. We propose that this genomic and phenotypic modularity emerged from repeated cycles of past hybridisation, enabling superfast adaptive radiation through combinatorial speciation.

evolutionary biology↗

Genetic parallelism underpins convergent mimicry coloration across Lepidoptera

Convergent evolution, the repeated evolution of similar phenotypes in response to the same selective pressures across multiple lineages, is widespread in nature. The extent to which the same genetic mechanisms contribute to convergent evolution could reveal whether the pathway towards these optimal endpoints is flexible or constrained to follow a particular route. Although mimicry of aposematic colour patterns is well known in Lepidoptera, our knowledge of the genetic basis of these convergent patterns is mostly restricted to a few closely-related species. Here we study the genetic basis of mimicry across seven species of Ithomiini and Heliconius butterflies and a day-flying Chetone moth, representing lineages that diverged between [~]1-120 Mya, each presenting similar colour pattern switches. In all the butterfly species, the genetic variants most strongly associated with convergent colour pattern switches are similarly located in non-coding regions near the genes ivory and optix. Colour pattern variation in the moth is associated with a [~]1 Mb inversion around ivory paralleling the supergene architecture of the co-mimic Heliconius numata. In contrast to previous studies in Heliconius, there is limited evidence of alleles shared by means of hybridization in convergence among closely-related ithomiine species. Repeated parallel evolution of regulatory switches via reuse of the same two genes suggests that convergent colour pattern evolution is highly constrained, even across large evolutionary timescales.

evolutionary biology↗

Genomes reveal age and demographic consequence of ultrafast adaptive radiation

New species typically evolve over several million years1. However, rates of speciation and ecological diversification vary by orders of magnitude across the tree of life1-3, with the fastest shown by some adaptive radiations. Eight hundred endemic species of cichlid fishes emerged and formed entire food webs in Lake Victoria and nearby lakes in East Africa. According to Victorias paleolimnological history4, five hundred may have arisen within the past 16,700 years, but molecular phylogenies estimated a much older origin5-8. We reconstruct the age and demography of all Lake Victoria region radiations from whole genomes. We show that indeed, in Lake Victoria all trophic guilds diverged <16,700 years ago, corresponding to between 537 and nearly 30000 speciation events per species per million years, the fastest speciation rate in metazoans1,2. Cichlid radiations in lakes Edward, Albert and Kivu too began <20,000 years ago, an order of magnitude faster than previously thought. Evolutionary transitions between trophic levels led to divergence in effective population sizes as predicted by the trophic pyramid of numbers concept9 and replicated across three parallel food web radiations. Our results demonstrate that classical theory of trophic interactions in ecologically assembled food webs applies equally to food webs that assembled through rapid adaptive radiation.

evolutionary biology↗

Genomics of Neotropical biodiversity indicators: two butterfly radiations with rampant chromosomal rearrangements and hybridisation

A major question in evolutionary biology is what drives the diversification of lineages. Rapid, recent radiations are ideal systems for addressing how new species arise because they still show key morphological and ecological adaptations associated with speciation. While most studied recent radiations have evolved in an insular environment, less research has been carried out on continental radiations with complex species interactions. Melinaea and Mechanitis butterflies (Nymphalidae: Ithomiini) have rapidly radiated in the Neotropics. They are classical models for Amazonian biogeography and colour pattern mimicry and have been proposed as biodiversity indicators. We generated reference genomes for five species of each genus, and whole-genome resequencing data of most species and subspecies covering a wide geographic range to assess phylogeographic relationships, patterns of hybridisation and chromosomal rearrangements. Our data help resolve the classification of these taxonomically challenging butterflies and reveal very high diversification rates. We find rampant evidence of historical hybridisation and putative hybrid species in both radiations, which may have facilitated their rapid diversification. Moreover, dozens of chromosomal fusions and fissions were identified between congeneric species, and even some within species. We conclude that interactions between geography, hybridisation and chromosomal rearrangements have contributed to these two rapid radiations in the highly diverse Neotropical region. We suggest that rapid radiations may be spurred by repeated periods of geographic isolation during Pleistocene climate oscillations, combined with lineage-specific rapid accumulation of incompatibilities during allopatric phases, followed by secondary contact with some gene exchange. Significance StatementUnderstanding factors contributing to rapid speciation is a key aim of evolutionary biology. Here we focus on two rapid radiations of Neotropical butterflies. Our genomic data with broad taxonomic and geographic coverage reveal rampant hybridisation and chromosomal rearrangements, each likely contributing to the high diversification rates. Our study highlights the use of genomic data to resolve taxonomically challenging species groups and elucidate drivers of diversification in rapid radiations. We show that for biodiversity hotspots with recent radiations, barcoding is insufficient to characterise species richness due to gene flow and recent speciation. The taxonomic implications of both introgression and karyotype diversity for species delimitation are important to consider during monitoring and management of biodiversity in these vulnerable habitats.

evolutionary biology↗

Cryptic diversity and signatures of domestication in the Black Soldier Fly (Hermetia illucens)

The Black Soldier Fly (Hermetia illucens) is the main species in the developing global industry of insects as food and feed, but little is known about its natural diversity or the genetic basis of its domestication. We obtained whole genome sequences for 54 individuals from both wild and captive populations. We identified two genetic lineages at least 3 million years divergent, revealing cryptic diversity within the species. Our study indicates that the most common populations used for commercial and academic applications are primarily derived from just one of these lineages, likely originating from a wild North American progenitor. We find that captive populations show strong reductions in genetic diversity, consistent with genome-wide effects of population bottlenecks and drift associated with rearing in captivity. Some limited evidence of gene flow between divergent lineages was observed, as well as evidence of hybridisation from domesticated populations into the wild. Our study suggests that natural genetic diversity could provide important variation for industrial purposes in this novel agricultural species. Author SummaryAnimals and plants have been domesticated by humans over thousands of years, shaping their genomes and yielding beneficial or improved traits for agriculture. Insect farming has recently reached industrial scales in order to recycle organic wastes into feed and food grade material. The Black Soldier Fly is the flagship insect species in this novel agriculture sector. However, the understanding of its evolutionary history and the genetic impact of intense farming has not been well studied to date. We examined whole genomes from populations sampled from across the worldwide distribution of Black Soldier Fly to investigate the impact of domestication and reveal the evolutionary history of the species. We found that farmed populations show distinct genomic regions showing reduced variation that could represent signatures of selection or demographic effects. We also identify two distinct lineages of Black Soldier Fly that have been diverging for millions of years, comparable to divergence between different species in other insect groups, yet show evidence of genetic exchange, indicating a lack of reproductive incompatibility in the populations tested. This work is the first to describe the genetic impact of domestication in the Black Soldier Fly and provide evolutionary insights using whole genomes. These results imply that considerable wild diversity could be harnessed for improving agricultural efficiency.

genomics↗

Repeated genetic adaptation to high altitude in two tropical butterflies

Repeated evolution can provide insight into the mechanisms that facilitate adaptation to novel or changing environments. Here we study adaptation to high altitude in two divergent tropical butterflies, H. erato and H. melpomene, which have repeatedly and independently adapted to high elevations on either side of the Andean mountains. We sequenced 518 whole genomes from elevational transects and found many regions under selection at high altitude, with repeated genetic differentiation across multiple replicates, including allopatric comparisons. In contrast, there is little molecular parallelism between H. erato and H. melpomene. With a further 85 whole genomes of five close relatives, we find that a large proportion divergent regions have arisen from standing variation and putative adaptive introgression from high-altitude specialist species. Taken together our study supports a key role of standing genetic variation and gene flow from pre-adapted species in promoting parallel genetic local adaptation to the environment.

evolutionary biology↗

Genomics of altitude-associated wing shape in two tropical butterflies

Understanding how organisms adapt to their local environment is central to evolution. With new whole-genome sequencing technologies and the explosion of data, deciphering the genomic basis of complex traits that are ecologically relevant is becoming increasingly feasible. Here we study the genomic basis of wing shape in two Neotropical butterflies that inhabit large geographical ranges. Heliconius butterflies at high elevations have been shown to generally have rounder wings than those in the lowlands. We reared over 1100 butterflies from 71 broods of H. erato and H. melpomene in common-garden conditions and show that wing aspect ratio, i.e. elongatedness, is highly heritable in both species and elevation-associated wing shape differences are maintained. Genome-wide associations with a published dataset of 666 whole genomes from across a hybrid zone, uncovered a highly polygenic basis to wing shape variation in the wild. We identify several genes that have roles in wing morphogenesis or wing shape variation in Drosophila flies, making them promising candidates for future studies. There was little evidence for molecular parallelism in the two species, with only one shared candidate gene, nor for a role of the four known colour pattern loci, except for optix in H. erato. Thus, we present the first insights into the heritability and genomic basis of within-species wing shape in two Heliconius species, adding to a growing body of evidence that polygenic adaptation may underlie many ecologically relevant traits.

evolutionary biology↗

Haplotype tagging reveals parallel formation of hybrid races in two butterfly species

Genetic variation segregates as linked sets of variants, or haplotypes. Haplotypes and linkage are central to genetics and underpin virtually all genetic and selection analysis. And yet, genomic data often lack haplotype information, due to constraints in sequencing technologies. Here we present "haplotagging", a simple, low-cost linked-read sequencing technique that allows sequencing of hundreds of individuals while retaining linkage information. We apply haplotagging to construct megabase-size haplotypes for over 600 individual butterflies (Heliconius erato and H. melpomene), which form overlapping hybrid zones across an elevational gradient in Ecuador. Haplotagging identifies loci controlling distinctive high- and lowland wing color patterns. Divergent haplotypes are found at the same major loci in both species, while chromosome rearrangements show no parallelism. Remarkably, in both species the geographic clines for the major wing pattern loci are displaced by 18 km, leading to the rise of a novel hybrid morph in the centre of the hybrid zone. We propose that shared warning signalling (Mullerian mimicry) may couple the cline shifts seen in both species, and facilitate the parallel co-emergence of a novel hybrid morph in both co-mimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations. One-sentence summaryHaplotagging, a novel linked-read sequencing technique that enables whole genome haplotyping in large populations, reveals the formation of a novel hybrid race in parallel hybrid zones of two co-mimicking Heliconius butterfly species through strikingly parallel divergences in their genomes.

evolutionary biology↗

A haplotype-resolved, de novo genome assembly for the wood tiger moth (Arctia plantaginis) through trio binning

BackgroundDiploid genome assembly is typically impeded by heterozygosity, as it introduces errors when haplotypes are collapsed into a consensus sequence. Trio binning offers an innovative solution which exploits heterozygosity for assembly. Short, parental reads are used to assign parental origin to long reads from their F1 offspring before assembly, enabling complete haplotype resolution. Trio binning could therefore provide an effective strategy for assembling highly heterozygous genomes which are traditionally problematic, such as insect genomes. This includes the wood tiger moth (Arctia plantaginis), which is an evolutionary study system for warning colour polymorphism. FindingsWe produced a high-quality, haplotype-resolved assembly for Arctia plantaginis through trio binning. We sequenced a same-species family (F1 heterozygosity [~]1.9%) and used parental Illumina reads to bin 99.98% of offspring Pacific Biosciences reads by parental origin, before assembling each haplotype separately and scaffolding with 10X linked-reads. Both assemblies are highly contiguous (mean scaffold N50: 8.2Mb) and complete (mean BUSCO completeness: 97.3%), with complete annotations and 31 chromosomes identified through karyotyping. We employed the assembly to analyse genome-wide population structure and relationships between 40 wild resequenced individuals from five populations across Europe, revealing the Georgian population as the most genetically differentiated with the lowest genetic diversity. ConclusionsWe present the first invertebrate genome to be assembled via trio binning. This assembly is one of the highest quality genomes available for Lepidoptera, supporting trio binning as a potent strategy for assembling highly heterozygous genomes. Using this assembly, we provide genomic insights into geographic population structure of Arctia plantaginis.

genomics↗

Movement of transposable elements contributes to cichlid diversity

African cichlid fishes are a prime model for studying the mechanisms of speciation. Despite the development of extensive genomic resources, it has been difficult to determine which sources of genetic variation are responsible for variation in cichlid phenotypes. Cichlids have some of the largest known shifts in vertebrate visual sensitivity. These shifts arise mainly from the differential expression of seven cone opsin genes. By mapping expression quantitative trait loci (eQTL) in intergeneric crosses of Lake Malawi (LM) cichlids, we have thus far identified four causative genetic variants that correspond to indels in the promoters of either key transcription factors or of the opsin gene itself. Here we show that these indels are caused by the movement of transposable elements (TEs). These precise indels are not found outside of LM, suggesting that these TEs are recently active and are segregating within the Malawi cichlid lineage. A similar indel has arisen independently outside of LM at one locus, suggesting that some locations are primed for TE insertion and the resulting indels. Increased TE mobility may be associated with interspecific hybridization, which disrupt mechanisms of TE suppression. Overall, our study suggests that TEs may contribute to key regulatory changes, and may facilitate rapid phenotypic change and possibly speciation in African cichlids.

evolutionary biology↗

Microclimate buffering and thermal tolerance across elevations in a tropical butterfly

Microclimatic variability in tropical forests plays a key role in shaping species distributions and their ability to cope with environmental change, especially for ectotherms. Yet, currently available climatic datasets lack data from the forest interior and our knowledge of thermal tolerance among tropical ectotherms is limited. To tackle this, we studied natural variation in the microclimate experienced by a tropical genus of butterflies (Heliconius sp.) along their Andean range across a single year. We found that the forest strongly buffers temperature and humidity in the understory, especially in the lowlands where temperatures are more extreme. There were systematic differences between our yearly records and macroclimate databases (WorldClim2), with lower interpolated minimum temperatures and maximum temperatures higher than expected. We then assessed thermal tolerance of ten Heliconius butterfly species in the wild and showed that populations at high elevations had significantly lower heat tolerance than those at lower elevations. However, when we reared populations of the widespread H. erato from high and low elevations in a common-garden environment, the difference in heat tolerance across elevations was reduced, indicating plasticity in this trait. Microclimate buffering is not currently captured in publicly available datasets but could be crucial for enabling upland shifting of species sensitive to heat such as highland Heliconius. Plasticity in thermal tolerance may alleviate the effects of global warming on some widespread ectotherm species, but more research is needed to understand the long-term consequences of plasticity on populations and species. Summary statementTropical forests along the Andes were found to greatly buffer climate. The butterflies inhabiting high elevations were less thermally tolerant but not when reared in common-garden conditions, indicating plasticity.

ecology↗

Adaptive introgression across semipermeable species boundaries between local Helicoverpa zea and invasive Helicoverpa armigera moths

Hybridization between invasive and native species has raised global concern given the dramatic increase in species range shifts and pest outbreaks due to climate change, development of suitable agroecosystems, and anthropogenic dispersal. Nevertheless, secondary contact between sister lineages of local and invasive species provides a natural laboratory to understand the factors that determine introgression and the maintenance or loss of species barriers. Here, we characterize the early evolutionary outcomes following secondary contact between invasive Helicoverpa armigera and H. zea in Brazil. We carried out whole-genome resequencing of Helicoverpa moths from Brazil in two temporal samples: during the outbreak of H. armigera in 2013, and more recent populations from 2017. There is evidence for a burst of hybridization and widespread introgression from local H. zea into invasive H. armigera coinciding with H. armigera expansion in 2013. However, in H. armigera, admixture proportions were reduced between 2013 and 2017, indicating a decline in hybridization rates. Recent populations also showed shorter introgressed tracks suggesting selection against admixture. In contrast to the genome-wide pattern, there was striking evidence for introgression of a single region including an insecticide-resistance allele from the invasive H. armigera into local H. zea, which increased in frequency over time but was localized within the genome. In summary, despite extensive gene-flow after secondary contact, the species boundaries are largely maintained except for the single introgressed region containing the insecticide-resistant locus. We document the worst-case scenario for an invasive species, in which there are now two pest species instead of one, and the native species has acquired resistance to pyrethroid insecticides through introgression and hybridization, with significant implications for pest management in future population expansions and introductions of novel resistance genes from new invasive H. armigera populations. Author summarySecondary contact occurs when related species with non-overlapping ranges are geographically reunited. Scenarios of secondary contact have increased due to anthropogenic movement of species outside of their native range, often resulting in invasive species that successfully spread and stabilised in the new environment. This is the case for Helicoverpa armigera, a major agricultural pest in the Old World that has recently invaded the Americas, where it reunited with its closest relative, H. zea. While some authors reported hybridisation, and hypothesised about the potential emergence of novel ecotypes and the exchange of pesticide-resistant genes, these outcomes have not been tested yet. We examine these outcomes by sequencing individuals from both species in Brazil, collected in 2013 after outbreaks of H. armigera were reported, and individuals collected during 2017. We discovered that despite hybridisation, these moths have not collapsed into a single species nor formed new ecotypes, and that the species distinctiveness is maintained through selection against most of the foreign genotypes that cross species boundaries. However, we found that hybridisation mediated the rapid acquisition of a H. armigera gene conferring resistance to pyrethroids by H. zea. The overall decline in populations of both species during the interval covered by this study means that our results are likely to reflect the consequences of hybridization events early after invasion, despite the likely ongoing introduction of H. armigera genetic diversity through trade across the South American continent. Our results provide a rare example of adaptive transferral of variation right after invasion and elucidate the dynamics of insecticide resistance evolution in H. zea.

evolutionary biology↗

A dense linkage map of Lake Victoria cichlids improved the Pundamilia genome assembly and revealed a major QTL for sex-determination

Genetic linkage maps are essential for comparative genomics, high quality genome sequence assembly and fine scale quantitative trait locus (QTL) mapping. In the present study we identified and genotyped markers via restriction-site associated DNA (RAD) sequencing and constructed a genetic linkage map based on 1,597 SNP markers of an interspecific F2 cross of two closely related Lake Victoria cichlids (Pundamilia pundamilia and P. sp. \"red head\"). The SNP markers were distributed on 22 linkage groups and the total map size was 1,594 cM with an average marker distance of 1.01 cM. This high-resolution genetic linkage map was used to anchor the scaffolds of the Pundamilia genome and estimate recombination rates along the genome. Via QTL mapping we identified a major QTL for sex in a [~]1.9 Mb region on Pun-LG10, which is homologous to Oreochromis niloticus LG 23 (Ore-LG23) and includes a well-known vertebrate sex-determination gene (amh).

evolutionary biology↗