| 1. |
- Backström, Niclas, 1969-, et al.
(author)
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Cis-regulatory sequence variation and association with Mycoplasma load in natural populations of the house finch (Carpodacus mexicanus)
- 2013
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In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 3:3, s. 655-666
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Journal article (peer-reviewed)abstract
- Characterization of the genetic basis of fitness traits in natural populations is important for understanding how organisms adapt to the changing environment and to novel events, such as epizootics. However, candidate fitness-influencing loci, such as regulatory regions, are usually unavailable in nonmodel species. Here, we analyze sequence data from targeted resequencing of the cis-regulatory regions of three candidate genes for disease resistance (CD74, HSP90α, and LCP1) in populations of the house finch (Carpodacus mexicanus) historically exposed (Alabama) and naïve (Arizona) to Mycoplasma gallisepticum. Our study, the first to quantify variation in regulatory regions in wild birds, reveals that the upstream regions of CD74 and HSP90α are GC-rich, with the former exhibiting unusually low sequence variation for this species. We identified two SNPs, located in a GC-rich region immediately upstream of an inferred promoter site in the gene HSP90α, that were significantly associated with Mycoplasma pathogen load in the two populations. The SNPs are closely linked and situated in potential regulatory sequences: one in a binding site for the transcription factor nuclear NFYα and the other in a dinucleotide microsatellite ((GC)6). The genotype associated with pathogen load in the putative NFYα binding site was significantly overrepresented in the Alabama birds. However, we did not see strong effects of selection at this SNP, perhaps because selection has acted on standing genetic variation over an extremely short time in a highly recombining region. Our study is a useful starting point to explore functional relationships between sequence polymorphisms, gene expression, and phenotypic traits, such as pathogen resistance that affect fitness in the wild.
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| 2. |
- Backström, Niclas, 1969-
(author)
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Gene Mapping in Ficedula Flycatchers
- 2009
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Doctoral thesis (other academic/artistic)abstract
- In order to get full understanding of how evolution proceeds in natural settings it is necessary to reveal the genetic basis of the phenotypic traits that play a role for individual fitness in different environments. There are a few possible approaches, most of which stem from traditional mapping efforts in domestic animals and other model species. Here we set the stage for gene mapping in natural populations of birds by producing a large number of anchor markers of broad utility for avian genetical research and use these markers to generate a genetic map of the collared flycatcher (Ficedula albicollis). The map reveals a very high degree of synteny and gene order conservation between bird species separated by as much as 100 million years. This is encouraging for later stages of mapping procedures in natural populations since this means that there is a possibility to use the information from already characterized avian genomes to track candidate genes for detailed analysis in non-model species. One interesting aspect of the low degree of rearrangements occurring in the avian genomes is that this could play a role in the low rate of hybridization barriers formed in birds compared to for instance mammals. An analysis of Z-linked gene markers reveals relatively long-range linkage disequilibrium (LD) in collared flycatchers compared to other outbred species but still, LD seems to decay within < 50 kb indicating that > 20.000 markers would be needed to cover the genome in an association scan. A detailed scan of 74 Z-linked genes evenly distributed along the chromosome in both the collared flycatcher and the pied flycatcher (Ficedula hypoleuca) indicates that there are regions that evolve under directional selection, regions that might harbor loci of importance for adaptive divergence and/or hybrid inviability.
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| 3. |
- Boman, Jesper, et al.
(author)
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Environmental stress during larval development induces DNA methylation shifts in the migratory painted lady butterfly (Vanessa cardui)
- 2023
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In: Molecular Ecology. - : John Wiley & Sons. - 0962-1083 .- 1365-294X. ; 32:13, s. 3513-3523
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Journal article (peer-reviewed)abstract
- Seasonal environmental fluctuations provide formidable challenges for living organisms, especially small ectotherms such as butterflies. A common strategy to cope with harsh environments is to enter diapause, but some species avoid unsuitable conditions by migrating. Despite a growing understanding of migration in the life cycles of some butterfly species, it remains unknown how individuals register and store environmental cues to determine whether and where to migrate. Here, we explored how competition and host plant availability during larval development affect patterns of DNA methylation in the migratory painted lady (Vanessa cardui) butterfly. We identify a set of potentially functional methylome shifts associated with differences in the environment, indicating that DNA methylation is involved in the response to different conditions during larval development. By analysing the transcriptome for the same samples used for methylation profiling, we also uncovered a non-monotonic relationship between gene body methylation and gene expression. Our results provide a starting point for understanding the interplay between DNA methylation and gene expression in butterflies in general and how differences in environmental conditions during development can trigger unique epigenetic marks that might be important for behavioural decisions in the adult stage.
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| 4. |
- Boman, Jesper, et al.
(author)
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Evolution of hybrid inviability associated with chromosome fusions
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Other publication (other academic/artistic)abstract
- Chromosomal rearrangements, such as inversions, have received considerable attention in the speciation literature due to their hampering effects on recombination. However, less is known about how other rearrangements, such as chromosome fissions and fusions, can affect the evolution of reproductive isolation. Here, we used crosses between populations of the wood white butterfly (Leptidea sinapis) with different karyotypes to identify genomic regions associated with hybrid inviability. We mapped candidate loci for hybrid inviability by contrasting allele frequencies between F2 hybrids that survived until the adult stage with individuals of the same cohort that succumbed to hybrid incompatibilities. Hybrid inviability factors were predominantly found in fast-evolving regions with reduced recombination rates, especially in regions where chromosome fusions have occurred. By analyzing sequencing coverage, we excluded aneuploidies as a direct link between hybrid inviability and chromosome fusions. Instead, our results point to an indirect relationship between hybrid inviability and chromosome fusions, possibly related to reductions in recombination rate caused by fusions. These results highlight that the extensive variation in chromosome numbers observed across the tree of life does not only distinguish species but can also be involved in speciation by being hotspots for the early evolution of postzygotic reproductive isolation.
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| 5. |
- Boman, Jesper, et al.
(author)
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Meiotic drive against chromosome fusions in butterfly hybrids
- 2024
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In: Chromosome Research. - : Springer. - 0967-3849 .- 1573-6849. ; 32:2
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Journal article (peer-reviewed)abstract
- Species frequently differ in the number and structure of chromosomes they harbor, but individuals that are heterozygous for chromosomal rearrangements may suffer from reduced fitness. Chromosomal rearrangements like fissions and fusions can hence serve as a mechanism for speciation between incipient lineages, but their evolution poses a paradox. How can rearrangements get fixed between populations if heterozygotes have reduced fitness? One solution is that this process predominantly occurs in small and isolated populations, where genetic drift can override natural selection. However, fixation is also more likely if a novel rearrangement is favored by a transmission bias, such as meiotic drive. Here, we investigate chromosomal transmission distortion in hybrids between two wood white (Leptidea sinapis) butterfly populations with extensive karyotype differences. Using data from two different crossing experiments, we uncover that there is a transmission bias favoring the ancestral chromosomal state for derived fusions, a result that shows that chromosome fusions actually can fix in populations despite being counteracted by meiotic drive. This means that meiotic drive not only can promote runaway chromosome number evolution and speciation, but also that it can be a conservative force acting against karyotypic change and the evolution of reproductive isolation. Based on our results, we suggest a mechanistic model for why chromosome fusion mutations may be opposed by meiotic drive and discuss factors contributing to karyotype evolution in Lepidoptera.
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| 6. |
- Boman, Jesper, et al.
(author)
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On the origin of an insular hybrid butterfly species
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Other publication (other academic/artistic)abstract
- Most species arise from the divergence of two populations within a species, but this is not only way speciation can occur. A new species can also evolve when diverging lineages hybridize and give rise to a persistent and ecologically differentiated species. Hybrid speciation in animals has been intensely debated, partly because hard evidence for the process have been difficult to gain. Recent access to large-scale, whole-genome sequencing data and development of novel analytical methods have made it more feasible to statistically test for hybrid origin of lineages. Here we report the discovery of a hybrid butterfly lineage. This lineage is mainly inhabiting an island in the Baltic Sea in Northern Europe and was previously described as a subspecies (horkei) of one of the parental species (Aricia artaxerxes). By analyzing whole-genome resequencing data, we conclude that horkei originated as a consequence of hybridization between A. artaxerxes and A. agestis. We show that this hybridization event occurred approximately 54,000 years ago, predating the last glaciation of the current distribution range. Horkei must therefore have persisted long enough to be able to colonize its current distribution range, despite that this range lies between the current ranges of the parental species. The hybrid origin, the maintenance of genomic integrity through time periods with dramatic climatic changes and the expression of a combination of parental traits - such as voltinism and host plant use - suggest that horkei can be considered a distinct species (Aricia horkei stat. nov.). Thus, we add to a growing list of hybrid speciation cases in animals.
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| 7. |
- Boman, Jesper, et al.
(author)
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The Effects of GC-Biased Gene Conversion on Patterns of Genetic Diversity among and across Butterfly Genomes
- 2021
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In: Genome Biology and Evolution. - : Oxford University Press. - 1759-6653. ; 13:5
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Journal article (peer-reviewed)abstract
- Recombination reshuffles the alleles of a population through crossover and gene conversion. These mechanisms have considerable consequences on the evolution and maintenance of genetic diversity. Crossover, for example, can increase genetic diversity by breaking the linkage between selected and nearby neutral variants. Bias in favor of G or C alleles during gene conversion may instead promote the fixation of one allele over the other, thus decreasing diversity. Mutation bias from G or C to A and T opposes GC-biased gene conversion (gBGC). Less recognized is that these two processes may-when balanced-promote genetic diversity. Here, we investigate how gBGC and mutation bias shape genetic diversity patterns in wood white butterflies (Leptidea sp.). This constitutes the first in-depth investigation of gBGC in butterflies. Using 60 resequenced genomes from six populations of three species, we find substantial variation in the strength of gBGC across lineages. When modeling the balance of gBGC and mutation bias and comparing analytical results with empirical data, we reject gBGC as the main determinant of genetic diversity in these butterfly species. As alternatives, we consider linked selection and GC content. We find evidence that high values of both reduce diversity. We also show that the joint effects of gBGC and mutation bias can give rise to a diversity pattern which resembles the signature of linked selection. Consequently, gBGC should be considered when interpreting the effects of linked selection on levels of genetic diversity.
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| 8. |
- Garcia-Berro, Aurora, et al.
(author)
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Migratory behaviour is positively associated with genetic diversity in butterflies
- 2023
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In: Molecular Ecology. - : John Wiley & Sons. - 0962-1083 .- 1365-294X. ; 32:3, s. 560-574
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Journal article (peer-reviewed)abstract
- Migration is typically associated with risk and uncertainty at the population level, but little is known about its cost–benefit trade-offs at the species level. Migratory insects in particular often exhibit strong demographic fluctuations due to local bottlenecks and outbreaks. Here, we use genomic data to investigate levels of heterozygosity and long-term population size dynamics in migratory insects, as an alternative to classical local and short-term approaches such as regional field monitoring. We analyse whole-genome sequences from 97 Lepidoptera species and show that individuals of migratory species have significantly higher levels of genome-wide heterozygosity, a proxy for effective population size, than do nonmigratory species. Also, we contribute whole-genome data for one of the most emblematic insect migratory species, the painted lady butterfly (Vanessa cardui), sampled across its worldwide distributional range. This species exhibits one of the highest levels of genomic heterozygosity described in Lepidoptera (2.95 ± 0.15%). Coalescent modelling (PSMC) shows historical demographic stability in V. cardui, and high effective population size estimates of 2–20 million individuals 10,000 years ago. The study reveals that the high risks associated with migration and local environmental fluctuations do not seem to decrease overall genetic diversity and demographic stability in migratory Lepidoptera. We propose a “compensatory” demographic model for migratory r-strategist organisms in which local bottlenecks are counterbalanced by reproductive success elsewhere within their typically large distributional ranges. Our findings highlight that the boundaries of populations are substantially different for sedentary and migratory insects, and that, in the latter, local and even regional field monitoring results may not reflect whole population dynamics. Genomic diversity patterns may elucidate key aspects of an insect's migratory nature and population dynamics at large spatiotemporal scales.
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| 9. |
- Höglund, Jacob, et al.
(author)
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A Chromosome-Level Genome Assembly and Annotation for the Clouded Apollo Butterfly (Parnassius mnemosyne) : A Species of Global Conservation Concern
- 2024
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In: Genome Biology and Evolution. - : Oxford University Press. - 1759-6653. ; 16:2
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Journal article (peer-reviewed)abstract
- The clouded apollo (Parnassius mnemosyne) is a palearctic butterfly distributed over a large part of western Eurasia, but population declines and fragmentation have been observed in many parts of the range. The development of genomic tools can help to shed light on the genetic consequences of the decline and to make informed decisions about direct conservation actions. Here, we present a high-contiguity, chromosome-level genome assembly of a female clouded apollo butterfly and provide detailed annotations of genes and transposable elements. We find that the large genome (1.5 Gb) of the clouded apollo is extraordinarily repeat rich (73%). Despite that, the combination of sequencing techniques allowed us to assemble all chromosomes (nc = 29) to a high degree of completeness. The annotation resulted in a relatively high number of protein-coding genes (22,854) compared with other Lepidoptera, of which a large proportion (21,635) could be assigned functions based on homology with other species. A comparative analysis indicates that overall genome structure has been largely conserved, both within the genus and compared with the ancestral lepidopteran karyotype. The high-quality genome assembly and detailed annotation presented here will constitute an important tool for forthcoming efforts aimed at understanding the genetic consequences of fragmentation and decline, as well as for assessments of genetic diversity, population structure, inbreeding, and genetic load in the clouded apollo butterfly.
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| 10. |
- Höök, Lars, et al.
(author)
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Dualistic dosage compensation and rapid evolution of expression balance in response to W chromosome degeneration in Leptidea butterflies
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Other publication (other academic/artistic)abstract
- The evolution of dimorphic sex chromosomes from initially homologous autosomes is generally explained by sex-specific selection to maintain linkage between a sex determining locus and genes that are beneficial to the same sex. While initially beneficial, the strong linkage and reduced recombination causes differentiation and degeneration of many initially shared genes. Reduced copy numbers can have severe consequences for the balance of gene expression levels between sex-linked genes and the rest of the genome. Consequently, dosage compensation has evolved independently in different lineages to mitigate the detrimental effects of unbalanced expression of sex-linked genes in the heterogametic sex. However, the variation in sex chromosome regulation in different lineages, puts the need to restore expression to ancestral levels into question. In particular, a general difference has been observed between male- (XY) and female-heterogametic (ZW) systems. In contrast to the X chromosome upregulation in heterogametic males in the XY-systems, the Z chromosomes are rarely upregulated in the heterogametic females in organisms with ZW-systems. Instead, the Z chromosomes are often downregulated in the homogametic males to achieve inter-sexual balance. Although progress has been made to understand what causes this discrepancy, comparative approaches are limited by long divergence times and ancient sex chromosome systems. An attractive approach is therefore to study the evolution of gene regulation on recently derived neo-sex chromosomes, formed through fusions between ancestral sex chromosomes and autosomes. Here, we investigated dosage compensation of neo-sex chromosomes in three closely related butterflies in the cryptic wood white clade (Leptidea). Importantly, the species have acquired multiple sex chromosomes, and dosage compensation could therefore have evolved repeatedly in the clade. Our analyses reveal a mixture of gene expression patterns which suggests that distinct modes of dosage compensation have evolved on the different Z chromosomes. In addition, we detect evidence that dosage balancing mechanisms have been rapidly recruited to the youngest neo-Z chromosome, to counteract an ongoing degeneration of neo-W gametologs. The results add to a growing list of examples where diverse dosage compensation mechanisms can evolve within a single species, and suggests that various regulatory mechanisms are not restricted to specific sex chromosome systems.
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