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Boman, J.

Publications and source records attributed to Boman, J..

13 recordsLinked to original sources

Contrasting modes of dosage compensation on ancestral and neo-Z chromosomes in butterflies

The evolution of sex chromosomes from homologous autosomes generally causes degeneration of the sex-limited chromosome (Y in XY systems and W in ZW systems), leading to altered or disrupted gene regulation. Dosage compensation has evolved repeatedly to mitigate the effects of such unbalanced expression of sex-linked genes. Previous analyses show that X chromosomes often are upregulated in males in XY-systems, while upregulation of the Z chromosome in females is unusual in ZW-systems, but understanding the generality of this pattern requires broader taxonomic sampling. In addition, little is known about how dosage compensation is established when sex chromosomes initially evolve. Here, we narrow this knowledge gap by characterizing dosage compensation in butterflies (Leptidea sp.) that harbor both ancestral, intermediate and recently derived sex chromosomes. Analyses of 120 samples, representing both sexes, different tissues and developmental stages, reveal a mixture of gene expression patterns. We confirm that downregulation in males is the predominant mode on the ancestral Z chromosome, but we find complex patterns of male downregulation and female upregulation for Z chromosomes with different evolutionary histories, as well as between different tissues. Dosage compensation has for example evolved rapidly in regions of the youngest neo-Z where the neo-W gametologs have lost function, but not in regions with functional gene copies on both Z and W. Our results provide novel insights into the complex evolutionary trajectories underlying dosage compensation and show that development of specific mechanisms likely depends on both sex chromosome system and dosage sensitivity of sex chromosome-linked genes.

evolutionary biology↗

Uniform annotation framework reveals genome size and LINE/LTR retrotransposons as predictors of gene family expansion across Coleoptera

Gene family evolution - the turnover of duplicated homologous genes - shapes genome architecture and fuels phenotypic innovation. Repetitive elements (REs) facilitate gene duplication and genome expansion, yet whether variation in repeat abundance and genome size (GS) scales with gene family evolution across species remains unclear. Coleoptera provides a well-suited system for examining these dynamics because of its major ecological diversification and extensive genome size variation. Comparative tests of these relationships are however hindered by heterogenous genome annotations that distort gene counts and orthogroup assignments. We first evaluate how repeat- and gene-annotation strategies influence gene- and orthogroup-detection across beetle genomes. We then apply unified re-annotations of both to identify rapidly evolving gene families and test whether GS and repeat content covary with gene family size evolution. Nearly 500 orthogroups are rapidly evolving in Coleoptera, many of which are linked to ecologically crucial functions such as chemosensory perception and detoxification. GS and RE abundance are correlated, and on average scale positively with gene family sizes. LINE and DNA transposable elements commonly flank rapidly expanding gene families, but with pronounced species-specific variation. Together, these findings position genome architecture and repeat dynamics as fundamental determinants of gene family evolvability.

evolutionary biology↗

No preference for performance: Host plant preference, offspring performance and host plant distribution in the butterfly Aricia artaxerxes

The connection between female host plant preference and offspring performance is important for understanding how relationships between plants and phytophagous insects have evolved. According to the preference-performance hypothesis, female insects should evolve to oviposit on host plants on which offspring performance is the highest. Here, we examined the preference-performance hypothesis in the northern brown argus (Aricia artaxerxes) butterfly in the province of Uppland, Sweden, by comparing female host plant preference and larval growth between the host plant species wood cranesbill (Geranium sylvaticum) and bloody cranesbill (G. sanguineum). We also investigated if host plant preference in A. artaxerxes was related to the geographic distribution of A. artaxerxes and its host plants in the province Uppland. We found that the A. artaxerxes females, contrary to the preference-performance hypothesis, preferred ovipositing on G. sylvaticum, even though larvae feeding on G. sylvaticum were slightly smaller than those feeding on G. sanguineum. Since G. sylvaticum is more abundant and probably more utilized than G. sanguineum in Uppland, an explanation for this negative preference-performance connection may be that there are advantages associated with utilizing a more common host plant species, even though larvae feeding on this plant show reduced growth rates. Overall, the results show that factors other than offspring performance, such as geographic distribution, may influence female host plant preference in A. artaxerxes.

evolutionary biology↗

Determinants of chromosomal rearrangements in holocentric Leptidea butterflies

Chromosomes can undergo large-scale rearrangements such as fissions and fusions. Occasional rearrangements can be common, especially in organisms with holocentric chromosomes such as butterflies. However, high rates of fissions and fusions have only been observed in a few taxonomic groups. One such group is the Palearctic Leptidea butterflies, where fissions and fusions have resulted in considerable inter- and intraspecific variation in chromosome numbers. The large number of rearrangements in Leptidea, provides a rare opportunity to study the mutational determinants of chromosomal rearrangements within a statistical framework. Using nine chromosome-level genome assemblies and 138 whole-genome re-sequenced individuals, we mapped evolutionary breakpoint regions and quantified the association between annotation features and rearrangements. Evolutionary breakpoint regions were significantly depleted in protein-coding genes and the majority resided in repetitive regions. However, rearrangements were only weakly associated with transposable elements. Instead, the strongest sequence predictors were large clusters of satellite DNA, ribosomal DNA and segmental duplications, with differing patterns among rearrangement types. Copy-number variation was observed in evolutionary breakpoint regions and lineages dominated by fissions or fusions were associated respectively with genome expansion and reduction. The results give novel insights into the mechanistic basis of interchromosomal rearrangements.

evolutionary biology↗

Programmed DNA elimination drives rapid genomic innovation in two thirds of all bird species

Bird genomes are among the most stable in terms of synteny and gene content across vertebrates. However, germline-restricted chromosomes (GRCs) represent a striking exception where programmed DNA elimination confines large-scale genomic changes to the germline. GRCs are known to occur in songbirds (oscines), but have been studied only in a few species of Passerides such as the zebra finch, the key model for passerine genomics. Their presence and evolutionary dynamics in most major passerine lineages remain largely unexplored, with suboscines entirely unexamined by cytogenetic or genomic methods. Here, we present the most comprehensive comparative analysis of GRCs to date, spanning 44 million years of passerine evolution. By generating the first germline reference genomes of an oscine and a suboscine, 22 novel germline draft genomes spanning nearly all major passerine lineages and a germline draft genome of a parrot outgroup, we show that the GRC is likely present in 6,700 passerine species. Our results reveal that the GRC evolves rapidly and distinctly from the standard A chromosomes (autosomes and sex chromosomes), yet retains functionally important, selectively maintained genes. We observed gene and repeat turnover occuring orders of magnitude faster than on the A chromosomes. Some GRC genes, such as cpeb1 and pim1, are widespread from an ancient duplication. In contrast, other GRC genes, like mfsd2b and bmp15, have been independently duplicated onto the GRC multiple times, suggesting adaptive constraints. The discovery of zglp1 on the zebra finch GRC, initially copied from chromosome 30 and subsequently lost from it, indicates functional replacement, where the GRC permits gene loss from the standard genome. As the GRC harbors the only zglp1 copy in most of the [~]4000 Passerides species, GRC loss would compromise essential germline functions. Our findings establish the GRC as a genomic innovator driving rapid germline evolution. This fact highlights its evolutionary significance for passerine diversification and suggests that programmed DNA elimination may be an overlooked yet phylogenetically widespread mechanism in many understudied animal lineages.

genomics↗

On the origin of an insular hybrid butterfly lineage

A new species can form through hybridization between species. Hybrid speciation in animals has been intensely debated, partly because hard evidence for the process has been difficult to obtain. Recent access to whole-genome sequencing data have made it more feasible to detect hybrid lineages. Here we report the discovery of a European hybrid butterfly lineage, a finding that can be considered surprising given the intense and long-term study of European butterflies. The lineage we describe is mainly inhabiting an island in the Baltic Sea and was previously designated as a subspecies (horkei) of one of the parental species (Aricia artaxerxes). By analysing whole-genome resequencing data, we determine that horkei originated by hybridization between the non-sister species A. artaxerxes and A. agestis. 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 range, despite that this area lies between the current distributions of the parental species. The hybrid origin, the maintenance of genomic integrity across times of dramatic climate change and the expression of a combination of parental traits suggest that horkei could be in the process of hybrid speciation.

evolutionary biology↗

Meiotic drive against chromosome fusions in butterfly hybrids

Species frequently differ in karyotype, but heterokaryotypic individuals may suffer from reduced fitness. Chromosomal rearrangements like fissions and fusions can thus serve as a mechanism for speciation between incipient lineages but their evolution poses a paradox. How does underdominant rearrangements evolve? One solution is the fixation of underdominant chromosomal rearrangements through genetic drift. However, this requires small and isolated populations. Fixation is more likely if a novel rearrangement is favored by a transmission bias, such as meiotic drive. Here, we investigate transmission ratio distortion in hybrids between two wood white (Leptidea sinapis) butterfly populations with extensive karyotype differences. Using data from two different crossing experiments, we uncover a transmission bias favoring the fused state at chromosome with unknown polarization in one experiment and a transmission bias favoring the unfused state of derived fusions in both experiments. The latter result support a scenario where chromosome fusions can fix in populations despite counteracting effects of meiotic drive. This means that meiotic drive not only can promote runaway chromosome number evolution and speciation, but also that this transmission bias 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 derived fusions may be opposed by meiotic drive and discuss factors contributing to karyotype evolution in Lepidoptera.

evolutionary biology↗

Regulatory and evolutionary impact of DNA methylation in two songbird species and their naturally occurring F1 hybrids

Regulation of transcription by DNA methylation in 5-CpG-3 context is a widespread mechanism allowing differential expression of genetically identical cells to persist throughout development. Consequently, differences in DNA methylation can reinforce variation in gene expression among cells, tissues, populations and species. Despite a surge in studies on DNA methylation, we know little about the importance of DNA methylation in population differentiation and speciation. Here we investigate the regulatory and evolutionary impact of DNA methylation in five tissues of two Ficedula flycatcher species and their naturally occurring F1 hybrids. We show that the density of CpG in the promoters of genes determines the strength of the association between gene expression and DNA methylation. The impact of DNA methylation on gene expression varies among tissues with brain showing unique patterns. Differentially expressed genes between parental species are predicted by genetic- and methylation differentiation in CpG-rich promoters. However, both these factors fail to predict hybrid misexpression suggesting that promoter mismethylation is not a main determinant of hybrid misexpression in Ficedula flycatchers. Using allele-specific methylation estimates in hybrids we also determine the genome-wide contribution of cis- and trans effects in DNA methylation differentiation. These distinct mechanisms are roughly balanced in all tissues except brain, where trans differences predominate. Overall, this study provides insight on the regulatory and evolutionary impact of DNA methylation in songbirds.

evolutionary biology↗

Evolution of hybrid inviability associated with chromosome fusions

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. By contrasting allele frequencies between F2 hybrids that survived until the adult stage with individuals of the same cohort that succumbed to hybrid incompatibilities, we show that candidate loci for hybrid inviability mainly are situated in fast-evolving regions with reduced recombination rates, especially in regions where chromosome fusions have occurred. Our results show that the extensive variation in chromosome numbers observed across the tree of life can be involved in speciation by being hotspots for the early evolution of postzygotic reproductive isolation.

evolutionary biology↗

"Patchiness" in Mechanical Stiffness across a Tumor as an Early-Stage Marker for Malignancy

Mechanical phenotyping of tumors, either at an individual cell level or tumor cell population level is gaining traction as a diagnostic tool. However, the extent of diagnostic and prognostic information that can be gained through these measurements is still unclear. In this work, we focus on the heterogeneity in mechanical properties of cells obtained from a single source such as a tissue or tumor as a potential novel biomarker. We believe that this heterogeneity is a conventionally overlooked source of information in mechanical phenotyping data. We use mechanics-based in-silico models of cell-cell interactions and cell population dynamics within 3D environments to probe how heterogeneity in cell mechanics drives tissue and tumor dynamics. Our simulations show that the initial heterogeneity in the mechanical properties of individual cells and the arrangement of these heterogenous sub-populations within the environment can dictate overall cell population dynamics and cause a shift towards the growth of malignant cell phenotypes within healthy tissue environments. The overall heterogeneity in the cellular mechanotype and their spatial distributions is quantified by a "patchiness" index, which is the ratio of the global to local heterogeneity in cell populations. We observe that there exists a threshold value of the patchiness index beyond which an overall healthy cell population of cells will show a steady shift towards a more malignant phenotype. Based on these results, we propose that the "patchiness" of a tumor or tissue sample, can be an early indicator for malignant transformation and cancer occurrence in benign tumors or healthy tissues. Additionally, we suggest that tissue patchiness, measured either by biochemical or biophysical markers, can become an important metric in predicting tissue health and disease likelihood just as landscape patchiness is an important metric in ecology.

cancer biology↗

Nascent evolution of recombination rate differences as a consequence of chromosomal rearrangements

Reshuffling of genetic variation occurs both by independent assortment of chromosomes and by homologous recombination. Such reshuffling can generate novel allele combinations and break linkage between advantageous and deleterious variants which increases both the potential and the efficacy of natural selection. Here we used high-density linkage maps to characterize global and regional recombination rate variation in two populations of the wood white butterfly (Leptidea sinapis) with distinct karyotypes. The recombination data were compared to estimates of genetic diversity and measures of selection to assess the relationship between chromosomal rearrangements, crossing over, maintenance of genetic diversity and adaptation. Our data show that the recombination rate is influenced by both chromosome size and number, but that the difference in recombination rate between karyotypes is reduced as a consequence of a higher frequency of double crossovers in larger chromosomes. As expected from effects of selection on linked sites, we observed an overall positive association between recombination rate and genetic diversity in both populations. Our results also revealed a significant effect of chromosomal rearrangements on the rate of intergenic diversity change between populations, but limited effects on polymorphisms in coding sequence. We conclude that chromosomal rearrangements can have considerable effects on the recombination landscape and consequently influence both maintenance of genetic diversity and efficiency of selection in natural populations. Author summaryReshuffling genetic variation is fundamental for maintaining genetic diversity and creating novel allelic combinations. The two main processes involved are the independent assortment of chromosomes and homologous recombination. The number and size of chromosomes can influence the amount of pairwise reshuffling and local recombination patterns. However, studying this in natural populations is challenging. In this study, we used the wood white butterfly, which exhibits an extreme within-species karyotype difference. Extensive fusions and fissions have resulted in almost twice as many chromosomes in the southern populations compared to the northeast populations. This unique system allowed us to assess the relationship between karyotype differences, pairwise reshuffling, recombination rate variation and subsequent effects on diversity and linked selection. We found that a higher number of chromosomes result in a higher recombination rate, although the difference was less than expected due to multiple recombination events occuring on longer chromosomes. Both populations showed an association between recombination rate and genome-wide patterns of genetic diversity and efficacy of selection. We provide evidence that chromosomal rearrangements have considerable effects on the recombination landscape and thereby influence the maintenance of genetic diversity in populations.

evolutionary biology↗

Environmental stress during larval development induces head methylome profile shifts in the migratory painted lady butterfly (Vanessa cardui)

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 the unsuitable conditions by migrating. Despite a growing understanding of migration in the life cycles of some butterfly species, it is 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-linear 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.

evolutionary biology↗

The effects of GC-biased gene conversion on patterns of genetic diversity among and across butterfly genomes

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 re-sequenced 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.

evolutionary biology↗