| 31. |
- Höglund, Jacob, et al.
(författare)
-
A Chromosome-Level Genome Assembly and Annotation for the Clouded Apollo Butterfly (Parnassius mnemosyne) : A Species of Global Conservation Concern
- 2024
-
Ingår i: Genome Biology and Evolution. - : Oxford University Press. - 1759-6653. ; 16:2
-
Tidskriftsartikel (refereegranskat)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.
|
|
| 32. |
- Höök, Lars, et al.
(författare)
-
Dualistic dosage compensation and rapid evolution of expression balance in response to W chromosome degeneration in Leptidea butterflies
-
Annan publikation (övrigt vetenskapligt/konstnärligt)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.
|
|
| 33. |
- Höök, Lars, et al.
(författare)
-
High-density linkage maps and chromosome level genome assemblies unveil direction and frequency of extensive structural rearrangements in wood white butterflies (Leptidea spp.)
-
Tidskriftsartikel (refereegranskat)abstract
- Karyotypes are generally conserved between closely related species and large chromosome rearrangements typically have negative fitness consequences in heterozygotes, potentially driving speciation. In the order Lepidoptera, most investigated species have the ancestral karyotype and gene synteny is often conserved across deep divergence, although examples of extensive genome reshuffling have recently been demonstrated. The genus Leptidea has an unusual level of chromosome variation and rearranged sex chromosomes, but the extent of restructuring across the rest of the genome is so far unknown. To explore the genomes of the wood white (Leptidea) species complex, we generated eight genome assemblies using a combination of 10X linked reads and HiC data, and improved them using linkage maps for two populations of the common wood white (L. sinapis) with distinct karyotypes. Synteny analysis revealed an extensive amount of rearrangements, both compared to the ancestral karyotype and between the Leptidea species, where only one of the three Z chromosomes was conserved across all comparisons. Most restructuring was explained by fissions and fusions, while translocations appear relatively rare. We further detected several examples of segregating rearrangement polymorphisms supporting a highly dynamic genome evolution in this clade. Fusion breakpoints were enriched for LINEs and LTR elements, which suggests that ectopic recombination might be an important driver in the formation of new chromosomes. Our results show that chromosome count alone may conceal the extent of genome restructuring and we propose that the amount of genome evolution in Lepidoptera might still be underestimated due to lack of taxonomic sampling.
|
|
| 34. |
- Höök, Lars, et al.
(författare)
-
High-density linkage maps and chromosome level genome assemblies unveil direction and frequency of extensive structural rearrangements in wood white butterflies (Leptidea spp.)
- 2023
-
Ingår i: Chromosome Research. - : Springer Science and Business Media LLC. - 0967-3849 .- 1573-6849. ; 31:1
-
Tidskriftsartikel (refereegranskat)abstract
- Karyotypes are generally conserved between closely related species and large chromosome rearrangements typically have negative fitness consequences in heterozygotes, potentially driving speciation. In the order Lepidoptera, most investigated species have the ancestral karyotype and gene synteny is often conserved across deep divergence, although examples of extensive genome reshuffling have recently been demonstrated. The genus Leptidea has an unusual level of chromosome variation and rearranged sex chromosomes, but the extent of restructuring across the rest of the genome is so far unknown. To explore the genomes of the wood white (Leptidea) species complex, we generated eight genome assemblies using a combination of 10X linked reads and HiC data, and improved them using linkage maps for two populations of the common wood white (L. sinapis) with distinct karyotypes. Synteny analysis revealed an extensive amount of rearrangements, both compared to the ancestral karyotype and between the Leptidea species, where only one of the three Z chromosomes was conserved across all comparisons. Most restructuring was explained by fissions and fusions, while translocations appear relatively rare. We further detected several examples of segregating rearrangement polymorphisms supporting a highly dynamic genome evolution in this clade. Fusion breakpoints were enriched for LINEs and LTR elements, which suggests that ectopic recombination might be an important driver in the formation of new chromosomes. Our results show that chromosome count alone may conceal the extent of genome restructuring and we propose that the amount of genome evolution in Lepidoptera might still be underestimated due to lack of taxonomic sampling.
|
|
| 35. |
- Höök, Lars, et al.
(författare)
-
Multilayered Tuning of Dosage Compensation and Z-Chromosome Masculinization in the Wood White (Leptidea sinapis) Butterfly
- 2019
-
Ingår i: Genome Biology and Evolution. - : OXFORD UNIV PRESS. - 1759-6653. ; 11:9, s. 2633-2652
-
Tidskriftsartikel (refereegranskat)abstract
- In species with genetic sex determination, dosage compensation can evolve to equal expression levels of sex-linked and autosomal genes. Current knowledge about dosage compensation has mainly been derived frommale-heterogametic (XX/XY) model organisms, whereas less is understood about the process in female-heterogametic systems (ZZ/ZW). In moths and butterflies, downregulation of Z-linked expression in males (ZZ) to match the expression level in females (ZW) is often observed. However, little is known about the underlying regulatory mechanisms, or if dosage compensation patterns vary across ontogenetic stages. In this study, we assessed dynamics of Z-linked and autosomal expression levels across developmental stages in the wood white (Leptidea sinapis). We found that although expression of Z-linked genes in general was reduced compared with autosomal genes, dosage compensation was actually complete for some categories of genes, in particular sex-biased genes, but equalization in females was constrained to a narrower gene set. We also observed a noticeable convergence in Z-linked expression between males and females after correcting for sex-biased genes. Sex-biased expression increased successively across developmental stages, and male-biased genes were enriched on the Z-chromosome. Finally, all five core genes associated with the ribonucleoprotein dosage compensation complex male-specific lethal were detected in adult females, in correspondence with a reduction in the expression difference between autosomes and the single Z-chromosome. We show that tuning of gene dosage is multilayered in Lepidoptera and argue that expression balance across chromosomal classes may predominantly be driven by enrichment of male-biased genes on the Z-chromosome and cooption of available dosage regulators.
|
|
| 36. |
- Höök, Lars, 1980-, et al.
(författare)
-
Temporal dynamics of faster neo-Z evolution in butterflies
-
Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- The faster-Z/X hypothesis predicts that sex-linked genes should diverge faster than autosomal genes and may therefore play important roles in speciation. However, studies across different lineages have shown mixed support for this effect, a variation that has been explained by various evolutionary mechanisms. So far, most analyses have focused on systems with old and well differentiated sex chromosomes, but less is known about divergence of more recently acquired neo-sex chromosomes. In the female heterogametic order Lepidoptera (moths and butterflies), fusions between the ancestral Z chromosome and autosomes are relatively frequent, but the evolutionary dynamics of neo Z-linked genes have not been explored in detail. Here, we analysed the faster-Z effect in Leptidea sinapis, a butterfly with an exceptionally reorganized genome and three Z chromosomes. We show that the neo-Z chromosomes have been acquired in a stepwise fashion, resulting in distinct strata of differentiation and masculinization. While Z-linked divergence generally seems to have been driven by adaptive processes, the relative effects of selection and drift showed a temporal trend where selection has been more prevalent for genes located on older Z linked regions, causing increased divergence of Z-linked genes with female-biased expression. In contrast, the intensity of selection on genes located on the most recently acquired neo-Z chromosome (Z3) appears to have been hampered by the presence of gametologs on the largely intact, homologous neo-W chromosome. However, the intermediately aged neo-Z chromosome (Z2), which is completely differentiated from W gametologs, showed less evolutionary constraint than the ancestral Z, resulting in particularly fast evolution. Our results therefore support that neo-sex chromosomes can constitute temporary hot-spots of adaptation and divergence. The underlying dynamics are likely causally linked to shifts in selective constraints, evolution of gene expression and the degeneration of W-linked gametologs which gradually expose Z-linked genes to selection.
|
|
| 37. |
- Höök, Lars, et al.
(författare)
-
Temporal dynamics of faster neo-Z evolution in butterflies
- 2024
-
Ingår i: Evolution. - 0014-3820 .- 1558-5646.
-
Tidskriftsartikel (refereegranskat)abstract
- The faster-Z/X hypothesis predicts that sex-linked genes should diverge faster than autosomal genes. However, studies across different lineages have shown mixed support for this effect. So far, most analyses have focused on old and well-differentiated sex chromosomes, but less is known about the divergence of more recently acquired neo-sex chromosomes. In Lepidoptera (moths and butterflies), Z-autosome fusions are frequent, but the evolutionary dynamics of neo-Z chromosomes have not been explored in detail. Here, we analyzed the faster-Z effect in Leptidea sinapis, a butterfly with three Z chromosomes. We show that the neo-Z chromosomes have been acquired stepwise, resulting in strata of differentiation and masculinization. While all Z chromosomes showed evidence of the faster-Z effect, selection for genes on the youngest neo-Z chromosome (Z3) appears to have been hampered by a largely intact, homologous neo-W chromosome. However, the intermediately aged neo-Z chromosome (Z2), which lacks W gametologs, showed fewer evolutionary constraints, resulting in particularly fast evolution. Our results therefore support that neo-sex chromosomes can constitute temporary hot-spots of adaptation and divergence. The underlying dynamics are likely causally linked to shifts in selective constraints, evolution of gene expression, and degeneration of W-linked gametologs which gradually expose Z-linked genes to selection.
|
|
| 38. |
- Höök, Lars, 1980-
(författare)
-
The Evolution of Sex Chromosomes and Dosage Compensation in Structurally Dynamic Butterfly Genomes
- 2023
-
Doktorsavhandling (övrigt vetenskapligt/konstnärligt)abstract
- Dimorphic sex chromosomes have evolved independently throughout evolution from initially homologous autosomes. Recombination suppression between the sex chromosomes causes one sex chromosome to degenerate, which will influence evolution of sex-linked genes. This thesis investigated the evolution of genes and regulatory mechanisms on the sex chromosomes in Leptidea butterflies. Butterflies are female heterogametic, and females carry a dimorphic Z/W pair, while males have two homologous Z chromosomes. Dosage compensation is expected to evolve to equalize gene expression differences which are caused by this imbalance. Our analyses showed that Z-linked gene expression was reduced in males to parity with females, and reduced compared to autosomal levels. This is likely an adaptation to homogenize expression patterns between the sexes. However, the Z chromosome was enriched with male-biased genes, and sex-biased genes were not downregulated, suggesting that specific tuning occur for subsets of genes. An exploration of the Leptidea genomes revealed an unprecedented amount of chromosomal rearrangements, and detection of chromosomal heterozygotes suggests that the process is ongoing. Transposable elements were enriched in fused chromosome regions and are likely promoting rearrangements. The observed restructuring has formed several neo-sex chromosomes, which makes Leptidea useful for studies of evolutionary dynamics of sex chromosomes. Z-linked genes showed a faster-Z effect, which was strongest for female-biased genes. In addition, the neo-Z chromosomes revealed a temporal dynamic, with younger Z chromosomes diverging faster. This could potentially be caused by an increased adaptive potential compared to the ancestral Z chromosome. Dualistic dosage compensation was found on the neo-Z chromosomes, with some chromosome regions being downregulated in males, and some regions being upregulated in females, in both cases resulting in inter-sexual expression balance. One Leptidea neo-W chromosome is largely intact, and analyses of allele specific expression provided strong evidence for W gametolog expression. Furthermore, male Z-linked expression was reduced for genes that lacked W gametologs, indicating that gene regulation has evolved rapidly to achieve dosage balance. This work has led to several interesting discoveries about gene regulation, chromosome rearrangements and sequence divergence of sex chromosomes, and in general revealed a more complex picture of how these specific chromosomes evolve.
|
|
| 39. |
- Kawakami, Takeshi, et al.
(författare)
-
Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array
- 2014
-
Ingår i: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 14:6, s. 1248-1260
-
Tidskriftsartikel (refereegranskat)abstract
- With the access to draft genome sequence assemblies and whole-genome resequencing data from population samples, molecular ecology studies will be able to take truly genome-wide approaches. This now applies to an avian model system in ecological and evolutionary research: Old World flycatchers of the genus Ficedula, for which we recently obtained a 1.1Gb collared flycatcher genome assembly and identified 13 million single-nucleotide polymorphism (SNP)s in population resequencing of this species and its sister species, pied flycatcher. Here, we developed a custom 50K Illumina iSelect flycatcher SNP array with markers covering 30 autosomes and the Z chromosome. Using a number of selection criteria for inclusion in the array, both genotyping success rate and polymorphism information content (mean marker heterozygosity=0.41) were high. We used the array to assess linkage disequilibrium (LD) and hybridization in flycatchers. Linkage disequilibrium declined quickly to the background level at an average distance of 17kb, but the extent of LD varied markedly within the genome and was more than 10-fold higher in genomic islands' of differentiation than in the rest of the genome. Genetic ancestry analysis identified 33 F-1 hybrids but no later-generation hybrids from sympatric populations of collared flycatchers and pied flycatchers, contradicting earlier reports of backcrosses identified from much fewer number of markers. With an estimated divergence time as recently as <1Ma, this suggests strong selection against F-1 hybrids and unusually rapid evolution of reproductive incompatibility in an avian system.
|
|
| 40. |
- Knief, Ulrich, et al.
(författare)
-
Association mapping of morphological traits in wild and captive zebra finches : reliable within, but not between populations
- 2017
-
Ingår i: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 26:5, s. 1285-1305
-
Tidskriftsartikel (refereegranskat)abstract
- Identifying causal genetic variants underlying heritable phenotypic variation is a long-standing goal in evolutionary genetics. We previously identified several quantitative trait loci (QTL) for five morphological traits in a captive population of zebra finches (Taeniopygia guttata) by whole-genome linkage mapping. We here follow up on these studies with the aim to narrow down on the quantitative trait variants (QTN) in one wild and three captive populations. First, we performed an association study using 672 single nucleotide polymorphisms (SNPs) within candidate genes located in the previously identified QTL regions in a sample of 939 wild-caught zebra finches. Then, we validated the most promising SNP-phenotype associations (n=25 SNPs) in 5228 birds from four populations. Genotype-phenotype associations were generally weak in the wild population, where linkage disequilibrium (LD) spans only short genomic distances. In contrast, in captive populations, where LD blocks are large, apparent SNP effects on morphological traits (i.e. associations) were highly repeatable with independent data from the same population. Most of those SNPs also showed significant associations with the same trait in other captive populations, but the direction and magnitude of these effects varied among populations. This suggests that the tested SNPs are not the causal QTN but rather physically linked to them, and that LD between SNPs and causal variants differs between populations due to founder effects. While the identification of QTN remains challenging in nonmodel organisms, we illustrate that it is indeed possible to confirm the location and magnitude of QTL in a population with stable linkage between markers and causal variants.
|
|
