Biology subjects

Wiklund, C.

Publications and source records attributed to Wiklund, C..

9 recordsLinked to original sources

bioRxiv2024

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↗

bioRxiv2023

Temporal Dynamics of Faster Neo-Z Evolution in Butterflies

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 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 analysed 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 less 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.

evolutionary biology↗

bioRxiv2023

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↗

bioRxiv2023

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↗

bioRxiv2022

Evolution of seasonal plasticity in response to climate change differs between life-stages of a butterfly

Climate change alters seasonal environments without altering photoperiod, creating a cue-environment mismatch for organisms that rely on photoperiod as a cue for seasonal plasticity and phenology. Evolution can potentially correct for this mismatch by altering the photoperiodic reaction norm, but often phenology depends on multiple plastic decisions made at different life stages and times of year. We tested whether seasonal plasticity in different life stages evolves independently or in concert under climate change using Pararge aegeria (Speckled wood butterfly). This butterfly uses day length as a cue for life history plasticity in two different life stages: larval development time and pupal diapause. Photoperiodic reaction norms for plasticity in these traits were first measured over 30 years ago for two different Swedish populations. In this study, we replicated historic experiments that measured these reaction norms using the contemporary populations. We found evidence for evolution of the reaction norm for larval development time, but in opposite directions in the two populations. In contrast, we found no evidence for evolution of the reaction norm for pupal diapause. These results show that different life stages can evolve differently in response to climate change and only studying one part of the life cycle will not always be enough to fully understand how climate change impacts phenotypic plasticity and phenology.

evolutionary biology↗

bioRxiv2022

The fine-scale recombination rate variation and associations with genomic features in a butterfly

Genetic recombination is a key molecular mechanism that has profound implications on both micro- and macro-evolutionary processes. However, the determinants of recombination rate variation in holocentric organisms are poorly understood, in particular in Lepidoptera (moths and butterflies). The wood white butterfly (Leptidea sinapis) shows considerable intraspecific variation in chromosome numbers and is a suitable system for studying regional recombination rate variation and its potential molecular underpinnings. Here, we developed a large wholegenome resequencing data set from a population of wood whites to obtain high-resolution recombination maps using linkage disequilibrium information. The analyses revealed that larger chromosomes had a bimodal recombination landscape, potentially due to interference between simultaneous chiasmata. The recombination rate was significantly lower in subtelomeric regions, with exceptions associated with segregating chromosome rearrangements, showing that fissions and fusions can have considerable effects on the recombination landscape. There was no association between the inferred recombination rate and base composition, supporting a negligible influence of GC-biased gene conversion in butterflies. We found significant but variable associations between the recombination rate and the density of different classes of transposable elements (TEs), most notably a significant enrichment of SINEs in genomic regions with higher recombination rate. Finally, the analyses unveiled significant enrichment of genes involved in farnesyltranstransferase activity in recombination cold-spots, potentially indicating that expression of transferases can inhibit formation of chiasmata during meiotic division. Our results provide novel information about recombination rate variation in holocentric organisms and has particular implications for forthcoming research in population genetics, molecular/genome evolution and speciation.

genomics↗

bioRxiv2022

High-density linkage maps and chromosome level genome assemblies unveil direction and frequency of extensive structural rearrangements in wood white butterflies (Leptidea spp.)

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.

evolutionary biology↗

bioRxiv2020

Timing of mating, reproductive status and resource availability in relation to migration in the painted lady butterfly, Vanessa cardui

In many migratory insects, migration occurs during the pre-reproductive phase of the life cycle. This trait probably arises from a trade-off between migration and reproduction and in females has been termed as the oogenesis-flight syndrome. However, the generality of this syndrome has been questioned, especially for monomorphic insects. We studied the relationship between migration and reproduction in the highly cosmopolitan painted lady butterfly, which in the Palaearctic undertakes the longest known multi-generational migration circuit of any insect. We tested for the oogenesis-flight syndrome in both spring and autumn migrants in two regions linked by migration, North Africa and northern Spain. Field observations were combined with laboratory experiments to determine the lifespan and the age at first mating to unravel the reproductive strategy observed in individuals captured in the wild. Females and males wait on average around 5-6 days before mating, and field data revealed that mating frequencies increase rapidly once females reach a medium wing wear category. There were seasonal differences in mating frequencies in the study regions depending on whether the region acted as a source or as a destination for migrants, and in the latter case there were almost twice as many mated females. Moreover, about 80% of females collected during migratory flights were unmated, the remaining females having mated only very recently. Our results thus strongly indicate that the painted lady fulfils the oogenesis-flight syndrome, as migration is concentrated in its relatively short pre-reproductive period. Field data also showed a high positive correlation between mating frequency and host plant abundance, which suggests that mated females have the ability to locate potential breeding areas. This, together with the very high fecundity estimated from over 1000 eggs in laboratory trials, makes the painted lady one of the most successful migratory insects on Earth.

animal behavior and cognition↗

bioRxiv2017

A butterfly chromonome reveals selection dynamics during extensive and cryptic chromosomal reshuffling

Chromosome evolution, an important component of mico- and macroevolutionary dynamics 1-5, presents an enigma in the mega-diverse Lepidoptera6. While most species exhibit constrained chromosome evolution, with nearly identical haploid chromosome counts and chromosome-level shared gene content and collinearity among species despite more than 140 Million years of divergence7, a small fraction of species independently exhibit dramatic changes in chromosomal count due to extensive fission and fusion events that are facilitated by their holocentric chromosomes7-9. Here we address this enigma of simultaneous conservation and dynamism in chromosome evolution in our analysis of the chromonome (chromosome level assembly10) of the green-veined white butterfly, Pieris napi (Pieridae, Linnaeus, 1758). We report an unprecedented reorganization of the standard Lepidopteran chromosome structure via more than 90 fission and fusion events that are cryptic at other scales, as the haploid chromosome number is identical to related genera and gene collinearity within the large rearranged segments matches other Lepidoptera. Furthermore, these rearranged segments are significantly enriched for clusters of functionally related genes and the maintenance of ancient telomeric ends. These results suggest an unexpected role for selection in shaping chromosomal evolution when the structural constraints of monocentricq chromosomes are relaxed.

evolutionary biology↗