| 1. |
- 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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| 2. |
- 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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| 3. |
- Höök, Lars, et al.
(author)
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Multilayered Tuning of Dosage Compensation and Z-Chromosome Masculinization in the Wood White (Leptidea sinapis) Butterfly
- 2019
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In: Genome Biology and Evolution. - : OXFORD UNIV PRESS. - 1759-6653. ; 11:9, s. 2633-2652
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Journal article (peer-reviewed)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.
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| 4. |
- Leal, Luis, et al.
(author)
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Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation
- 2018
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In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 27:4, s. 935-948
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Journal article (peer-reviewed)abstract
- In temperate latitudes, many insects enter diapause (dormancy) during the cold season, a period during which developmental processes come to a standstill. The wood white (Leptidea sinapis) is a butterfly species distributed across western Eurasia that shows photoperiod-induced diapause with variation in critical day-length across populations at different latitudes. We assembled transcriptomes and estimated gene expression levels at different developmental stages in experimentally induced directly developing and diapausing cohorts of a single Swedish population of L. sinapis to investigate the regulatory mechanisms underpinning diapause initiation. Different day lengths resulted in expression changes of developmental genes and affected the rate of accumulation of signal molecules, suggesting that diapause induction might be controlled by increased activity of monoamine neurotransmitters in larvae reared under short-day light conditions. Expression differences between light treatment groups of two monoamine regulator genes (DDC and ST) were observed already in instar III larvae. Once developmental pathways were irreversibly set at instar V, a handful of genes related to dopamine production were differentially expressed leading to a significant decrease in expression of global metabolic genes and increase in expression of genes related to fatty acid synthesis and sequestration. This is in line with a time-dependent (hour-glass) model of diapause regulation where a gradual shift in the concentration of monoamine neurotransmitters and their metabolites during development of larvae under short-day conditions leads to increased storage of fat, decreased energy expenditures, and ultimately developmental stasis at the pupal stage.
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| 5. |
- Näsvall, Karin, et al.
(author)
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Base composition, codon usage and patterns of gene sequence evolution in butterflies.
- 2023
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In: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653. ; 15:8
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Journal article (peer-reviewed)abstract
- Coding sequence evolution is influenced by both natural selection and neutral evolutionary forces. In many species, the effects of mutation bias, codon usage and GC-biased gene conversion (gBGC) on gene sequence evolution have not been detailed. Quantification of how these forces shape substitution patterns is therefore necessary to understand the strength and direction of natural selection. Here, we used comparative genomics to investigate the association between base composition and codon usage bias on gene sequence evolution in butterflies and moths (Lepidoptera), including an in-depth analysis of underlying patterns and processes in one species, Leptidea sinapis. The data revealed significant G/C to A/T substitution bias at third codon position with some variation in the strength among different butterfly lineages. However, the substitution bias was lower than expected from previously estimated mutation rate ratios, partly due to the influence of gBGC. We found that A/T-ending codons were overrepresented in most species and there was a negative association between the magnitude of codon usage bias and GC-content in third codon positions. In contrast, the tRNA-gene population in L. sinapis showed higher GC-content at third codon positions compared to coding sequences in general and less overrepresentation of A/T-ending codons. There was an inverse relationship between synonymous substitutions and codon usage bias indicating selection on synonymous sites. We conclude that the evolutionary rate in Lepidoptera is affected by a complex interaction between underlying G/C -> A/T mutation bias and partly counteracting fixation biases, predominantly conferred by overall purifying selection, gBGC and selection on codon usage.
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| 6. |
- Näsvall, Karin, et al.
(author)
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Host plant diet affects growth and induces altered gene expression and microbiome composition in the wood white (Leptidea sinapis) butterfly
- 2021
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In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 30:2, s. 499-516
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Journal article (peer-reviewed)abstract
- In a time with decreasing biodiversity, especially among insects, a detailed understanding about specific resource utilization strategies is crucial. The physiological and behavioural responses to host switches in phytophagous insects are poorly understood. Earlier studies indicate that a host plant switch might be associated with distinctive molecular and physiological responses in different lineages. Expanding the assessment of such associations across Lepidoptera will reveal if there are general patterns in adaptive responses, or if each switch event is more of a unique character. We investigated host plant preference, fitness consequences, effects on expression profiles and gut microbiome composition in two common wood white (Leptidea sinapis) populations with different host plant preferences from the extremes of the species distribution area (Sweden and Catalonia). Our results show that female Catalonian wood whites lack preference for either host plant (Lotus corniculatus or L. dorycnium), while Swedish females laid significantly more eggs on L. corniculatus. Individuals from both populations reared on L. dorycnium had longer developmental times and smaller body size as adults. This indicates that both environmental and genetic factors determine the choice to use a specific host plant. Gene expression analysis revealed a more pronounced response to host plant in the Catalonian compared to the Swedish population. In addition, host plant treatment resulted in a significant shift in microbiome community structure in the Catalonian population. Together, this suggests that population specific plasticity associated with local conditions underlies host plant utilisation in wood whites.
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| 7. |
- Stoy, Kayla S., et al.
(author)
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Evaluating coevolution in a horizontally transmitted mutualism
- 2023
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In: Evolution. - : OXFORD UNIV PRESS. - 0014-3820 .- 1558-5646. ; 77:1, s. 166-185
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Journal article (peer-reviewed)abstract
- Many interspecific interactions are shaped by coevolution. Transmission mode is thought to influence opportunities for coevolution within symbiotic interactions. Vertical transmission maintains partner fidelity, increasing opportunities for coevolution, but horizontal transmission may disrupt partner fidelity, potentially reducing opportunities for coevolution. Despite these predictions, the role of coevolution in the maintenance of horizontally transmitted symbioses is unclear. Leveraging a tractable insect-bacteria symbiosis, we tested for signatures of pairwise coevolution by assessing patterns of host-symbiont specialization. If pairwise coevolution defines the interaction, we expected to observe evidence of reciprocal specialization between hosts and their local symbionts. We found no evidence for local adaptation between sympatric lineages of Anasa tristis squash bugs and Caballeronia spp. symbionts across their native geographic range. We also found no evidence for specialization between three co-localized Anasa host species and their native Caballeronia symbionts. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia symbionts. We predict that selection from multiple host species may favor generalist symbiont traits through diffuse coevolution. Alternatively, selection for generalist traits may be a consequence of selection by hosts for fixed cooperative symbiont traits without coevolution.
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| 8. |
- Talla, Venkat, et al.
(author)
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Dissecting the Effects of Selection and Mutation on Genetic Diversity in Three Wood White (Leptidea) Butterfly Species
- 2019
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In: Genome Biology and Evolution. - : Oxford University Press. - 1759-6653. ; 11:10, s. 2875-2886
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Journal article (peer-reviewed)abstract
- The relative role of natural selection and genetic drift in evolution is a major topic of debate in evolutionary biology. Most knowledge spring from a small group of organisms and originate from before it was possible to generate genome-wide data on genetic variation. Hence, it is necessary to extend to a larger number of taxonomic groups, descriptive and hypothesis-based research aiming at understanding the proximate and ultimate mechanisms underlying both levels of genetic polymorphism and the efficiency of natural selection. In this study, we used data from 60 whole-genome resequenced individuals of three cryptic butterfly species (Leptidea sp.), together with novel gene annotation information and population recombination data. We characterized the overall prevalence of natural selection and investigated the effects of mutation and linked selection on regional variation in nucleotide diversity. Our analyses showed that genome-wide diversity and rate of adaptive substitutions were comparatively low, whereas nonsynonymous to synonymous polymorphism and substitution levels were comparatively high in Leptidea, suggesting small long-term effective population sizes. Still, negative selection on linked sites (background selection) has resulted in reduced nucleotide diversity in regions with relatively high gene density and low recombination rate. We also found a significant effect of mutation rate variation on levels of polymorphism. Finally, there were considerable population differences in levels of genetic diversity and pervasiveness of selection against slightly deleterious alleles, in line with expectations from differences in estimated effective population sizes.
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| 9. |
- Talla, Venkat, et al.
(author)
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Heterogeneous Patterns of Genetic Diversity and Differentiation in European and Siberian Chiffchaff (Phylloscopus collybita abietinus/P. tristis)
- 2017
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In: G3. - : Oxford University Press (OUP). - 2160-1836. ; 7:12, s. 3983-3998
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Journal article (peer-reviewed)abstract
- Identification of candidate genes for trait variation in diverging lineages and characterization of mechanistic underpinnings of genome differentiation are key steps toward understanding the processes underlying the formation of new species. Hybrid zones provide a valuable resource for such investigations, since they allow us to study how genomes evolve as species exchange genetic material and to associate particular genetic regions with phenotypic traits of interest. Here, we use whole-genome resequencing of both allopatric and hybridizing populations of the European (Phylloscopus collybita abietinus) and the Siberian chiffchaff (P. tristis)-two recently diverged species which differ in morphology, plumage, song, habitat, and migration-to quantify the regional variation in genome-wide genetic diversity and differentiation, and to identify candidate regions for trait variation. We find that the levels of diversity, differentiation, and divergence are highly heterogeneous, with significantly reduced global differentiation, and more pronounced differentiation peaks in sympatry than in allopatry. This pattern is consistent with regional differences in effective population size and recurrent background selection or selective sweeps reducing the genetic diversity in specific regions prior to lineage divergence, but the data also suggest that post-divergence selection has resulted in increased differentiation and fixed differences in specific regions. We find that hybridization and backcrossing is common in sympatry, and that phenotype is a poor predictor of the genomic composition of sympatric birds. The combination of a differentiation scan approach with identification of fixed differences pinpoint a handful of candidate regions that might be important for trait variation between the two species.
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| 10. |
- Talla, Venkat, et al.
(author)
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Lack of gene flow : Narrow and dispersed differentiation islands in a triplet of Leptidea butterfly species
- 2019
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In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 28:16, s. 3756-3770
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Journal article (peer-reviewed)abstract
- Genome scans in recently separated species can inform on molecular mechanisms and evolutionary processes driving divergence. Large-scale polymorphism data from multiple species pairs are also key to investigate the repeatability of divergence-whether radiations tend to show parallel responses to similar selection pressures and/or underlying molecular forces. Here, we used whole-genome resequencing data from six wood white (Leptidea sp.) butterfly populations, representing three closely related species with karyomorph variation, to infer the species' demographic history and characterize patterns of genomic diversity and differentiation. The analyses supported previously established species relationships, and there was no evidence for postdivergence gene flow. We identified significant intraspecific genetic structure, in particular between karyomorph extremes in the wood white (L. sinapis)-a species with a remarkable chromosome number cline across the distribution range. The genomic landscapes of differentiation were erratic, and outlier regions were narrow and dispersed. Highly differentiated (FST ) regions generally had low genetic diversity (θπ ), but increased absolute divergence (DXY ) and excess of rare frequency variants (low Tajima's D). A minority of differentiation peaks were shared across species and population comparisons. However, highly differentiated regions contained genes with overrepresented functions related to metabolism, response to stimulus and cellular processes, indicating recurrent directional selection on a specific set of traits in all comparisons. In contrast to the majority of genome scans in recently diverged lineages, our data suggest that divergence landscapes in Leptidea have been shaped by directional selection and genetic drift rather than stable recombination landscapes and/or introgression.
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| 11. |
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| 12. |
- Talla, Venkat, et al.
(author)
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Rapid Increase in Genome Size as a Consequence of Transposable Element Hyperactivity in Wood-White (Leptidea) Butterflies
- 2017
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In: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653. ; 9:10, s. 2491-2505
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Journal article (peer-reviewed)abstract
- Characterizing and quantifying genome size variation among organisms and understanding if genome size evolves as a consequence of adaptive or stochastic processes have been long-standing goals in evolutionary biology. Here, we investigate genome size variation and association with transposable elements (TEs) across lepidopteran lineages using a novel genome assembly of the common wood-white (Leptidea sinapis) and population re-sequencing data from both L. sinapis and the closely related L. reali and L. juvernica together with 12 previously available lepidopteran genome assemblies. A phylogenetic analysis confirms established relationships among species, but identifies previously unknown intraspecific structure within Leptidea lineages. The genome assembly of L. sinapis is one of the largest of any lepidopteran taxon so far (643Mb) and genome size is correlated with abundance of TEs, both in Lepidoptera in general and within Leptidea where L. juvernica from Kazakhstan has considerably larger genome size than any other Leptidea population. Specific TE subclasses have been active in different Lepidoptera lineages with a pronounced expansion of predominantly LINEs, DNA elements, and unclassified TEs in the Leptidea lineage after the split from other Pieridae. The rate of genome expansion in Leptidea in general has been in the range of four Mb/Million year (My), with an increase in a particular L. juvernica population to 72Mb/My. The considerable differences in accumulation rates of specific TE classes in different lineages indicate that TE activity plays a major role in genome size evolution in butterflies and moths.
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| 13. |
- Talla, Venkat
(author)
-
Speciation genetics of recently diverged species :
- 2018
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Doctoral thesis (other academic/artistic)abstract
- Species differentiation can be a consequence of evolutionary forces including natural selection and random genetic drift. Patterns of genomic differentiation vary across the tree of life. This variation seems to be dependent on, for example, differences in genomic architecture and molecular mechanisms. However, the knowledge we currently possess, both regarding the processes driving speciation and the resulting genomic signatures, is from a very small subset of the overall biodiversity that resides on the planet. Therefore, characterization of the architecture of genomic divergence from more organism groups will be important to understand the effects of molecular mechanisms and evolutionary forces driving divergence between lineages. Hence it has not been possible to come to a consensus on the relative importance of genetic drift and natural selection on divergence processes in general. In this thesis, I use genomic approaches to investigate the forces underlying species and population differentiation in the European cryptic wood white butterflies (Leptidea sinapis, L. reali and L. juvernica) and two closely related bird species, the chiffchaff (Phylloscopus collybita abietinus) and the Siberian chiffchaff (P. tristis). Both these groups contain recently diverged species, a prerequisite for investigating initial differentiation processes. However, the study systems also differ in several respects, allowing for applying distinct approaches to understand the divergence process in each system.In summary, by applying a suite of genomic approaches, my thesis work gives novel insights into the speciation history of wood whites and chiffchaff. I identify candidate genes for local adaptation in both systems and concludes that genome differentiation in wood white butterflies have been driven by a combination of random genetic drift and week directional selection in allopatry. In the chiffchaff, the general differentiation landscape seems to have been shaped by recurrent background selection (and potentially selective sweeps), likely as a consequence of regional variation in the recombination rate which has also been observed in other genome-scans in birds. Potentially, some of the highly differentiated regions contain barriers to gene-flow as these regions are still present in sympatry, where species exchange genetic material at a high rate.
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| 14. |
- Talla, Venkat, et al.
(author)
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Whole genome re-sequencing uncovers significant population structure and low genetic diversity in the endangered clouded apollo (Parnasssius mnemosyne) in Sweden
- 2023
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In: Conservation Genetics. - : Springer. - 1566-0621 .- 1572-9737. ; 24, s. 305-314
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Journal article (peer-reviewed)abstract
- The clouded apollo (Parnassius mnemosyne) used to have a wide distribution in Fennoscandia. Recent population declines have, however, led to regional extinctions and in Sweden it is currently one of the most endangered butterflies, confined to three geographically separated metapopulations: Blekinge, Roslagen and Vasternorrland. Especially the Blekinge population has declined dramatically and few imagines have been observed during recent census efforts (< 10 in some localities). The clouded apollo is subject to a species action plan which includes both habitat restorations and captive breeding to produce individuals for release and reintroductions. Here, we apply whole-genome resequencing of clouded apollo individuals collected in the three natural populations and the captive population in Sweden and apply population genomic approaches to get a better understanding of the genetic structure and levels of genetic diversity in the species. We find that the clouded apollo populations in the different geographic regions have similar, but comparatively low levels of genetic diversity and we find evidence for significant genetic differentiation between the northernmost population and the populations in southern Sweden. Additional analysis, including previously available mitochondrial data, unveil that a bi-directional re-colonization of Fennoscandia after the latest glacial maximum most likely is the explanation for the considerable differentiation between some Swedish populations. Finally, we find evidence for population sub-structure in one of the Swedish populations. The results provide insights into the genetic consequences of population size declines and fragmentation in general and provide important information for direct conservation actions for the clouded apollo in Sweden in particular.
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