1. |
- Braga, Mariana P., et al.
(författare)
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Bayesian Inference of Ancestral Host-Parasite Interactions under a Phylogenetic Model of Host Repertoire Evolution
- 2020
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Ingår i: Systematic Biology. - : Oxford University Press (OUP). - 1063-5157 .- 1076-836X. ; 69:6, s. 1149-1162
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Tidskriftsartikel (refereegranskat)abstract
- Intimate ecological interactions, such as those between parasites and their hosts, may persist over long time spans, coupling the evolutionary histories of the lineages involved. Most methods that reconstruct the coevolutionary history of such interactions make the simplifying assumption that parasites have a single host. Many methods also focus on congruence between host and parasite phylogenies, using cospeciation as the null model. However, there is an increasing body of evidence suggesting that the host ranges of parasites are more complex: that host ranges often include more than one host and evolve via gains and losses of hosts rather than through cospeciation alone. Here, we develop a Bayesian approach for inferring coevolutionary history based on a model accommodating these complexities. Specifically, a parasite is assumed to have a host repertoire, which includes both potential hosts and one or more actual hosts. Over time, potential hosts can be added or lost, and potential hosts can develop into actual hosts or vice versa. Thus, host colonization is modeled as a two-step process that may potentially be influenced by host relatedness. We first explore the statistical behavior of our model by simulating evolution of host-parasite interactions under a range of parameter values. We then use our approach, implemented in the program RevBayes, to infer the coevolutionary history between 34 Nymphalini butterfly species and 25 angiosperm families. Our analysis suggests that host relatedness among angiosperm families influences how easily Nymphalini lineages gain new hosts.
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2. |
- Braga, Mariana P., et al.
(författare)
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Phylogenetic reconstruction of ancestral ecological networks through time for pierid butterflies and their host plants
- 2021
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Ingår i: Ecology Letters. - : Wiley. - 1461-023X .- 1461-0248. ; 24:10, s. 2134-2145
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Tidskriftsartikel (refereegranskat)abstract
- The study of herbivorous insects underpins much of the theory that concerns the evolution of species interactions. In particular, Pieridae butterflies and their host plants have served as a model system for studying evolutionary arms races. To learn more about the coevolution of these two clades, we reconstructed ancestral ecological networks using stochastic mappings that were generated by a phylogenetic model of host-repertoire evolution. We then measured if, when, and how two ecologically important structural features of the ancestral networks (modularity and nestedness) evolved over time. Our study shows that as pierids gained new hosts and formed new modules, a subset of them retained or recolonised the ancestral host(s), preserving connectivity to the original modules. Together, host-range expansions and recolonisations promoted a phase transition in network structure. Our results demonstrate the power of combining network analysis with Bayesian inference of host-repertoire evolution to understand changes in complex species interactions over time.
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3. |
- Celorio-Mancera, Maria de la Paz, et al.
(författare)
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Chromosome Level Assembly of the Comma Butterfly (Polygonia c-album)
- 2021
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Ingår i: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653. ; 13:5
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Tidskriftsartikel (refereegranskat)abstract
- The comma butterfly (Polygonia c-album, Nymphalidae, Lepidoptera) is a model insect species, most notably in the study of phenotypic plasticity and plant-insect coevolutionary interactions. In order to facilitate the integration of genomic tools with a diverse body of ecological and evolutionary research, we assembled the genome of a Swedish comma using 10X sequencing, scaffolding with matepair data, genome polishing, and assignment to linkage groups using a high-density linkage map. The resulting genome is 373 Mb in size, with a scaffold N50 of 11.7 Mb and contig N50 of 11,2Mb. The genome contained 90.1% of single-copy Lepidopteran orthologs in a BUSCO analysis of 5,286 genes. A total of 21,004 gene-models were annotated on the genome using RNA-Seq data from larval and adult tissue in combination with proteins from the Arthropoda database, resulting in a high-quality annotation for which functional annotations were generated. We further documented the quality of the chromosomal assembly via synteny assessment with Melitaea cinxia. The resulting annotated, chromosome-level genome will provide an important resource for investigating coevolutionary dynamics and comparative analyses in Lepidoptera.
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4. |
- Chazot, Nicolas, et al.
(författare)
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Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies
- 2021
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Ingår i: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 12:1
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Tidskriftsartikel (refereegranskat)abstract
- The global increase in species richness toward the tropics across continents and taxonomic groups, referred to as the latitudinal diversity gradient, stimulated the formulation of many hypotheses to explain the underlying mechanisms of this pattern. We evaluate several of these hypotheses to explain spatial diversity patterns in a butterfly family, the Nymphalidae, by assessing the contributions of speciation, extinction, and dispersal, and also the extent to which these processes differ among regions at the same latitude. We generate a time-calibrated phylogeny containing 2,866 nymphalid species (~45% of extant diversity). Neither speciation nor extinction rate variations consistently explain the latitudinal diversity gradient among regions because temporal diversification dynamics differ greatly across longitude. The Neotropical diversity results from low extinction rates, not high speciation rates, and biotic interchanges with other regions are rare. Southeast Asia is also characterized by a low speciation rate but, unlike the Neotropics, is the main source of dispersal events through time. Our results suggest that global climate change throughout the Cenozoic, combined with tropical niche conservatism, played a major role in generating the modern latitudinal diversity gradient of nymphalid butterflies.
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5. |
- Eriksson, Maertha, et al.
(författare)
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Structural plasticity of olfactory neuropils in relation to insect diapause
- 2020
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Ingår i: Ecology and Evolution. - : Wiley. - 2045-7758. ; 10:24, s. 14423-14434
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Tidskriftsartikel (refereegranskat)abstract
- Many insects that live in temperate zones spend the cold season in a state of dormancy, referred to as diapause. As the insect must rely on resources that were gathered before entering diapause, keeping a low metabolic rate is of utmost importance. Organs that are metabolically expensive to maintain, such as the brain, can therefore become a liability to survival if they are too large. Insects that go through diapause as adults generally do so before entering the season of reproduction. This order of events introduces a conflict between maintaining low metabolism during dormancy and emerging afterward with highly developed sensory systems that improve fitness during the mating season. We investigated the timing of when investments into the olfactory system are made by measuring the volumes of primary and secondary olfactory neuropils in the brain as they fluctuate in size throughout the extended diapause life-period of adult Polygonia c-album butterflies. Relative volumes of both olfactory neuropils increase significantly during early adult development, indicating the importance of olfaction to this species, but still remain considerably smaller than those of nondiapausing conspecifics. However, despite butterflies being kept under the same conditions as before the dormancy, their olfactory neuropil volumes decreased significantly during the postdormancy period. The opposing directions of change in relative neuropil volumes before and after diapause dormancy indicate that the investment strategies governing structural plasticity during the two life stages could be functionally distinct. As butterflies were kept in stimulus-poor conditions, we find it likely that investments into these brain regions rely on experience-expectant processes before diapause and experience-dependent processes after diapause conditions are broken. As the shift in investment strategies coincides with a hard shift from premating season to mating season, we argue that these developmental characteristics could be adaptations that mitigate the trade-off between dormancy survival and reproductive fitness.
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6. |
- Keehnen, Naomi, et al.
(författare)
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Geographic variation in hemocyte diversity and phagocytic propensity shows a diffuse genomic signature in the green veined white butterfly
- 2024
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Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- Insects rely on their innate immune system to successfully mediate complex interactions with their internal microbiota, as well as the microbes present in the environment. Given the variation in microbes across habitats, the challenges to respond to them is likely to result in local adaptation in the immune system. Here we focus upon phagocytosis, a mechanism by which pathogens and foreign particles are engulfed in order to be contained, killed and processed for antigen presentation. We investigated the phenotypic and genetic variation related to phagocytosis, in two allopatric populations of the butterfly Pieris napi. We found that the populations differ in their hemocyte composition, and overall phagocytic capability, driven by the increased phagocytic propensity of each cell type. However, no evidence for divergence in phagocytosis-related genes was observed, though an enrichment of genes involved in glutamine metabolism was found, which have recently been linked to immune cell differentiation in mammals.
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7. |
- Keehnen, Naomi L.P., et al.
(författare)
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A Population Genomic Investigation of Immune Cell Diversity and Phagocytic Capacity in a Butterfly
- 2021
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Ingår i: Genes. - : MDPI AG. - 2073-4425. ; 12:2
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Tidskriftsartikel (refereegranskat)abstract
- Insects rely on their innate immune system to successfully mediate complex interactions with their internal microbiota, as well as the microbes present in the environment. Given the variation in microbes across habitats, the challenges to respond to them are likely to result in local adaptations in the immune system. Here we focus upon phagocytosis, a mechanism by which pathogens and foreign particles are engulfed in order to be contained, killed, and processed. We investigated the phenotypic and genetic variation related to phagocytosis in two allopatric populations of the butterfly Pieris napi. Populations were found to differ in their hemocyte composition and overall phagocytic capability, driven by the increased phagocytic propensity of each cell type. Yet, genes annotated to phagocytosis showed no large genomic signal of divergence. However, a gene set enrichment analysis on significantly divergent genes identified loci involved in glutamine metabolism, which recently have been linked to immune cell differentiation in mammals. Together these results suggest that heritable variation in phagocytic capacity arises via a quantitative trait architecture with variation in genes affecting the activation and/or differentiation of phagocytic cells, suggesting them as potential candidate genes underlying these phenotypic differences.
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8. |
- Keehnen, Naomi L. P., et al.
(författare)
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Physiological Tradeoffs of Immune Response Differs by Infection Type in Pieris napi
- 2021
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Ingår i: Frontiers in Physiology. - : Frontiers Media SA. - 1664-042X. ; 11
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Tidskriftsartikel (refereegranskat)abstract
- Understanding the tradeoffs that result from successful infection responses is central to understanding how life histories evolve. Gaining such insights, however, can be challenging, as they may be pathogen specific and confounded with experimental design. Here, we investigated whether infection from gram positive or negative bacteria results in different physiological tradeoffs, and whether these infections impact life history later in life (post-diapause development), in the butterfly Pieris napi. During the first 24 h after infection (3, 6, 12, and 24 h), after removing effects due to injection, larvae infected with Micrococcus luteus showed a strong suppression of all non-immunity related processes while several types of immune responses were upregulated. In contrast, this tradeoff between homeostasis and immune response was much less pronounced in Escherichia coli infections. These differences were also visible long after infection, via weight loss and slower development, as well as an increased mortality at higher infection levels during later stages of development. Individuals infected with M. luteus, compared to E. coli, had a higher mortality rate, and a lower pupal weight, developmental rate and adult weight. Further, males exhibited a more negative impact of infection than females. Thus, immune responses come at a cost even when the initial infection has been overcome, and these costs are likely to affect later life history parameters with fitness consequences.
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9. |
- Keehnen, Naomi L. P., et al.
(författare)
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The consequences of surviving infection across the metamorphic boundary : tradeoff insights from RNAseq and life history measures
- 2024
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Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- The broad diversity of insect life has been shaped, in part, by pathogen pressure, yet the influence of injury and infection during critical periods of development is understudied. During development, insects undergo metamorphosis, wherein the organism experiences a dramatic shift in their overall morphology, and physiology. In temperate zones, metamorphosis is often directly followed by a developmental arrest called diapause, for which the insect needs to acquire enough energy reserves before the onset of winter. We investigated the long-term effects of injury and infection using two bacteria in the butterfly Pieris napi, revealing that the negative consequences of bacterial infection carry across the metamorphic boundary. Initial direct effects of infection were weight loss and slower development, as well as an increased mortality at higher infection levels. The detrimental effects were stronger in the gram-positive Micrococcus luteus compared to gram-negative Escherichia coli. Transcriptome-wide differences between the two bacteria were already observed in the gene expression profile of the first 24 hours after infection. Larvae infected with M. luteus showed a strong suppression of all non-immunity related processes, with several types of immune responses being activated. The impact of these transcriptomic changes, a tradeoff between homeostasis and immune response, were visible in the life history data, wherein individuals infected with M. luteus had the highest mortality rate, along with the lowest pupal weight, developmental rate and adult weight of all the treatments. Overall, we find that the cost of infection and wounding in the final larval instar carries over the metamorphic boundary, and is expected to negatively affect their lifetime fitness.
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10. |
- Lindestad, Olle, 1988-
(författare)
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Geographic variation in life cycles : Local adaptation and ecological genetics in a temperate butterfly
- 2020
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Doktorsavhandling (övrigt vetenskapligt/konstnärligt)abstract
- Conditions in nature change with the seasons, necessitating seasonal adaptations that synchronize the life cycles of organisms with their surroundings. Such regulatory adaptations must vary between populations to track local variation in climate and seasonality; this local adaptation is facilitated by locally specific seasonal cues, but may be hampered by gene flow and genetic history. For populations of temperate insects, two central features of adaptation to local climate are voltinism, the yearly number of generations; and diapause, the state of arrested development and suppressed metabolism in which most temperate insects spend winter. Delaying diapause allows for an additional generation to be produced within the same year, but this is only adaptive if the season is sufficiently long to safely accommodate such a life cycle. Hence, selection to express a locally adaptive voltinism should drive divergence between populations in diapause regulation and associated life history traits. In this thesis, I investigate variation in voltinism and life cycle regulation in a set of populations of the butterfly Pararge aegeria. Population-level variation in seasonal plasticity was tested in two sets of experiments. The first (Paper I) focused on photoperiodic plasticity during the growing season, and revealed considerable differences between populations in diapause induction and developmental reaction norms. Mechanistic modeling based on the laboratory results indicated that differences in voltinism are actively maintained by these genetic differences. Next, I tested the idea that shorter diapause may help populations achieve higher voltinism through earlier emergence in the spring (Paper II). This idea was not supported; instead, populations differed in a manner that suggests that diapause duration is selected upon by the need to avoid premature development under warm autumn conditions. The genetic background of seasonal adaptation in these populations was also explored. Phylogeographic structures inferred from genome-wide data put the results of the laboratory experiments into a historic context, and were used as the basis for a scan for genetic loci showing signs of differential selection (Paper III). The scan revealed novel variation in two circadian genes that have been shown to be linked to diapause control in P. aegeria, including a large deletion in the gene timeless. Finally, a test of two previously described circadian mutations (Paper IV) showed that, while these mutations may affect photoperiodic plasticity on a between-population level, they seemingly have no effect within a single population located at intermediate latitudes. Closer inspection revealed novel, locally unique mutations in the same genes, possibly compensating for the effect of diapause-delaying variants in a setting where an attempted second generation is not adaptive. I have shown that voltinism variation in P. aegeria is enabled by population differences in seasonal plasticity, with population differences playing a greater role during some parts of the year than others. These results present voltinism as a complex trait resulting from plasticity acting at different levels of geographic specificity. Although much of the genetic variation enabling the observed local adaptation remains uncharacterized, the considerably variable circadian genes seen in these populations provide an intriguing target for future investigation.
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11. |
- Lindestad, Olle, et al.
(författare)
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Local adaptation of life cycles in a butterfly is associated with variation in several circadian clock genes
- 2022
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Ingår i: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 31:5, s. 1461-1475
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Tidskriftsartikel (refereegranskat)abstract
- Many insects exhibit geographical variation in voltinism, the number of generations produced per year. This includes high-latitude species in previously glaciated areas, meaning that divergent selection on life cycle traits has taken place during or shortly after recent colonization. Here, we use a population genomics approach to compare a set of nine Scandinavian populations of the butterfly Pararge aegeria that differ in life cycle traits (diapause thresholds and voltinism) along both north-south and east-west clines. Using a de novo-assembled genome, we reconstruct colonization histories and demographic relationships. Based on the inferred population structure, we then scan the genome for candidate loci showing signs of divergent selection potentially associated with population differences in life cycle traits. The identified candidate genes include a number of components of the insect circadian clock (timeless, timeless2, period, cryptochrome and clockwork orange). Most notably, the gene timeless, which has previously been experimentally linked to life cycle regulation in P. aegeria, is here found to contain a novel 97-amino acid deletion unique to, and fixed in, a single population. These results add to a growing body of research framing circadian gene variation as a potential mechanism for generating local adaptation of life cycles.
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12. |
- Ma, Lijun, et al.
(författare)
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A phylogenomic tree inferred with an inexpensive PCR-generated probe kit resolves higher-level relationships among Neptis butterflies (Nymphalidae: Limenitidinae)
- 2020
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Ingår i: Systematic Entomology. - : Wiley. - 0307-6970 .- 1365-3113. ; 45:4, s. 924-934
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Tidskriftsartikel (refereegranskat)abstract
- Recent advances in obtaining reduced representation libraries for next-generation sequencing permit phylogenomic analysis of species-rich, recently diverged taxa. In this study, we performed sequence capture with homemade PCR-generated probes to study diversification among closely related species in a large insect genus to examine the utility of this method. We reconstructed the phylogeny of Neptis Fabricius, a large and poorly studied nymphalid butterfly genus distributed throughout the Old World. We inferred relationships among 108 Neptis samples using 89 loci totaling up to 84 519 bp per specimen. Our taxon sample focused on Palearctic, Oriental and Australasian species, but included 8 African species and outgroups from 5 related genera. Maximum likelihood and Bayesian analyses yielded identical trees with full support for almost all nodes. We confirmed that Neptis is not monophyletic because Lasippa heliodore (Fabricius) and Phaedyma amphion (Linnaeus) are nested within the genus, and we redefine species groups for Neptis found outside of Africa. The statistical support of our results demonstrates that the probe set we employed is useful for inferring phylogenetic relationships among Neptis species and likely has great value for intrageneric phylogenetic reconstruction of Lepidoptera. Based on our results, we revise the following two taxa: Neptis heliodore comb. rev. and Neptis amphion comb. rev.
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13. |
- Nielsen, Matthew, et al.
(författare)
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Evolution of butterfly seasonal plasticity driven by climate change varies across life stages
- 2023
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Ingår i: Ecology Letters. - 1461-023X .- 1461-0248. ; 26:9, s. 1548-1558
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Tidskriftsartikel (refereegranskat)abstract
- Photoperiod is a common cue for seasonal plasticity and phenology, but climate change can create cue-environment mismatches for organisms that rely on it. Evolution could potentially correct these mismatches, but phenology often depends on multiple plastic decisions made during different life stages and seasons that may evolve separately. For example, Pararge aegeria (Speckled wood butterfly) has photoperiod-cued seasonal life history plasticity in two different life stages: larval development time and pupal diapause. We tested for climate change-associated evolution of this plasticity by replicating common garden experiments conducted on two Swedish populations 30 years ago. We found evidence for evolutionary change in the contemporary larval reaction norm-although these changes differed between populations-but no evidence for evolution of the pupal reaction norm. This variation in evolution across life stages demonstrates the need to consider how climate change affects the whole life cycle to understand its impacts on phenology.
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14. |
- Pruisscher, Peter, et al.
(författare)
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Extensive transcriptomic profiling of pupal diapause in a butterfly reveals a dynamic phenotype
- 2022
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Ingår i: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 31:4, s. 1269-1280
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Tidskriftsartikel (refereegranskat)abstract
- Diapause is a common adaptation for overwintering in insects that is characterized by arrested development and increased tolerance to stress and cold. While the expression of specific candidate genes during diapause have been investigated, there is no general understanding of the dynamics of the transcriptional landscape as a whole during the extended diapause phenotype. Such a detailed temporal insight is important as diapause is a vital aspect of life cycle timing. Here, we performed a time-course experiment using RNA-Seq on the head and abdomen in the butterfly Pieris napi. In both body parts, comparing diapausing and nondiapausing siblings, differentially expressed genes are detected from the first day of pupal development and onwards, varying dramatically across these formative stages. During diapause there are strong gene expression dynamics present, revealing a preprogrammed transcriptional landscape that is active during the winter. Different biological processes appear to be active in the two body parts. Finally, adults emerging from either the direct or diapause pathways do not show large transcriptomic differences, suggesting the adult phenotype is strongly canalized.
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