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Functional genomics of diapause in two temperate butterflies
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-6987-5839
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Natural selection will act on a given phenotype to maximize fitness in a particular environment, even if this would result in reduced fitness in other environments. In insects some of the strongest selection pressures act on timing life cycles to seasonal variation in environmental conditions, in order to maximize growth, reproduction, and to anticipate the onset of winter. Many temperate insects survive winter by entering a pre-programmed state of developmental arrest, called diapause. The decision to induce diapause is predominantly based on measuring day length. Populations have adapted to latitudinal variation in photoperiod, thereby synchronizing with local seasonal variation. However, there is no general understanding of the genetic basis for controlling diapause induction, maintenance and termination. In this thesis I aimed to gain a better understanding of the genetic basis underlying variation in the induction decision, as well as to gain insights into gene expression changes during diapause in temperate butterflies.

 

I started by revealing local adaptation in the photoperiodic response of two divergent populations of Pieris napi (Paper I). I found that variation in diapause induction among populations of both P. napi and Pararge aegeria showed strong sex-linked inheritance in inter-population crosses (Paper I and II). The genome-wide variation across populations was relatively low in both species. However, there was strong divergence in genomic regions containing the circadian clock genes timeless and period in P. aegeria, and period, cycle, and clock in P. napi. The genetic variation in these specific regions segregated between diapausing and direct developing individuals of inter-population crosses, showing that allelic variation at few genes with known functions in the circadian clock correlated to variation in diapause induction (Paper II and III).

 

Furthermore, I investigated the transcriptional dynamics in two tissues (head and abdomen) during diapause (Paper IV). Already at the first day of pupal development there are on average 409 differentially expressed genes (DEG) each up and down regulated between the direct development and diapause pathways, and this increases dramatically across these formative stages to an average of 2695. Moreover, gene expression is highly dynamic during diapause, showing more than 2600 DEG’s in the first month of diapause development, but only 20 DEG’s in the third month. Moreover, gene expression is independent of environmental conditions, revealing a pre-programmed transcriptional landscape that is active during the winter. Still, adults emerging from either the direct or diapause pathways do not show large transcriptomic differences, suggesting the adult phenotype is strongly canalized.

 

Thus, by integrating whole-genome scans with targeted genotyping and bulk-segregant analyses in population crosses, I demonstrate that adaptive variation in seasonal life cycle regulation in the two butterflies P. napi and P. aegeria both converge on genes of the circadian clock, suggesting convergent evolution in these distantly related butterflies.

Moreover, the diapause program is a dynamic process with a distinct transcriptional profile in comparison to direct development, showing that on a transcriptome level diapause development and direct development are two distinct developmental strategies.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2019. , p. 27
Keywords [en]
diapause induction, adaptation, genomics, transcriptomics
National Category
Evolutionary Biology
Research subject
Population Genetics
Identifiers
URN: urn:nbn:se:su:diva-168042ISBN: 978-91-7797-719-3 (print)ISBN: 978-91-7797-720-9 (electronic)OAI: oai:DiVA.org:su-168042DiVA, id: diva2:1305365
Public defence
2019-06-05, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2019-05-13 Created: 2019-04-16 Last updated: 2019-05-06Bibliographically approved
List of papers
1. Sex-linked inheritance of diapause induction in the butterfly Pieris napi
Open this publication in new window or tab >>Sex-linked inheritance of diapause induction in the butterfly Pieris napi
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2017 (English)In: Physiological entomology (Print), ISSN 0307-6962, E-ISSN 1365-3032, Vol. 42, no 3, p. 257-265Article in journal (Refereed) Published
Abstract [en]

Many temperate insects survive harsh environmental conditions, such as winter, by entering a state of developmental arrest. This diapause state is predominantly induced by photoperiod. The photoperiod varies with latitude and has led to local adaptation in the photoperiodic induction of diapause in many insects. To understand the rapid evolution of the photoperiodic threshold, it is important to investigate and understand the underlying genetic mechanisms. In the present study, the genetic basis of photoperiodic diapause induction is investigated in the green-veined white butterfly Pieris napi (Lepidoptera, Pieridae) by assaying diapause induction in a range of conditions for a Swedish and Spanish population. Furthermore, the inheritance of diapause induction is assessed in reciprocal F1 hybrids and backcrosses between the two populations. The southern population shows a clear photoperiodic threshold determining diapause or direct development, whereas the northern populations show a high incidence of diapause, regardless of photoperiod. The hybrid crosses reveal that the inheritance of diapause induction is strongly sex-linked, and that diapause incidence in the genetic crosses is highly dependent on photoperiod. This emphasizes the importance of assaying a range of conditions in diapause inheritance studies. The results indicate a strongly heritable diapause induction with a major component on the Z-chromosome, as well as a minor effect of the autosomal background.

Keywords
Diapause induction, inheritance, Lepidoptera, photoperiodic response, sex-linked
National Category
Biological Sciences
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-147002 (URN)10.1111/phen.12194 (DOI)000409281600008 ()
Available from: 2017-09-29 Created: 2017-09-29 Last updated: 2019-04-17Bibliographically approved
2. Genetic variation underlying local adaptation of diapause induction along a cline in a butterfly
Open this publication in new window or tab >>Genetic variation underlying local adaptation of diapause induction along a cline in a butterfly
2018 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, no 18, p. 3613-3626Article in journal (Refereed) Published
Abstract [en]

Diapause is a life history strategy allowing individuals to arrest development until favourable conditions return, and it is commonly induced by shortened day length that is latitude specific for local populations. Although understanding the evolutionary dynamics of a threshold trait like diapause induction provides insights into the adaptive process and adaptive potential of populations, the genetic mechanism of variation in photoperiodic induction of diapause is not well understood. Here, we investigate genetic variation underlying latitudinal variation in diapause induction and the selection dynamics acting upon it. Using a genomewide scan for divergent regions between two populations of the butterfly Pararge aegeria that differ strongly in their induction thresholds, we identified and investigated the patterns of variation in those regions. We then tested the association of these regions with diapause induction using between-population crosses, finding significant SNP associations in four genes present in two chromosomal regions, one with the gene period, and the other with the genes kinesin, carnitine O-acetyltransferase and timeless. Patterns of allele frequencies in these two regions in population samples along a latitudinal cline suggest strong selection against heterozygotes at two genes within these loci (period, timeless). Evidence for additional loci modifying the diapause decision was found in patterns of allelic change in relation to induction thresholds over the cline, as well as in backcross analyses. Taken together, population-specific adaptations of diapause induction appear to be due to a combination of alleles of larger and smaller effect size, consistent with an exponential distribution of effect sizes involved in local adaption.

Keywords
adaptation, crosses, diapause induction, ecological genetics, Lepidoptera, selection dynamics
National Category
Biological Sciences
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-161128 (URN)10.1111/mec.14829 (DOI)000444577100005 ()30105798 (PubMedID)
Available from: 2018-10-24 Created: 2018-10-24 Last updated: 2019-11-11Bibliographically approved
3. A chromosomal block containing clock genes associates with variation in diapause induction
Open this publication in new window or tab >>A chromosomal block containing clock genes associates with variation in diapause induction
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Developmental plasticity describes the capacity of individuals with the same genotype to induce permanent change in a phenotype depending on a specific external input. One well-studied example of adaptive developmental plasticity is the induction of facultative diapause in insects. Studies investigating the inheritance of diapause induction have suggested diverse genetic backgrounds. However, only few studies have performed unbiased genome scans to identify genes affecting the induction decision. Here we perform an unbiased whole genome scan to identify divergence between two populations that differ in their propensity to diapause, finding low divergence between these populations. We then investigate genetic differences between diapausing and directly developing siblings from backcrosses of these populations that revealed one particular region of divergence. This region is located on the Z-chromosome and contained three circadian clock genes, cyc_2, clock, and per. The results from this study help understand the genetic basis that is underlying plasticity.

National Category
Evolutionary Biology
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-168040 (URN)
Available from: 2019-04-16 Created: 2019-04-16 Last updated: 2019-04-17Bibliographically approved
4. Transcriptomic profiling of pupal diapause in the butterfly Pieris napi
Open this publication in new window or tab >>Transcriptomic profiling of pupal diapause in the butterfly Pieris napi
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Diapause is a common means of overwintering among insects that is characterized by arrested development and increased tolerance to stress and cold. Diapause is a vital aspect of life cycle timing, and 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. 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 diapause and directly developing 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 independent of environmental conditions, revealing a pre-programmed transcriptional landscape that is active during the winter. Different biological processes appear to be active in the two body parts. Still, adults emerging from either the direct or diapause pathways do not show large transcriptomic differences, suggesting the adult phenotype is strongly canalized.

National Category
Evolutionary Biology
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-168041 (URN)
Available from: 2019-04-16 Created: 2019-04-16 Last updated: 2019-04-17Bibliographically approved

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