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Genetic variation underlying local adaptation of diapause induction along a cline in a butterfly
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-6987-5839
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Number of Authors: 42018 (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.

Place, publisher, year, edition, pages
2018. Vol. 27, no 18, p. 3613-3626
Keywords [en]
adaptation, crosses, diapause induction, ecological genetics, Lepidoptera, selection dynamics
National Category
Biological Sciences
Research subject
Population Genetics
Identifiers
URN: urn:nbn:se:su:diva-161128DOI: 10.1111/mec.14829ISI: 000444577100005PubMedID: 30105798OAI: oai:DiVA.org:su-161128DiVA, id: diva2:1258440
Available from: 2018-10-24 Created: 2018-10-24 Last updated: 2019-04-17Bibliographically approved
In thesis
1. Functional genomics of diapause in two temperate butterflies
Open this publication in new window or tab >>Functional genomics of diapause in two temperate butterflies
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
diapause induction, adaptation, genomics, transcriptomics
National Category
Evolutionary Biology
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-168042 (URN)978-91-7797-719-3 (ISBN)978-91-7797-720-9 (ISBN)
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

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