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Analyzing the neutral and adaptive background of butterfly voltinism reveals structural variation in a core circadian gene
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-8226-3167
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Many insects exhibit geographic variation in voltinism, the number of generations produced per year. This includes high-latitude species in previously glaciated areas, implying divergent selection on life cycle traits during or shortly after recent colonization. Here, we use a whole-genome approach to genetically characterize a set of populations of the butterfly Pararge aegeria that differ in voltinism. We construct a high-quality de novo genome for P. aegeria, and assess genome-wide genetic diversity and differentiation between populations. We then use the inferred phylogeographic relationships as the basis for a scan for loci showing signs of divergent selection associated with voltinism differences. The genic outliers detected include population-specific mutations of circadian loci, most notably a locally fixed 97-amino acid deletion in the circadian gene timeless. Variation in timeless has previously been implicated as underlying variation in life cycle regulation in wild populations in our study species, as well as in other insects. These results add to a growing body of research framing circadian gene variation as a mechanism for generating local adaptation of life cycles.

National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-176986OAI: oai:DiVA.org:su-176986DiVA, id: diva2:1377566
Available from: 2019-12-12 Created: 2019-12-12 Last updated: 2019-12-13Bibliographically approved
In thesis
1. Geographic variation in life cycles: Local adaptation and ecological genetics in a temperate butterfly
Open this publication in new window or tab >>Geographic variation in life cycles: Local adaptation and ecological genetics in a temperate butterfly
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

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.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2020. p. 28
Keywords
voltinism, local adaptation, insect, life cycle, seasonality, genomics, life history
National Category
Ecology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-176993 (URN)978-91-7797-947-0 (ISBN)978-91-7797-948-7 (ISBN)
Public defence
2020-02-14, Vivi Täckholm-salen (Q-salen), NPQ-huset, Svante Arrheniusväg 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 2: Accepted. Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2020-01-22 Created: 2019-12-12 Last updated: 2019-12-20Bibliographically approved

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