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Geographic variation in life cycles: Local adaptation and ecological genetics in a temperate butterfly
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-8226-3167
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 [en]
voltinism, local adaptation, insect, life cycle, seasonality, genomics, life history
National Category
Ecology
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-176993ISBN: 978-91-7797-947-0 (print)ISBN: 978-91-7797-948-7 (electronic)OAI: oai:DiVA.org:su-176993DiVA, id: diva2:1377626
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
List of papers
1. Local adaptation of photoperiodic plasticity maintains life cycle variation within latitudes in a butterfly
Open this publication in new window or tab >>Local adaptation of photoperiodic plasticity maintains life cycle variation within latitudes in a butterfly
2019 (English)In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 100, no 1, article id e02550Article in journal (Refereed) Published
Abstract [en]

The seasonal cycle varies geographically and organisms are under selection to express life cycles that optimally exploit their spatiotemporal habitats. In insects, this often means producing an annual number of generations (voltinism) appropriate to the local season length. Variation in voltinism may arise from variation in environmental factors (e.g., temperature or photoperiod) acting on a single reaction norm shared across populations, but it may also result from local adaptation of reaction norms. However, such local adaptation is poorly explored at short geographic distances, especially within latitudes. Using a combination of common-garden rearing and life cycle modeling, we have investigated the causal factors behind voltinism variation in Swedish populations of the butterfly Pararge aegeria, focusing on a set of populations that lie within a single degree of latitude but nonetheless differ in season length and voltinism. Despite considerable differences in ambient temperature between populations, modeling suggested that the key determinant of local voltinism was in fact interpopulation differences in photoperiodic response. These include differences in the induction thresholds for winter diapause, as well as differences in photoperiodic regulation of larval development, a widespread but poorly studied phenomenon. Our results demonstrate previously neglected ways that photoperiodism may mediate insect phenological responses to temperature, and emphasize the importance of local adaptation in shaping phenological patterns in general, as well as for predicting the responses of populations to changes in climate.

Keywords
insects, Lepidoptera, life history, local adaptation, phenology, photoperiodism, plasticity, voltinism
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-165790 (URN)10.1002/ecy.2550 (DOI)000454706400021 ()30375642 (PubMedID)
Available from: 2019-02-19 Created: 2019-02-19 Last updated: 2020-02-20Bibliographically approved
2. Variation in butterfly diapause duration in relation to voltinism suggests adaptation to autumn warmth, not winter cold
Open this publication in new window or tab >>Variation in butterfly diapause duration in relation to voltinism suggests adaptation to autumn warmth, not winter cold
(English)In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435Article in journal (Refereed) Accepted
Abstract [en]

The life cycles of animals vary in relation to local climate, as a result of both direct environmental effects and population-level variation in plastic responses. Insects often respond to the approach of winter by entering diapause, a hormonally programmed resting state where development is suspended and metabolism suppressed. Populations often differ in the duration of diapause, but the adaptive reasons for this are unclear. We performed a common-garden overwintering experiment with respirometric measurements in order to investigate the progression of diapause in the butterfly Pararge aegeria. Both the duration of diapause and the depth of metabolic suppression were shown to vary between populations. In contrast to previous results from various insects, diapause duration did not correspond to the local length of winter. Instead, the observed pattern was consistent with a scenario in which diapause duration is primarily a product of selection for suppressed metabolism during warm autumn conditions. The relationship between optimal diapause duration and the length of the warm season is complicated by variation in the number of yearly generations (voltinism). These results shed new light on variation in diapause ecophysiology, and highlight voltinism as an integrated product of selection at multiple points in the seasonal cycle.

National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-176991 (URN)
Available from: 2019-12-12 Created: 2019-12-12 Last updated: 2020-03-05
3. Analyzing the neutral and adaptive background of butterfly voltinism reveals structural variation in a core circadian gene
Open this publication in new window or tab >>Analyzing the neutral and adaptive background of butterfly voltinism reveals structural variation in a core circadian gene
(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:nbn:se:su:diva-176986 (URN)
Available from: 2019-12-12 Created: 2019-12-12 Last updated: 2020-02-20Bibliographically approved
4. Context-dependent candidate genes: a test of within-population genetic variation for photoperiodic plasticity
Open this publication in new window or tab >>Context-dependent candidate genes: a test of within-population genetic variation for photoperiodic plasticity
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Components of the circadian clock have been implicated as involved in photoperiodic regulation of diapause across various insect groups, hence contributing to adaptation to adverse seasonal conditions. Such studies typically involve either characterization of nondiapause mutants, or comparisons of populations differing in diapause induction thresholds, leaving within-population variation unexplored. Here, we present a test of the effects on diapause induction of within-population variation at two circadian loci, timeless and period, in the butterfly Pararge aegeria. Variation at both loci has previously shown to be associated with diapause induction on an interpopulation level. However, in the present study, no effect on induction was found of either locus at a within-population level. Examination of sequence data revealed novel variation at both timeless and period in the studied population. We hypothesize that selection for a northern-type life cycle may have promoted compensatory variants, ensuring a high rate of diapause induction despite the presence of southern, diapause-averting SNP alleles. Additionally, both timeless and period showed considerable variation across Scandinavian populations, with an unusually high rate of nonsynonymous substitutions compared to the rest of the genome, raising new questions about the fine-scale adaptive dynamics of circadian genes.

National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-176989 (URN)
Available from: 2019-12-12 Created: 2019-12-12 Last updated: 2020-02-20Bibliographically approved

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