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Spring Phenology of Butterflies: The role of seasonal variation in life-cycle regulation
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-1911-1742
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Animals and plants in temperate regions must adapt their life cycle to pronounced seasonal variation. The research effort that has gone into studying these cyclical life history events, or phenological traits, has increased greatly in recent decades. As phenological traits are often correlated to temperature, they are relevant to study in terms of understanding the effect of short term environmental variation as well as long term climate change. Because of this, changes in phenology are the most obvious and among the most commonly reported responses to climate change. Moreover, phenological traits are important for fitness as they determine the biotic and abiotic environment an individual encounters. Fine-tuning of phenology allows for synchronisation at a local scale to mates, food resources and appropriate weather conditions. On a between-population scale, variation in phenology may reflect regional variation in climate. Such differences can not only give insights to life cycle adaptation, but also to how populations may respond to environmental change through time. This applies both on an ecological scale through phenotypic plasticity as well as an evolutionary scale through genetic adaptation. In this thesis I have used statistical and experimental methods to investigate both the larger geographical patterns as well as mechanisms of fine-tuning of phenology of several butterfly species. The main focus, however, is on the orange tip butterfly, Anthocharis cardamines, in Sweden and the United Kingdom. I show a contrasting effect of spring temperature and winter condition on spring phenology for three out of the five studied butterfly species. For A. cardamines there are population differences in traits responding to these environmental factors between and within Sweden and the UK that suggest adaptation to local environmental conditions. All populations show a strong negative plastic relationship between spring temperature and spring phenology, while the opposite is true for winter cold duration. Spring phenology is shifted earlier with increasing cold duration. The environmental variables show correlations, for example, during a warm year a short winter delays phenology while a warm spring speeds phenology up. Correlations between the environmental variables also occur through space, as the locations that have long winters also have cold springs. The combined effects of these two environmental variables cause a complex geographical pattern of phenology across the UK and Sweden. When predicting phenology with future climate change or interpreting larger geographical patterns one must therefore have a good enough understanding of how the phenology is controlled and take the relevant environmental factors in to account. In terms of the effect of phenological change, it should be discussed with regards to change in life cycle timing among interacting species. For example, the phenology of the host plants is important for A. cardamines fitness, and it is also the main determining factor for oviposition. In summary, this thesis shows that the broad geographical pattern of phenology of the butterflies is formed by counteracting environmental variables, but that there also are significant population differences that enable fine-tuning of phenology according to the seasonal progression and variation at the local scale.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2016. , 42 p.
Keyword [en]
Phenology, Life cycle regulation, Phenotypic plasticity, Local adaptation, Butterflies, Diapause, Pupal development, Anthocharis cardamines, Herbivore – host plant interaction
National Category
Behavioral Sciences Biology
Research subject
Ethology
Identifiers
URN: urn:nbn:se:su:diva-132278ISBN: 978-91-7649-442-4OAI: oai:DiVA.org:su-132278DiVA: diva2:950993
Public defence
2016-09-09, 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 paper was unpublished and had a status as follows: Paper 4: Manuscript.

Available from: 2016-08-17 Created: 2016-08-04 Last updated: 2016-08-23Bibliographically approved
List of papers
1. Dissecting the contributions of plasticity and local adaptation to the phenology of a butterfly and its host plants
Open this publication in new window or tab >>Dissecting the contributions of plasticity and local adaptation to the phenology of a butterfly and its host plants
2012 (English)In: American Naturalist, ISSN 0003-0147, E-ISSN 1537-5323, Vol. 180, no 5, 655-670 p.Article in journal (Refereed) Published
Abstract [en]

Phenology affects the abiotic and biotic conditions that an organism encounters and, consequently, its fitness. For populations of high-latitude species, spring phenology often occurs earlier in warmer years and regions. Here we apply a novel approach, a comparison of slope of phenology on temperature over space versus over time, to identify the relative roles of plasticity and local adaptation in generating spatial phenological variation in three interacting species, a butterfly, Anthocharis cardamines, and its two host plants, Cardamine pratensis and Alliaria petiolata. All three species overlap in the time window over which mean temperatures best predict variation in phenology, and we find little evidence that a day length requirement causes the sensitive time window to be delayed as latitude increases. The focal species all show pronounced temperature-mediated phenological plasticity of similar magnitude. While we find no evidence for local adaptation in the flowering times of the plants, geographic variation in the phenology of the butterfly is consistent with countergradient local adaptation. The butterfly's phenology appears to be better predicted by temperature than it is by the flowering times of either host plant, and we find no evidence that coevolution has generated geographic variation in adaptive phenological plasticity.

Keyword
plasticity, local adaptation, space-for-time substitution, phenology, plant-herbivore, coevolution
National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-83024 (URN)10.1086/667893 (DOI)000309976800012 ()
Note

AuthorCount:4;

Available from: 2012-12-05 Created: 2012-12-03 Last updated: 2016-08-23Bibliographically approved
2. Variation in two phases of post-winter development of a butterfly
Open this publication in new window or tab >>Variation in two phases of post-winter development of a butterfly
2014 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 27, no 12, 2644-2653 p.Article in journal (Refereed) Published
Abstract [en]

The temporal aspects of life cycle characteristics, such as diapause development, are under strong selection in seasonal environments. Fine-tuning of the life cycle may be particularly important to match the phenology of potential mates and resources as well as for optimizing abiotic conditions at eclosion. Here, we experimentally study the spring phenology of the orange tip butterfly, Anthocharis cardamines, by analysing post-winter pupal development in three populations along a latitudinal cline in each of Sweden and the United Kingdom. These countries differ substantially in their seasonal temperature profile. By repeatedly recording pupal weights, we established that post-winter development has two separate phases, with a more rapid weight loss in the second phase than in the first, likely corresponding to a ramping up of the rate of development. Variation in the duration of the first phase contributed more strongly than the second phase to the differences in phenology between the localities and sexes. We found that insects from Sweden had a faster overall rate of development than those from the United Kingdom, which is consistent with countergradient variation, as Sweden is colder during the spring than the United Kingdom. Similar trends were not observed at the within-country scale, however. A cogradient pattern was found within Sweden, with populations from the north developing more slowly, and there was no clear latitudinal trend within the United Kingdom. In all localities, males developed faster than females. Our results point to the importance of variation in the progression of post-winter development for spring phenology.

Keyword
Anthocharis cardamines, countergradient variation, local adaptation, orange tip butterfly, phenology, post-winter development, ramping up
National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-112907 (URN)10.1111/jeb.12519 (DOI)000346280100007 ()
Note

AuthorCount:4;

Available from: 2015-01-22 Created: 2015-01-19 Last updated: 2016-08-23Bibliographically approved
3. Effect of winter cold duration on spring phenology of the orange tip butterfly, Anthocharis cardamines 
Open this publication in new window or tab >>Effect of winter cold duration on spring phenology of the orange tip butterfly, Anthocharis cardamines 
2015 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 5, no 23, 5509-5520 p.Article in journal (Refereed) Published
Abstract [en]

The effect of spring temperature on spring phenology is well understood in a wide range of taxa. However, studies on how winter conditions may affect spring phenology are underrepresented. Previous work on Anthocharis cardamines (orange tip butterfly) has shown population-specific reaction norms of spring development in relation to spring temperature and a speeding up of post-winter development with longer winter durations. In this experiment, we examined the effects of a greater and ecologically relevant range of winter durations on post-winter pupal development of A. cardamines of two populations from the United Kingdom and two from Sweden. By analyzing pupal weight loss and metabolic rate, we were able to separate the overall post-winter pupal development into diapause duration and post-diapause development. We found differences in the duration of cold needed to break diapause among populations, with the southern UK population requiring a shorter duration than the other populations. We also found that the overall post-winter pupal development time, following removal from winter cold, was negatively related to cold duration, through a combined effect of cold duration on diapause duration and on post-diapause development time. Longer cold durations also lead to higher population synchrony in hatching. For current winter durations in the field, the A. cardamines population of southern UK could have a reduced development rate and lower synchrony in emergence because of short winters. With future climate change, this might become an issue also for other populations. Differences in winter conditions in the field among these four populations are large enough to have driven local adaptation of characteristics controlling spring phenology in response to winter duration. The observed phenology of these populations depends on a combination of winter and spring temperatures; thus, both must be taken into account for accurate predictions of phenology.

National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-124985 (URN)10.1002/ece3.1773 (DOI)000367433000007 ()
Available from: 2016-01-07 Created: 2016-01-07 Last updated: 2016-08-23Bibliographically approved
4. Spring warmth and winter chilling have contrasting effects on spring phenology of pupal-overwintering butterflies
Open this publication in new window or tab >>Spring warmth and winter chilling have contrasting effects on spring phenology of pupal-overwintering butterflies
(English)Manuscript (preprint) (Other academic)
National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-131229 (URN)
Available from: 2016-06-14 Created: 2016-06-14 Last updated: 2016-08-23Bibliographically approved
5. Phenological matching rather than genetic variation in host preference underlies geographical variation in host plants used by the orange tip butterflies
Open this publication in new window or tab >>Phenological matching rather than genetic variation in host preference underlies geographical variation in host plants used by the orange tip butterflies
Show others...
2016 (English)In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312Article in journal (Refereed) Epub ahead of print
Abstract [en]

An insect species that shows variation in host species association across its geographical range may do so either because of local adaptation in host plant preference of the insect, or through environmentally or genetically induced differences in the plants, causing variation in host plant suitability between regions. Here we experimentally investigate host plant preference of Anthocharis cardamines (orange tip butterfly) of two populations from UK and two from Sweden. Previous reports indicate that A. cardamines larvae are found on different host plant species in different regions of the United Kingdom, and some variation has been reported in Sweden. Host plant choice trials showed that females prefer to oviposit on plants in an earlier phenological stage, as well as on larger plants. When controlling for plant phenological stage and size, the host species had no statistically significant effect on the choice of the females. Moreover, there were no differences in host plant species preference among the four butterfly populations. Based on our experiment, the oviposition choice by A. cardamines mainly depends on the phenological stage and the size of the host plant. This finding supports the idea that the geographical patterns of host-plant association of A. cardamines in the UK and Sweden are consequences of the phenology and availability of local hosts, rather than regional genetic differences in host species preference of the butterfly.

Keyword
Alliaria petiolata, Anthocharis cardamines, Cardamine pratensis, host plant preference, oviposition, plant-herbivore interaction
National Category
Zoology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-131164 (URN)10.1111/bij.12838 (DOI)
Available from: 2016-06-14 Created: 2016-06-14 Last updated: 2016-09-14

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