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Life-history consequenses of host plant choice in the comma butterfly
Stockholm University, Faculty of Science, Department of Zoology.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

There is much evidence that herbivory is a key innovation for the tremendous success of insect. In this thesis I have investigated different aspects of host plant utilization and phenotypic plasticity using the polyphagous comma butterfly, Polygonia c-album. Even though external conditions affect a phenotypic plastic response, the outcome is often influenced by a genetic background which may differ among populations. In Paper I we suspected the genetic background to seasonal polymorphism to be X-linked. However, results from interspecific hybridization between two populations suggested that diapause response is instead inherited in a mainly autosomally additive fashion, with a possible influence of sexual antagonism on males. In Paper II we showed that female oviposition preference is not a plastic response influenced by larval experience, but has a genetic background coupled to host plant suitability. Further, there is a strong individual correlation between larval host plant acceptance and female host plant specificity (Paper III). We believe this to be a larval feed-back genetically linked to female host specificity: offspring to ‘choosy’ specialist mothers benefit by remaining on the original host while offspring to less discriminating generalist mothers should risk inspecting the surroundings, thus compensating for potential poor female choice. In the larval mid-gut, genes are differentially expressed depending on host plant diet (Paper IV). Therefore, we expected to find fitness consequences of host plant switch. However, although growth rate was affected in a few treatments, larvae were generally surprisingly good at adjusting to new diets (Paper V). To conclude, host plant choice in both female and larval life stage is connected to performance. Combined with increased understanding about the plastic response to diet intake and seasonal polymorphism we have gained further insights into the processes of local adaptations and speciation in the Lepidoptera.

Place, publisher, year, edition, pages
Department of Zoology, Stockholm University , 2012. , 36 p.
Keyword [en]
Nymphalidae, voltinism, larval performance, Hopkins’ Host Selection Principle, GeneFishing, real-time qPCR, Urtica dioica, Salix cinerea, Betula pubescens, Ulmus glabra, Ribes uva-crispa.
National Category
Zoology
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-68076ISBN: 978-91-7447-432-9 (print)OAI: oai:DiVA.org:su-68076DiVA: diva2:471762
Public defence
2012-02-10, Magnélisalen, Kemiska övningslaboratoriet, Svante Arrhenius väg 16 B, 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: Submitted Manuscript; Paper 5: ManuscriptAvailable from: 2012-01-19 Created: 2012-01-02 Last updated: 2014-10-28Bibliographically approved
List of papers
1. Genetics of diapause in the comma butterfly Polygonia c-album
Open this publication in new window or tab >>Genetics of diapause in the comma butterfly Polygonia c-album
2011 (English)In: Physiological entomology (Print), ISSN 0307-6962, E-ISSN 1365-3032, Vol. 36, no 1, 8-13 p.Article in journal (Refereed) Published
Abstract [en]

The processes of local adaptation and ecological speciation can be better understood by studying the genetic background of life-history decisions. The sex chromosomes host genes for many population differences in the Lepidoptera and therefore the inheritance of diapause determination in the butterfly Polygonia c-album may be hypothesized to be sex-linked. In the present study, Polygonia c-album (L.) from Spain and Sweden and hybrid offspring are raised under an LD 17 : 7 h photocycle that induces most pure Swedish individuals to develop into the diapausing dark morph and most pure Spanish individuals into the light and directly-developing morph. If inheritance of the daylength threshold for diapause is X-linked, as is known to be the case for host-plant preferences, females should follow the developmental path of their male parents' populations. However, female hybrids instead have a diapause propensity intermediate to that of their parental stocks and, consequentially, diapause determination is not X-linked. However, male hybrids eclose as the diapausing morph to a higher extent than females and, moreover, this pattern is more pronounced in the Spanish female x Swedish male cross than in the reciprocal cross. Hence, it is concluded that the genetic determination of the critical daylength for diapause is mainly autosomal but with some influence of sex-linked genes and/or parental effects, possibly as an effect of the importance of protandry for males. Such sex effects could provide a starting point for the evolution of population differences inherited on the sex chromosomes.

Keyword
Autosomal inheritance, intraspecific hybridization, parental effect, photoperiod, seasonal polyphenism, sex effect, sex linkage
National Category
Zoology
Identifiers
urn:nbn:se:su:diva-67901 (URN)10.1111/j.1365-3032.2010.00756.x (DOI)000287790900002 ()
Note
authorCount :2Available from: 2012-01-03 Created: 2012-01-02 Last updated: 2017-12-08Bibliographically approved
2. No effect of larval experience on adult host preferences in Polygonia c-album (Lepidoptera: Nymphalidae): on the persistence of Hopkins' host selection principle
Open this publication in new window or tab >>No effect of larval experience on adult host preferences in Polygonia c-album (Lepidoptera: Nymphalidae): on the persistence of Hopkins' host selection principle
2009 (English)In: Ecological Entomology, ISSN 0307-6946, E-ISSN 1365-2311, Vol. 34, no 1, 50-57 p.Article in journal (Refereed) Published
Abstract [en]

1. The possible effect of juvenile imprinting or 'chemical legacy' on the subsequent oviposition - often called the 'Hopkins' host selection principle' - has been a controversial but recurrent theme in the literature on host-plant preference. While it appears possible in principle, experimental support for the hypothesis is equivocal. The present study points out that it is also important to consider its theoretical implications, and asks under what circumstances, if any, it should be favoured by natural selection.

2. Following this reasoning, it is predicted that host preference in the polyphagous butterfly Polygonia c-album L. (Lepidoptera, Nymphalidae) should not be influenced by larval environment. This was tested by rearing larvae on three natural host plants: the high-ranked Urtica dioica and the medium-ranked Salix cinerea and Ribes uva-crispa, and exposing the naive females to oviposition choices involving the same set of plants.

3. It was found that larval host plant had no effect on oviposition decisions of the adult female. Hence, the Hopkins' host selection principle does not seem to be applicable in this species.

4. Based on recent insights on how accuracy of environmental versus genetic information should affect the control of developmental switches, the conditions that could favour the use of juvenile cues in oviposition decisions are discussed. Although the Hopkins' host selection hypothesis cannot be completely ruled out, we argue that the circumstances required for it to be adaptive are so specific that it should not be invoked as a general hypothesis for host selection in plant-feeding insects.

 

Place, publisher, year, edition, pages
Oxford: Blackwell, 2009
Keyword
Chemical legacy, environmental cues, genetic cues, host-plant preference, Polygonia c-album, phenotypic plasticity, pre-imaginal conditioning, specialisation
National Category
Ecology Ecology Developmental Biology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-28284 (URN)10.1111/j.1365-2311.2008.01041.x (DOI)000262468000007 ()
Available from: 2009-06-12 Created: 2009-06-12 Last updated: 2017-12-13Bibliographically approved
3. When mother does not know best: Contrasting host plant choice across life stages in individuals of the comma butterfly
Open this publication in new window or tab >>When mother does not know best: Contrasting host plant choice across life stages in individuals of the comma butterfly
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Since host plant choice is often crucial for the fitness of herbivorous insects we investigated if individual variation in such decisions is consistent throughout life. In the comma butterfly, Polygonia c-album, (Nymphalidae, Nymphalini) newly hatched larvae and adult females have been found to rank hosts plants similarly, suggesting that the host plant recognition mechanisms could be preserved through metamorphosis. 

We measured preference for Urtica dioica relative to Salix cinerea when the plants were encountered by the same individuals in the two different life stages, finding no relationship between the two measurements. This was however found when we instead measured acceptance of a suboptimal host: First instar larvae were placed on the suboptimal S. cinerea, and were scored as to whether they accepted this host or if they instead moved to feed on the generally more preferred host U. dioica. The same individuals were then tested once more as ovipositing females, in a cage setup arranged so that females would encounter the low-ranked hosts S. cinerea and Betula pubescens more often than the high-ranked host U. dioica.

Individuals that chose to abandon S. cinerea as larvae differed in oviposition behaviour later in life from those that accepted this low-ranked host, but did so by laying a higher proportion eggs on the low-ranked hosts as adults. We interpret this initially unexpected result as a result of possible genetic correlation between female host-plant specificity and larval acceptance for the plant chosen by their mother: Offspring of ‘choosy’ specialist mothers have a strong tendency to remain on their original host, whereas less discriminating generalist mothers beget larvae with lower acceptance for their original plant when it is suboptimal. Ecologically, this presents a further explanation for how a generalist oviposition strategy can be sustained since larval mobility to some extent compensates for poor female choice.

Keyword
insect-plant interactions, host plant choice, life-history, preference-performance correlations, personality, behavioural syndrome
National Category
Zoology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-68074 (URN)
Available from: 2012-01-02 Created: 2012-01-02 Last updated: 2014-10-28Bibliographically approved
4. Phylogenetic relatedness and host plant growth form influence gene expression of the polyphagous comma butterfly (Polygonia c-album).
Open this publication in new window or tab >>Phylogenetic relatedness and host plant growth form influence gene expression of the polyphagous comma butterfly (Polygonia c-album).
Show others...
2009 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 10, no 1, 506- p.Article in journal (Refereed) Published
Abstract [en]

ABSTRACT: BACKGROUND: The mechanisms that shape the host plant range of herbivorous insect are to date not well understood but knowledge of these mechanisms and the selective forces that influence them can expand our understanding of the larger ecological interaction. Nevertheless, it is well established that chemical defenses of plants influence the host range of herbivorous insects. While host plant chemistry is influenced by phylogeny, also the growth forms of plants appear to influence the plant defense strategies as first postulated by Feeny (the "plant apparency" hypothesis). In the present study we aim to investigate the molecular basis of the diverse host plant range of the comma butterfly (Polygonia c-album) by testing differential gene expression in the caterpillars on three host plants that are either closely related or share the same growth form. RESULTS: In total 120 differentially expressed genes were identified in P. c-album after feeding on different host plants, 55 of them in the midgut and 65 in the restbody of the caterpillars. Expression patterns could be confirmed with an independent method for 14 of 27 tested genes. Pairwise similarities in upregulation in the midgut of the caterpillars were higher between plants that shared either growth form or were phylogenetically related. No known detoxifying enzymes were found to be differently regulated in the midgut after feeding on different host plants. CONCLUSIONS: Our data suggest a complex picture of gene expression in response to host plant feeding. While each plant requires a unique gene regulation in the caterpillar, both phylogenetic relatedness and host plant growth form appear to influence the expression profile of the polyphagous comma butterfly, in agreement with phylogenetic studies of host plant utilization in butterflies.

National Category
Zoology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-31352 (URN)10.1186/1471-2164-10-506 (DOI)000271883700002 ()19878603 (PubMedID)
Available from: 2009-11-10 Created: 2009-11-10 Last updated: 2017-12-12Bibliographically approved
5. Effects of sequential diets in the comma butterfly, Polygonia c-album: testing predictions from gene expression
Open this publication in new window or tab >>Effects of sequential diets in the comma butterfly, Polygonia c-album: testing predictions from gene expression
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Differential gene expression, depending on host plant diet, has been found in the larval mid-gut of the polyphagous butterfly Polygonia c-album. Expression similarities between the hosts elm/sallow and between elm/stinging nettle suggest that there are special patterns of genes for utilizing trees and others for urticalean rosids.

In order to assess the importance of different genes tailored to host use, we investigated the costs of switching larval diet. Negative effects were expected to be more pronounced when switching between nettle/sallow than between elm/nettle (urticalean rosids) or elm/sallow (trees) since similarities in mid-gut gene expression are fewer.

However, larvae seemed surprisingly good at adjusting to new environments. Although costs were found after a single switch from sallow to nettle in the 3rd instar as well as on a daily basis the results were not consistent. More surprisingly, we found evidence that costs are involved with a single diet switch to elm. Results suggest rapid physiological adjustment to the new environment, signifying that the induced gene expression is reversible or at least does not seem to inhibit the induction of another gene complex.

Keyword
phenotypic plasticity, polyspecialist, Nymphalidae
National Category
Zoology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-68075 (URN)
Available from: 2012-01-02 Created: 2012-01-02 Last updated: 2014-10-28Bibliographically approved

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