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Why stay in a bad relationship? The effect of local host phenology on a generalist butterfly feeding on a low-ranked host
Stockholm University, Faculty of Science, Department of Zoology. Paris-Est Créteil University, France.
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: 4
2016 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 16, 144Article in journal (Refereed) Published
Abstract [en]

Background: In plant-feeding insects, the evolutionary retention of polyphagy remains puzzling. A better understanding of the relationship between these organisms and changes in the metabolome of their host plants is likely to suggest functional links between them, and may provide insights into how polyphagy is maintained. Results: We investigated the phenological change of Cynoglossum officinale, and how a generalist butterfly species, Vanessa cardui, responded to this change. We used untargeted metabolite profiling to map plant seasonal changes in both primary and secondary metabolites. We compared these data to differences in larval performance on vegetative plants early and late in the season. We also performed two oviposition preference experiments to test females' ability to choose between plant developmental stages (vegetative and reproductive) early and late in the season. We found clear seasonal changes in plant primary and secondary metabolites that correlated with larval performance. The seasonal change in plant metabolome reflected changes in both nutrition and toxicity and resulted in zero survival in the late period. However, large differences among families in larval ability to feed on C. officinale suggest that there is genetic variation for performance on this host. Moreover, females accepted all plants for oviposition, and were not able to discriminate between plant developmental stages, in spite of the observed overall differences in metabolite profile potentially associated with differences in suitability as larval food. Conclusions: In V. cardui, migratory behavior, and thus larval feeding times, are not synchronized with plant phenology at the reproductive site. This lack of synchronization, coupled with the observed lack of discriminatory oviposition, obviously has potential fitness costs. However, this opportunistic behavior may as well function as a source of potential host plant evolution, promoting for example the acceptance of new plants.

Place, publisher, year, edition, pages
2016. Vol. 16, 144
Keyword [en]
Adaptation, GC-MS, Host plant range, Larval performance, LC-MS, Metabolomics, Oviposition preference, Plasticity, Primary and secondary metabolites, Vanessa cardui
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-132390DOI: 10.1186/s12862-016-0709-xISI: 000378675500004PubMedID: 27356867OAI: oai:DiVA.org:su-132390DiVA: diva2:952646
Available from: 2016-08-15 Created: 2016-08-11 Last updated: 2017-03-16Bibliographically approved
In thesis
1. Effect of climate and land use on niche utilization and distribution of nettle-feeding  butterflies
Open this publication in new window or tab >>Effect of climate and land use on niche utilization and distribution of nettle-feeding  butterflies
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Anthropogenic changes in climate and land use are causing a dramatic erosion of biodiversity. To understand this erosion, and predict future transformations of biodiversity, we need to understand better species’ response to these changes at different spatial and temporal scales. Modeling studies have identified correlations between physical parameters of the environment and species’ distribution at large spatial scales. However, this does not accurately characterize the response of a specific species, since this does not account for the constraints arising from the biology of the species. This thesis shall combine knowledge on the biology of species obtained from laboratory experiments with modeling studies. This will allow us (i) to identify life history traits and biotic interactions that influence species’ adaptive potential, and hence, explain possible differences in species’ distribution, and (ii) to consider, not only the ecological but also the evolutionary aspects of species’ response to changes. This integrative approach is likely to improve our predictions on species’ population dynamic in a changing environment.

I focus on a community of butterflies in Sweden (Vanessa cardui, Polygonia c-album, Aglais urticae, Aglais io, Araschnia levana) that feeds on the stinging nettle (Urtica dioica). The available knowledge on the biology of these species and their short life cycles, which allow investigations of their response to changes on a short-time scale, make them a good system to study. Among three of these species, I showed great differences in organisms’ response to variation in food nutrient content. This is a potentially important finding considering the increased use of chemical fertilizers. These differences are to a large extent explained by differences among species in their degree of host plant specialization and voltinism (paper II). Thus, life history traits determine the response of species to environmental changes, but are themselves likely to evolve in response to such changes. Climate change, for instance, may alter the phenological synchrony between plant-feeding insects and their host plants, making it necessary for the insects to evolve their host plant range in order to ensure the availability of resources during larval development (paper I & III). The biology of a species, including biotic interactions, helps to explain the observed shift in a species’ distribution and environmental niche that result from climate change. I have shown that the recent establishment of A. levana in southern Sweden has modified the niche of the resident species, A. urticae and A. io (Paper IV). Niche partitioning in this community is likely mediated by parasite-driven apparent competition.

Abstract [sv]

Mänsklig påverkan på klimat och markanvändning har orsakat en dramatisk förlust av biologisk mångfald. Effekten av dessa förändringar på lokal och regional nivå är dock komplex, och kräver integrativa strategier för att kunna förstå och förutsäga förändringar, på individ-, art- och samhällsnivå. Experimentella studier har utforskat arters plastiska och evolutionära respons till främst abiotiska förändringar, och observationsdata har använts för att modellera skiften i fenologi och utbredning som en konsekvens av klimatförändringar. Trots detta är det fortfarande mycket kvar att förstå för att kunna förutsäga hur miljöförändringar ska påverka arters respons på olika rumsliga och tidsliga skalor. Denna avhandling undersöker i vilken utsträckning arters specifika livshistoria och artinteraktioner kan förklara deras ekologiska och evolutionära respons på miljöförändringar.

För att angripa detta har jag fokuserat på ett samhälle av fjärilar i Sverige (Vanessa cardui, Polygonia c-album, Aglais urticae, Aglais io, Araschnia levana) som alla lever på brännässla (Urtica dioica). Den tillgängliga kunskapen om dessa arters biologi samt deras korta livscykler gör det möjligt att undersöka deras svar på förändringar över korta tidsskalor, vilket gör dem till ett lämpligt studiesystem. Huvudslutsatsen från denna avhandling är att för att beskriva hur en art svarar på en förändring måste man ta hänsyn till variation i livshistorieegenskaper och artinteraktioner. Till exempel har den ökade användningen av kemiska gödningsmedel förändrat näringstillgången även i naturliga ekosystem, vilket gynnar växtarter som är kapabla att växa under höga näringsnivåer, som brännässla. Variation i växternas näringsinnehåll kommer i sin tur att påverka herbivorerna som äter av dem, och artikel II visar att skillnader mellan fjärilsarter i hur de svarar på variation i näringstillgång till stor del beror på specialiseringsgrad och voltinism (antal generationer per år). Livshistorieegenskaper avgör således hur arter kommer att svara på förändringar i klimat och markanvändning, men sådana miljöförändringar påverkar i sin tur också evolution av livshistorieegenskaperna (artikel I & III). Slutligen, förändringar i utbredning som ett resultat av klimatförändring kommer även att påverka den lokala sammansättningen av interagerande arter (resurser, predatorer, konkurrenter). Ett exempel på detta är hur den relativt nyliga koloniseringen av södra Sverige av A. levana har förändrat nischerna hos de inhemska arterna A. urticae och A. io (artikel IV).

Abstract [fr]

Le réchauffement climatique et les changements d’occupation des terres d'origine anthropique provoquent une forte érosion de la biodiversité. Pour comprendre cette érosion, et prédire les transformations futures de la biodiversité, il nous faut mieux connaitre la réponse des espèces à ces changements, aux différentes échelles spatiales et temporelles. Grâce à des outils de modélisation statistique, des corrélations entre les paramètres physiques de l’environnement et la distribution des espèces à grande échelle spatiale ont été observées. Mais ceci ne suffit pas à caractériser finement la réponse d’une espèce donnée, car celle-ci dépend des caractéristiques biologiques propres de l’espèce. Cette thèse se propose donc d’associer les connaissances sur la biologie des espèces obtenues par des expériences en laboratoire à des études de modélisation. Ceci permettra (i) d’identifier des traits d’histoire de vie et les relations biotiques qui influencent le potentiel adaptatif des espèces, et donc expliquent d’éventuelles différences de répartition, et (ii) d’envisager, au-delà des aspects écologiques, la composante évolutive de cette réponse. Une telle approche intégrative est susceptible d’améliorer nos prédictions sur la dynamique des espèces dans un environnement changeant.

Le système d’étude de cette thèse est une communauté de papillons en Suède (Vanessa cardui, Polygonia c-album, Aglais urticae, Aglais io, Araschnia levana), se nourrissant de l'ortie (Urtica dioica). La biologie de ces espèces est bien connue et leur cycle de vie rapide permet d’étudier leur réponse aux changements à une échelle de temps court. Chez trois de ces espèces, j’ai mis en évidence des réponses très différentes à une augmentation de la teneur en nutriments de leur nourriture, conséquence attendue de l’utilisation accrue d’engrais chimiques. Ces différences sont dans une large mesure expliquée par la gamme de plantes hôtes utilisées et le voltinisme (article II). Ces traits d'histoire de vie déterminent donc la réponse des espèces aux changements, mais sont eux-mêmes susceptibles d’évoluer. Par exemple, le réchauffement climatique modifie la synchronie entre les insectes herbivores et leurs plantes hôtes et pousse à l’évolution du régime alimentaire des papillons afin que la présence de ressources soit assurée durant le développement des larves (articles I & III). Les connaissances sur la biologie des espèces, y compris leurs interactions biotiques, permettent de comprendre les variations de leur distribution spatiale et de leur niche environnementale. Ainsi, l’établissement récent d’A. levana dans le sud de la Suède, suite au réchauffement, a modifié les niches des espèces résidentes, A. urticae et A. io (article IV).

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2015. 39 p.
National Category
Zoology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-119719 (URN)978-91-7649-202-4 (ISBN)
Public defence
2015-10-02, De Geersalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 10:00 (English)
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Supervisors
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Ekoklim
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: Manuscript. Paper 4: Manuscript.

Available from: 2015-09-10 Created: 2015-08-23 Last updated: 2017-03-16Bibliographically approved

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