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Evolution of host repertoires and the diversification of butterflies
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-1253-2536
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

All herbivorous insects are specialized to some extent to their host plants, but the level of specialization varies greatly. Insect-plant coevolution is often invoked to explain the large diversity of herbivorous insects, but the role of specialization during diversification is still controversial. Although well-studied, our understanding of the evolution of species interactions is still improving, and recent theoretical developments have highlighted the role of generalization (via colonization of new hosts) on diversification. In this thesis, various approaches are combined for a detailed study of the origins of macroevolutionary patterns of host use and butterfly diversity. Chapter I provides a mechanistic basis for such patterns through simulations of lineages evolved in silico. By separating the effects of the number of hosts used by a parasite lineage and the diversity of resources they encompass, we found that resource diversity, rather than host range per se, was the main driver of parasite species richness in both simulated and empirical systems. In Chapter II, we combined network and phylogenetic analyses to quantify support for the two main hypothesized drivers of diversification of herbivorous insects. Based on analyses of two butterfly families, Nymphalidae and Pieridae, we found that variability in host use is essential for diversification, while radiation following the colonization of a new host is rare but can produce high diversity. We then reconciled the two alternative hypotheses into a unified process of host-associated diversification where continuous probing of new hosts and retention of the ability to use hosts colonized in the past are the main factors shaping butterfly-plant networks. While network analysis is a powerful tool for investigating patterns of interaction, other methods are necessary to directly test the mechanisms generating the observed patterns. Therefore, in Chapter III we describe a model of host repertoire evolution we developed for Bayesian inference of evolution of host-parasite interactions. The approach was validated with both simulated and empirical data sets. Finally, in Chapter IV we used the method described in Chapter III to explicitly test the predictions made in Chapter II about the evolution of butterfly-plant networks. We found direct evidence for the role of expansion of fundamental host repertoire and phylogenetic conservatism as important drivers of host repertoire evolution. Thus, using three different approaches, we found overall support for the idea that variation in host use accumulated over evolutionary time is essential for butterfly diversification.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2019. , p. 27
Keywords [en]
coevolution, host-parasite interaction, inference, networks
National Category
Ecology Evolutionary Biology
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-163179ISBN: 978-91-7797-568-7 (print)ISBN: 978-91-7797-569-4 (electronic)OAI: oai:DiVA.org:su-163179DiVA, id: diva2:1271841
Public defence
2019-02-15, 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 papers were unpublished and had a status as follows: Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2019-01-23 Created: 2018-12-18 Last updated: 2019-01-15Bibliographically approved
List of papers
1. Host use dynamics in a heterogeneous fitness landscape generates oscillations in host range and diversification
Open this publication in new window or tab >>Host use dynamics in a heterogeneous fitness landscape generates oscillations in host range and diversification
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2018 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, no 9, p. 1773-1783Article in journal (Refereed) Published
Abstract [en]

Colonization of novel hosts is thought to play an important role in parasite diversification, yet little consensus has been achieved about the macroevolutionary consequences of changes in host use. Here, we offer a mechanistic basis for the origins of parasite diversity by simulating lineages evolved in silico. We describe an individual-based model in which (i) parasites undergo sexual reproduction limited by genetic proximity, (ii) hosts are uniformly distributed along a one-dimensional resource gradient, and (iii) host use is determined by the interaction between the phenotype of the parasite and a heterogeneous fitness landscape. We found two main effects of host use on the evolution of a parasite lineage. First, the colonization of a novel host allowed parasites to explore new areas of the resource space, increasing phenotypic and genotypic variation. Second, hosts produced heterogeneity in the parasite fitness landscape, which led to reproductive isolation and therefore, speciation. As a validation of the model, we analyzed empirical data from Nymphalidae butterflies and their host plants. We then assessed the number of hosts used by parasite lineages and the diversity of resources they encompass. In both simulated and empirical systems, host diversity emerged as the main predictor of parasite species richness.

Keywords
Host range, individual-based model, parasite diversity, phenotypic amplitude
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-161117 (URN)10.1111/evo.13557 (DOI)000444946400003 ()30019746 (PubMedID)
Available from: 2018-10-29 Created: 2018-10-29 Last updated: 2019-03-01Bibliographically approved
2. Unifying host-associated diversification processes using butterfly-plant networks
Open this publication in new window or tab >>Unifying host-associated diversification processes using butterfly-plant networks
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2018 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 5155Article in journal (Refereed) Published
Abstract [en]

Explaining the exceptional diversity of herbivorous insects is an old problem in evolutionary ecology. Here we focus on the two prominent hypothesised drivers of their diversification, radiations after major host switch or variability in host use due to continuous probing of new hosts. Unfortunately, current methods cannot distinguish between these hypotheses, causing controversy in the literature. Here we present an approach combining network and phylogenetic analyses, which directly quantifies support for these opposing hypotheses. After demonstrating that each hypothesis produces divergent network structures, we then investigate the contribution of each to diversification in two butterfly families: Pieridae and Nymphalidae. Overall, we find that variability in host use is essential for butterfly diversification, while radiations following colonisation of a new host are rare but can produce high diversity. Beyond providing an important reconciliation of alternative hypotheses for butterfly diversification, our approach has potential to test many other hypotheses in evolutionary biology.

National Category
Ecology Evolutionary Biology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-163178 (URN)10.1038/s41467-018-07677-x (DOI)000452042500006 ()
Available from: 2018-12-18 Created: 2018-12-18 Last updated: 2019-03-01Bibliographically approved
3. Bayesian analysis of host repertoire evolution
Open this publication in new window or tab >>Bayesian analysis of host repertoire evolution
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(English)Manuscript (preprint) (Other academic)
National Category
Ecology Evolutionary Biology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-163176 (URN)
Available from: 2018-12-18 Created: 2018-12-18 Last updated: 2019-03-01Bibliographically approved
4. Evolution of butterfly-plant networks revealed by Bayesian inference of host repertoire
Open this publication in new window or tab >>Evolution of butterfly-plant networks revealed by Bayesian inference of host repertoire
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(English)Manuscript (preprint) (Other academic)
National Category
Ecology Evolutionary Biology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-163177 (URN)
Available from: 2018-12-18 Created: 2018-12-18 Last updated: 2019-03-01Bibliographically approved

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