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Host use dynamics in a heterogeneous fitness landscape generates oscillations in host range and diversification
Stockholm University, Faculty of Science, Department of Zoology.
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Number of Authors: 82018 (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.

Place, publisher, year, edition, pages
2018. Vol. 72, no 9, p. 1773-1783
Keywords [en]
Host range, individual-based model, parasite diversity, phenotypic amplitude
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-161117DOI: 10.1111/evo.13557ISI: 000444946400003PubMedID: 30019746OAI: oai:DiVA.org:su-161117DiVA, id: diva2:1259397
Available from: 2018-10-29 Created: 2018-10-29 Last updated: 2019-03-01Bibliographically approved
In thesis
1. Evolution of host repertoires and the diversification of butterflies
Open this publication in new window or tab >>Evolution of host repertoires and the diversification of butterflies
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
coevolution, host-parasite interaction, inference, networks
National Category
Ecology Evolutionary Biology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-163179 (URN)978-91-7797-568-7 (ISBN)978-91-7797-569-4 (ISBN)
Public defence
2019-02-15, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
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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

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