Abstract
Island biotas provide a great opportunity to study not only the phylogeographic patterns of a group of species, but also to explore the differentiation in their coevolutionary interactions. Drosophila and their parasitoids are exemplary systems for studying complex interaction patterns. However, there is a lack of studies combining interaction-based and molecular marker-based methods. We applied an integrated approach combining phylogeography, interaction, and host-choice behavior studies, with the aim to understand how coevolutionary interactions evolve in Drosophila-parasitoid island populations. The study focused on the three most abundant Drosophila species in Ryukyu archipelago and Taiwan: D. albomicans, D. bipectinata, and D. takahashii, and the Drosophila-parasitoid Leptopilina ryukyuensis. We determined mitochondrial COI haplotypes for samples representing five island populations of Drosophila and four island populations of L. ryukyuensis. We additionally sequenced parts of the autosomal Gpdh for Drosophila samples, and the ITS2 for parasitoid samples. Phylogenetic and coalescent analyses were used to test for demographic events and to place them in a temporal framework. Geographical differences in Drosophila-parasitoid interactions were studied in host-acceptance, host-suitability, and host-choice experiments. All four species showed species-specific phylogeographic patterns. A general trend of the haplotype diversity increasing towards the south was observed. D. albomicans showed very high COI haplotype diversity, and had the most phylogeographically structured populations, with differentiation into the northern and the southern population-group, divided by the Kerama gap. Differentiation in host suitability was observed only between highly structured populations of D. albomicans, possibly facilitated by restricted gene flow. Differentiation in host-acceptance in D. takahashii, and host-acceptance and host-choice in L. ryukyuensis was found, despite there being no differentiation in these two species according to molecular markers. Host choice assays show that L. ryukyuensis populations that have had more time to coevolve adapt their behavior to exploit the most suitable host – D. albomicans. L. ryukyuensis parasitoids on border ranges may, on the other hand, benefit from broader host-acceptance, that may facilitate adaptation to uncertain and variable environments. All results indicate that Drosophila-parasitoid populations in the Ryukyu archipelago and Taiwan have different evolutionary trajectories, and coevolve in a dynamic, complex, and local-specific way.
Highlights
In evolutionary and ecological studies attention is increasingly shifting to interspecific interactions and coevolutionary systems
Using samples from five island populations of flies, four island populations of the parasitoid, and three laboratory strains for each study species we conducted the following analyses: (1) We used mitochondrial COI partial sequences, and the partial sequences of the autosomal glycerol-3-phosphate dehydrogenase (Gpdh) for flies, and ITS2 for wasps, to explore the phylogeography of the four insect species and determine to what extent the phylogeography of the three Drosophila and the parasitoid L. ryukyuensis in this area are shaped by barriers to gene flow, and/or coevolutionary interactions; (2) we tested for differentiation in host-parasitoid interactions by host-acceptance and host-suitability experiments in laboratory; (3) we explored the host choice of L. ryukyuensis in a two-choice assay, designed based on the outcomes of host-acceptance and hostsuitability experiments
COI showed more diversity than Gpdh in D. takahashii and D. albomicans, while Gpdh/ITS2 was more diverse compared to COI in D. bipectinata and L. ryukyuensis
Summary
In evolutionary and ecological studies attention is increasingly shifting to interspecific interactions and coevolutionary systems. Host-parasitoid interaction studies have focused on comparative phylogeography [4,5,6,7], or more often interaction traits [8,9,10], but these approaches have rarely been combined [11]. No comparative phylogeographic studies of Drosophila and their parasitoids have been conducted so far. We use an integrated approach, studying phylogeography, interaction, and host choice behavior in Drosophila-parasitoid systems, with an aim to deepen the understanding of how these interactions evolve in more or less isolated populations
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