Phylogeography, Interaction Patterns and the Evolution of Host Choice in Drosophila-Parasitoid Systems in Ryukyu Archipelago and Taiwan

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.

Semi-natural habitats boost Drosophila suzukii populations and crop damage in sweet cherry

“…Although at the moment the presence of forest habitats appears to be a greater source of pest than of natural enemies, one should consider the potential of semi-natural habitats to provide biocontrol in the future by providing suitable conditions for the populations of both native natural enemies and potential released biocontrol agents. Shifts of native natural enemies to a new invasive pest are common but they usually occur in the long-term (Novković and Kimura, 2015) and, therefore, cannot be expected to regulate the exotic species population at the beginning of its spread. Considering the emerging problems linked to the invasion of exotic generalist pests across several temperate countries across Europe and North America, our study emphasizes the need to explore the potential effects of landscape processes on the spatio-temporal dynamics of pest populations.…”

The widespread misconception about the Japanese major biogeographic boundary, the Watase line (Tokara gap), revealed by bibliographic and beta diversity analyses

“…In most such studies, this biogeographic or phylogeographic boundary is usually placed between two islands of the Tokara Archipelago, Akusekijima (Akuseki) and Kodakarajima (Kodakara) Islands (gap 5 in Fig. 1) [10,19,20]. It is plausibly explained that migrations of terrestrial and freshwater organisms over the strait have been limited since the Pliocene throughout glacial cycling because of the deep submarine canyon 1000 m below sea level between the two islands [16,20-24] that resulted in the boundary line between the Palearctic and Oriental realms.…”

Drosophilaparasitoids (Hymenoptera) ofJapan

“…2007; Mitsui & Kimura 2010; Kimura & Suwito 2014; Takigahira et al . 2014, 2015; Kimura & Novković 2015; Novković & Kimura 2015). This suggests that host–parasitoid association has evolved through their local coevolutionary interactions (i.e.…”

“…Most parasitoids are generalists; they use a number of drosophilid species as host (Mitsui et al 2007;Mitsui & Kimura 2010;Novkovi c et al 2012;Kasuya et al 2013a;Kimura & Novkovi c 2015). Exceptions are G. brasiliensis-G1 and A. triangulata, which have been recorded only from D. suzukii, a pest of soft fruit at least in Tokyo (Kasuya et al 2013b;Nomano et al 2017;Matsuura et al 2018).…”

“…The host range of these generalist parasitoids is, to some extent, affected by host taxonomy (Kimura & Suwito 2014; Kimura & Novkovi c 2015), probably because closely related host species share common features that determine their suitability as host. However, sibling or closely related drosophilid species or different geographic populations of the same species sometimes differ in resistance to parasitoids (Carton et al 1986;Eslin & Prévost 1998;Fleury et al 2004Fleury et al , 2009Dubuffet et al 2007;Mitsui & Kimura 2010;Kimura & Suwito 2014;Takigahira et al 2014Takigahira et al , 2015Kimura & Novkovi c 2015;Novkovi c & Kimura 2015). This suggests that host-parasitoid association has evolved through their local coevolutionary interactions (i.e.…”