Widespread plant specialization in the polyphagous planthopper Hyalesthes obsoletus (Cixiidae), a major vector of stolbur phytoplasma: Evidence of cryptic speciation.

Milana Mitrović,Wolfgang Arthofer,Andrea Kosovac,Ivo Toševski,Jes Johannesen,Jelena Jović,Oliver Krstić,Tatjana Cvrković

doi:10.1371/journal.pone.0196969

Milana Mitrović, Wolfgang Arthofer + Show 6 more

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https://doi.org/10.1371/journal.pone.0196969

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Abstract

The stolbur phytoplasma vector Hyalesthes obsoletus is generally considered as a polyphagous species associated with numerous wild and cultivated plants. However, recent research in southeastern Europe, the distribution centre of H. obsoletus and the area of most stolbur-inflicted crop diseases, points toward specific host-plant associations of the vector, indicating specific vector-based transmission routes. Here, we study the specificity of populations associated with four host-plants using mitochondrial and nuclear genetic markers, and we evaluate the evolution of host-shifts in H. obsoletus. Host-plant use was confirmed for Convolvulus arvensis, Urtica dioica, Vitex agnus-castus and Crepis foetida. Mitochondrial genetic analysis showed sympatric occurrence of three phylogenetic lineages that were ecologically delineated by host-plant preference, but were morphologically inseparable. Nuclear data supported the existence of three genetic groups (Evanno’s ΔK(3) = 803.72) with average genetic membership probabilities > 90%. While populations associated with C. arvensis and U. dioica form a homogenous group, populations affiliated with V. agnus-castus and C. foetida constitute two independent plant-associated lineages. The geographical signal permeating the surveyed populations indicated complex diversification processes associated with host-plant selection and likely derived from post-glacial refugia in the eastern Mediterranean. This study provides evidence for cryptic species diversification within H. obsoletus sensu lato: i) consistent mitochondrial differentiation (1.1–1.5%) among host-associated populations in syntopy and in geographically distant areas, ii) nuclear genetic variance supporting mitochondrial data, and iii) average mitochondrial genetic distances among host-associated meta-populations are comparable to the most closely related, morphologically distinguishable species, i.e., Hyalesthes thracicus (2.1–3.3%).

Highlights

Knowledge of changes in insect genetic structure and the possibility of cryptic divergence are important for pest populations because management strategies must be adapted to the ecological diversity of the pest [1,2,3,4,5,6]
Target host-plants were searched for associated H. obsoletus populations across the surveyed area (Fig 1) to obtain information on the geographic range of each insect-host association, distribution overlap, population structure and genetic differentiation in syntopy
Surveys indicated that H. obsoletus populations in southeastern Europe are i) high density and Widespread plant specialization in Hyalesthes obsoletus: Evidence of cryptic speciation very common in association with Urtica dioica (Ud); ii) rare and low density in association with Convolvulus arvensis (Ca); iii) usually very common and in high density in association with Vitex agnus-castus (Vac), it is restricted to the coastal distribution of the host-plant; and iv) high in number and very common in association with Crepis foetida (Cf) in the eastern parts of the surveyed area but absent in the south (Fig 1)

Summary

Introduction

Knowledge of changes in insect genetic structure and the possibility of cryptic divergence are important for pest populations because management strategies must be adapted to the ecological diversity of the pest [1,2,3,4,5,6]. If host-plant preferences change and cause alterations in the vector’s feeding behavior (e.g. mono-, oligo- or polyphagous), such changes may initiate host-plant specialization and drive populations through successive stages of ambiguous, taxonomically indistinguishable but ecologically adapted populations. Such populations known as "host races", "ecological races" or "biotypes" lead toward true species status [16,17,18]. Of primary importance for elucidating the distribution, dispersal, impact and epidemiology of vector-transmitted plant diseases is knowledge of the evolutionary relationship between the vector and its hostplant(s). This is reflected through levels of host-plant association(s) and the extent of genetic segregation, i.e., specialization of the species in question

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