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Multilocus Phylogeny and Ecological Differentiation of the “Eupelmus Urozonus Species Group” (Hymenoptera, Eupelmidae) in the West-Palaearctic F

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Multilocus Phylogeny and Ecological Differentiation of the “Eupelmus Urozonus Species Group” (Hymenoptera, Eupelmidae) in the West-Palaearctic F Al khatib et al. BMC Evolutionary Biology (2016) 16:13 DOI 10.1186/s12862-015-0571-2 RESEARCH ARTICLE Open Access Multilocus phylogeny and ecological differentiation of the “Eupelmus urozonus species group” (Hymenoptera, Eupelmidae) in the West-Palaearctic F. Al khatib1,3*, A. Cruaud2, L. Fusu4, G. Genson2, J.-Y. Rasplus2, N. Ris1 and G. Delvare3 Abstract Background: The ecological differentiation of insects with parasitic life-style is a complex process that may involve phylogenetic constraints as well as morphological and/or behavioural adaptations. In most cases, the relative importance of these driving forces remains unexplored. We investigate here this question for the “Eupelmus urozonus species group” which encompasses parasitoid wasps of potential interest in biological control. This was achieved using seven molecular markers, reliable records on 91 host species and a proxy of the ovipositor length. Results: After using an adequate partitioning scheme, Maximum likelihood and Bayesian approaches provide a well-resolved phylogeny supporting the monophyly of this species group and highlighting its subdivision into three sub-groups. Great variations of both the ovipositor length and the host range (specialist versus generalist) were observed at this scale, with these two features being not significantly constrained by the phylogeny. Ovipositor length was not shown as a significant predictor of the parasitoid host range. Conclusions: This study provides firstly the first evidence for the strong lability of both the ovipositor’slength and the realised host range in a set of phylogenetically related and sympatric species. In both cases, strong contrasts were observed between sister species. Moreover, no significant correlation was found between these two features. Alternative drivers of the ecological differentiation such as interspecific interactions are proposed and the consequences on the recruitment of these parasitoids on native and exotic pests are discussed. Keywords: Ecological specialization, Ectoparasitoid, Host range evolution, Molecular phylogeny, Morphological adaptation, Ovipositor, Phylogenetic constraint Background mechanism linking divergent selection to reproductive Ecological speciation is a process in which polymorph- isolation. Among plant-feeding insects, several empirical ism within populations (e.g. in resource use or habitat studies support this scenario [1, 5, 6], which can also preference) ultimately induces the appearance of two occur for insects with a parasitic lifestyle, in particular sister species, each adapted to a different niche [1–4]. within the upper trophic levels. For such organisms, eco- According to Rundle and Nosil [2], three principal com- logical differentiation between sister species can also be ponents must be involved: i) a source of divergent selec- driven by the ecological differentiation of their hosts via a tion, ii) a form of reproductive isolation, and iii) a genetic process called sequential or cascading speciation [7–9]. If pervasive enough, such processes should lead to the clus- * Correspondence: [email protected] tering of phylogenetically related specialists. 1INRA, University of Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Additionally, transitions between generalists to spe- Sophia Agrobiotech, Sophia Antipolis 06900, France cialists (and vice-versa) are also occurring and, so far, 3CIRAD, UMR 55 CBGP, 755 Avenue du Campus Agropolis, CS 30016 F-34988, Montferrier-sur-Lez Cedex, France empirical data provide a mixed picture about the Full list of author information is available at the end of the article © 2016 Al khatib et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Al khatib et al. BMC Evolutionary Biology (2016) 16:13 Page 2 of 20 relative frequencies of evolution toward specialisation the “E. urozonus species complex/group” which was re- and generalization [10–13]. However, transitions from peatedly investigated [27, 29–31] until its recent revision generalist ancestors to specialized species are probably within the Palaearctic region by Al khatib et al. [32, 33], recurrent as (i) generalist species are unlikely to pro- which identified 11 new species in this region. Semantic- duce “jack-of-all trades-master of none” genotypes be- ally, the term “complex” used in Al khatib et al. [32, 33] is cause of genetic or physiological trade-off [14–16]; (ii) substituted here by the term “species group” (Al khatib et the subsequent acquisition of specialized genotypes al. in preparation). As a consequence of this unsuspected may be a primary step towards speciation [17–19]; biodiversity, most of the published host records for these and (iii) specialist species may be more prone to ex- species are unreliable because all of the common species tinction [13, 20]. At a phylogenetic level, both kinds with a comparatively short ovipositor (E. gemellus Al kha- of transitions should lead to the mixing of both spe- tib, 2015, E. confusus Al khatib, 2015, and especially E. cialists and generalists within the same cluster. kiefferi De Stefani, 1898) were misidentified as E. urozonus Questions of (i) the host range (specialist versus gener- Dalman, 1820, while the two common species with a com- alist) of ancestral species of current specialists and (ii) paratively long ovipositor (E. azureus Ratzeburg, 1844 and the distribution of host ranges within a phylogeny were E. annulatus Nees, 1834) were both frequently mistreated recently addressed by Hardy and Otto [21]. They illus- under E. annulatus [29, 34]. trated them using two notions, respectively “the musical Inthepresentstudy,wefirstprovideareliablemo- chairs hypothesis” (specialists originate from specialists lecular phylogeny of the “E. urozonus species group” through host switch) and the “oscillation hypothesis” using a multi-locus approach. Then, for most of the (specialists originate from generalists, with some special- species, we compile host records and data on oviposi- ists widening their host range before the next speciation tor length. We finally carry out a comparative analysis event). The extent to which one of these scenarios is to evaluate the role of phylogenetic constraints in the more frequent has nevertheless still to be evaluated evolution of ovipositor length and host range as well rigorously for the organisms with a parasitic lifestyle. as the role of the ovipositor’s length in determining Parasitoids are organisms (mainly Hymenoptera and the host range. Diptera) whose pre-imaginal life depends on the success- ful exploitation of a single host [22, 23]. Behind this sim- Methods ple definition, a great diversity of life history strategies Sampling and physiological adaptations are observed. In particular, A total of 31 species, with 91 individuals, sampled in the the ovipositor allows egg-laying by the female and is Palaearctic region were included in this study. thus a key organ especially for species that are exploiting concealed or protected hosts [24, 25]. The features (in – Eighteen of the 21 species within the “urozonus particular the length) of this organ and its ability to species group” that were recently revised using both evolve could contribute to drive specialization and/or morphological and molecular characters [32, 33]: E. speciation. Focusing on the “Eupelmus urozonus species acinellus Askew, 2009, E. annulatus, E. azureus, E. group” (Hymenoptera: Eupelmidae), we examine here cerris Förster, 1860, E. confusus, E. fulvipes Förster, whether the host range is subject to phylogenetic con- 1860, E. gemellus, E. janstai Delvare and Gibson, straints and/or whether the ovipositor length is a signifi- 2015, E. kiefferi, E. longicalvus Al khatib & Fusu, cant driver of host use. 2015, E. minozonus Delvare, 2015, E. opacus Within the subfamily Eupelminae (33 genera), the Delvare, 2015, E. pistaciae Al khatib, 2015, E. genus Eupelmus Dalman is the most diverse, with 91 priotoni Delvare, 2015, E. purpuricollis Fusu & Al available valid species names in the Palaearctic region khatib, 2015, E. simizonus Al khatib, 2015, E. [26]. Species of Eupelmus are primary or facultative sec- tibicinis Bouček, 1963 and E. urozonus. ondary ectoparasitoids whose larvae develop as idio- – Thirteen species were used as outgroup including (i) bionts on the immature stages (larvae, pupae and more species belonging to the three subgenera of rarely eggs) of many insects (beetles, flies, moths, wasps Eupelmus sensu Gibson (1995): Eupelmus [E. or cicadas) that are concealed or protected in plant tis- atropurpureus Dalman, 1820, E. matranus Erdős, sues (stems, galls, fruits or seeds) [27]. Most Eupelmus 1947, E. microzonus Förster, 1860, E. pini Taylor, are considered as generalist parasitoids [27, 28]. How- 1927 and E. vindex Erdős, 1955]; Macroneura ever, because of both the extreme sexual dimorphism Walker [E. falcatus (Nikol’skaya, 1952) and E. characterizing the subfamily and the existence of species seculatus Kalina, 1981], and Episolindelia Girault groups possibly hiding
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