Potential Host Manipulation by the Aphid Parasitoid Aphidius avenae to Enhance Cold Tolerance

RESEARCH ARTICLE Potential Host Manipulation by the Aphid Parasitoid Aphidius avenae to Enhance Cold Tolerance Lucy Alford¤*, Annabelle Androdias, Thomas Franco, Jean-Sébastien Pierre, Françoise Burel, Joan van Baaren UMR 6553 ECOBIO, Université de Rennes I, Avenue du Général Leclerc, Rennes Cedex, France ¤ Current address: Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Davidson Building, Glasgow, United Kingdom * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Alford L, Androdias A, Franco T, Pierre JS, Burel F, van Baaren J (2016) Potential Host Manipulation by the Aphid Parasitoid Aphidius avenae to Enhance Cold Tolerance. PLoS ONE 11 (12): e0168693. doi:10.1371/journal. pone.0168693 Editor: Owain Rhys Edwards, CSIRO, AUSTRALIA Received: April 25, 2016 Accepted: December 4, 2016 Abstract During parasitoid development, the immature parasitoid is confined to the host species. As a result, any potential to modify the physiology or behaviour of the host could play an important role in parasitoid fitness. The potential for host manipulation by the aphid parasitoid Aphidius avenae to increase cold thermotolerance was investigated using the aphid host species Metopolophium dirhodum and Sitobion avenae. Aphids were parasitized at L3/L4 instar stage (5 d old) and allowed to develop into pre-reproductive adults (10 d old) containing a 5 d old parasitoid larva. A control group was created of non-parasitized pre-reproductive adults (10 d old). The inherent physiological thermotolerance (LT50) and potential behavioural thermoregulation (behaviour in a declining temperature regime) of parasitized and non-parasitized aphids were investigated. Results revealed no effect of parasitism on the physiological thermotolerance of S. avenae and M. dirhodum. Significant differences in the behaviour of parasitized and non-parasitized aphids were observed, in addition to differences between host species, and such behaviours are discussed in view of the potential for host manipulation. Published: December 22, 2016 Copyright: © 2016 Alford et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper. Funding: This work was funded by a Marie Curie Intra-European Fellowship for the project ‘Climland’ (FP7-PEOPLE-2012-IEF-326943) awarded to L Alford, F Burel and J van Baaren. Competing Interests: The authors have declared that no competing interests exist. Introduction When subjected to unfavourable thermal conditions, an organism’s survival is governed by its inherent physiological thermotolerance. For ectothermic organisms, although comparatively limited in their ability to internally thermoregulate, the inherent physiological thermotolerance that they do possess is conferred via a variety of biochemical and physiological mechanisms [1, 2]. In addition to inherent physiological thermotolerance, organisms may employ behavioural mechanisms as a form of thermoregulation, such as habitat selection across large spatial scales, involving extensive seasonal migrations to suitable overwintering sites [3], or microhabitat selection such as basking or burying [4, 5]. Whilst the role of physiological thermotolerance and behavioural thermoregulation of ectotherms is well studied, parasitic organisms and parasitoids pose an interesting scenario due to PLOS ONE | DOI:10.1371/journal.pone.0168693 December 22, 2016 1 / 14 Potential Host Manipulation by an Aphid Parasitoid to Enhance Cold Tolerance their dependence upon a host species to complete their lifecycle. Parasitoid insects, for example, which are largely dominated by the order Hymenoptera [6], lay their eggs on or within a host species and are consequently intricately linked to their host during the immature instar stage [7]. Their ability to utilise behavioural thermoregulation during immature development is subsequently severely reduced. Furthermore, should the host die prior to parasitoid pupation, so too will the developing parasitoid. As a consequence, any potential to modify the behaviour or physiology of the host could play an important role in parasite and parasitoid fitness [8]. Changes in physiology or behaviour following parasitization by a parasitoid wasp (or infection by a parasite more generally) may evolve if the change results in greater fitness, either to the parasite or to the host [9, 10]. Indeed, the majority of documented changes to parasitized animals are behaviours, considered parasite adaptations, acting to enhance transmission success [9]. Host adaptations are also plausible whereby changes may enhance host fitness, for example by aiding parasite removal or compensating against the effects of parasitization [9, 11]. However, to be truly considered an adaptive manipulation and not simply a pathological by-product of infection, the change must result in an increase in fitness for either the parasite or the host; a variable that is often difficult to measure [9]. Within the context of parasitoid wasps, documented changes to the host following parasitization fall into the category of parasite adaptations, with enhanced parasitoid fitness commonly attributed to behavioural changes induced in the host which bring about a reduction in the rate of predation and hyperparasitism [12–14], However, whilst host manipulation by parasitoids is well documented, the potential for host manipulation to enhance thermotolerance is a topic that has received considerably little research attention. There is evidence to suggest that a parasitoid may alter both the physiology and the behaviour of the host to withstand or avoid unfavourable thermal conditions, although both mechanisms have been studied in isolation. Physiological changes to the host following parasitization within the context of thermal tolerance have received little research attention [15, 16] and have not been studied for the aphid parasitoids. However, comparison of two separate studies suggests that physiological modification acting to aid thermotolerance may occur in the Russian wheat aphid, Diuraphis noxia, when parasitized by Aphelinus albipodus, Aphelinus asychis and Diaeretiella rapae. Here, nonparasitized D. noxia possessed a supercooling point of -25˚C [17]. However, the supercooling point is lowered to -30˚ and below when parasitized [18], suggesting that parasitism may enhance the cold tolerance of the host via physiological changes. Since the parasitoid is intricately linked to its aphid host, premature death of the aphid (i.e. prior to parasitoid pupation) will result in the death of the parasitoid also. Therefore, any ability to enhance the thermotolerance of the aphid host, thus enhancing aphid surviv (...truncated)