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Hymenoptera; Argidae) Edinburgh Research Explorer Tracking of host defenses and phylogeny during the radiation of neotropical Inga-feeding sawflies (Hymenoptera; Argidae) Citation for published version: Endara, M-J, Nicholls, J, Coley, PD, Forrister, DL, Younkin, GC, Dexter, K, Kidner, C, Pennington, RT, Stone, G & Kursar, TA 2018, 'Tracking of host defenses and phylogeny during the radiation of neotropical Inga-feeding sawflies (Hymenoptera; Argidae)' Frontiers in plant science, vol. 9, 2137. DOI: 10.3389/fpls.2018.01237 Digital Object Identifier (DOI): 10.3389/fpls.2018.01237 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: Frontiers in plant science Publisher Rights Statement: Copyright © 2018 Endara, Nicholls, Coley, Forrister, Younkin, Dexter, Kidner, Pennington, Stone and Kursar. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 05. Apr. 2019 fpls-09-01237 August 22, 2018 Time: 9:41 # 1 ORIGINAL RESEARCH published: 23 August 2018 doi: 10.3389/fpls.2018.01237 Tracking of Host Defenses and Phylogeny During the Radiation of Neotropical Inga-Feeding Sawflies (Hymenoptera; Argidae) María-José Endara1,2*†, James A. Nicholls3†, Phyllis D. Coley1,4, Dale L. Forrister1, Gordon C. Younkin1, Kyle G. Dexter5,6, Catherine A. Kidner3,5, R. T. Pennington5, Graham N. Stone3‡ and Thomas A. Kursar1,4‡ 1 Department of Biology, The University of Utah, Salt Lake City, UT, United States, 2 Centro de Investigación de la Biodiversidad y Cambio Climático (BioCamb) e Ingeniería en Biodiversidad y Recursos Genéticos, Facultad de Ciencias de Medio Ambiente, Universidad Tecnológica Indoamérica, Quito, Ecuador, 3 Ashworth Laboratories, Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh, United Kingdom, 4 Smithsonian Tropical Research Institute, Panama City, Panama, 5 Royal Botanic Garden Edinburgh, Edinburgh, United Kingdom, 6 School of GeoSciences, The University of Edinburgh, Edinburgh, United Kingdom Coevolutionary theory has long predicted that the arms race between plants and Edited by: herbivores is a major driver of host selection and diversification. At a local scale, plant Tara Joy Massad, defenses contribute significantly to the structure of herbivore assemblages and the high Rhodes College, United States alpha diversity of plants in tropical rain forests. However, the general importance of plant Reviewed by: defenses in host associations and divergence at regional scales remains unclear. Here, Tobias Zuest, Universität Bern, Switzerland we examine the role of plant defensive traits and phylogeny in the evolution of host Brian Traw, range and species divergence in leaf-feeding sawflies of the family Argidae associated Berea College, United States with Neotropical trees in the genus Inga throughout the Amazon, the Guiana Shield and *Correspondence: María-José Endara Panama. Our analyses show that the phylogenies of both the sawfly herbivores and their [email protected] Inga hosts are congruent, and that sawflies radiated at approximately the same time, or †These authors share first authorship more recently than their Inga hosts. Analyses controlling for phylogenetic effects show ‡ These authors share senior that the evolution of host use in the sawflies associated with Inga is better correlated authorship with Inga chemistry than with Inga phylogeny, suggesting a pattern of delayed host Specialty section: tracking closely tied to host chemistry. Finally, phylogenetic analyses show that sister This article was submitted to species of Inga-sawflies are dispersed across the Neotropics, suggesting a role for Plant Metabolism and Chemodiversity, allopatric divergence and vicariance in Inga diversification. These results are consistent a section of the journal with the idea that host defensive traits play a key role not only in structuring the herbivore Frontiers in Plant Science assemblages at a single site, but also in the processes shaping host association and Received: 25 April 2018 Accepted: 06 August 2018 species divergence at a regional scale. Published: 23 August 2018 Keywords: coevolution, defense traits, herbivores, host tracking, Inga, plant–insect interactions, sawflies, tropical Citation: rain forests Endara M-J, Nicholls JA, Coley PD, Forrister DL, Younkin GC, Dexter KG, Kidner CA, Pennington RT, Stone GN INTRODUCTION and Kursar TA (2018) Tracking of Host Defenses and Phylogeny During Insect herbivores and their plant hosts dominate terrestrial biodiversity (Hunt et al., 2007), and the Radiation of Neotropical Inga-Feeding Sawflies (Hymenoptera; the processes that drive their interaction and diversification remain an enduring focus of research Argidae). Front. Plant Sci. 9:1237. in ecology and evolution (Futuyma and Agrawal, 2009; Janz, 2011; Hembry et al., 2014; Forbes doi: 10.3389/fpls.2018.01237 et al., 2017; Nakadai, 2017). This is especially true in the tropics where most of the species occur. Frontiers in Plant Science| www.frontiersin.org 1 August 2018| Volume 9| Article 1237 fpls-09-01237 August 22, 2018 Time: 9:41 # 2 Endara et al. Herbivores Track Defenses During Diversification A central paradigm is that insect-plant associations have been the same Inga traits structure herbivore associations in widely shaped by arms race coevolution between plant defenses and separated communities. Previous analyses have also found little insect countermeasures (Becerra, 1997; Becerra et al., 2009; Volf phylogenetic pattern in Inga defenses (Kursar et al., 2009; et al., 2018). Ehrlich and Raven(1964) observed that closely Endara et al., 2015, 2017), and related lepidopteran herbivores related plants are often attacked by closely related herbivores, a attack Ingas with similar defenses, rather than those that are pattern they attributed to an ‘escape and radiate’ model, in which closely related (Endara et al., 2017). Our hypothesis is that plant lineages diversify following evolutionary innovation of a herbivores have driven rapid diversification of defensive traits key defense trait, and specialist herbivore lineages diversify across in Inga, with herbivore associations resulting from evolutionary the plant radiation through evolution of a key countermeasure tracking of similar defensive phenotypes (i.e., host-resource (Wheat et al., 2007). Where these traits are phylogenetically tracking) rather than cospeciation (Coley et al., 2018). Here we conserved in each lineage, we expect some degree of phylogenetic test this hypothesis using data for four regional communities concordance between plant and herbivore lineages, resulting that span the Amazon Basin, in Panama, Peru, Ecuador, and either from simultaneous co-diversification (Cruaud et al., 2012), French Guiana. We focus on sawflies (Hymenoptera; Symphyta) or delayed herbivore colonization of an existing plant radiation in the superfamily Tenthredinoidea, shown in previous work (tracking of host resources; Janz, 2011). Thus, plant defenses in other regions of the world to be highly sensitive to (and play a prominent role in the evolution of host associations often dependent on) toxic host plant chemistry (Petre et al., (Thompson, 1988), yet they are often not considered in studies of 2007; Boevé et al., 2013; Naya et al., 2016). Thus, they are plant-herbivore diversification. Robust analyses require not only an excellent candidate taxon in which to explore the impact phylogenetic histories of both plants and herbivores, but also data of diversification in this key aspect of Inga defenses. We use on ecologically important traits such as plant defenses. novel data on Inga-sawfly associations and an analytical approach Although insect herbivores are expected to show evolutionary incorporating phylogenies for both lineages (Hadfield et al., 2014) conservatism in host use (Ehrlich and Raven, 1964; Brooks and defense trait data to address the following questions: (i) Is and McLennan, 2002), many studies show herbivore shifts there phylogenetic patterning in Inga defenses? (ii) Does Inga between distantly related hosts that disrupt any signature of phylogeny (cospeciation) or defenses (resource tracking) best codiversification. Some shifts are between hosts with similar predict Inga-sawfly associations? (iii) Over what geographic scale chemical defenses for which herbivore countermeasures are have Inga-sawfly associations evolved? Are sister sawfly or Inga to some extent preadapted, implying a process of host- species commonly
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