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      The Biochemical Toxin Arsenal from Ant Venoms

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          Abstract

          Ants (Formicidae) represent a taxonomically diverse group of hymenopterans with over 13,000 extant species, the majority of which inject or spray secretions from a venom gland. The evolutionary success of ants is mostly due to their unique eusociality that has permitted them to develop complex collaborative strategies, partly involving their venom secretions, to defend their nest against predators, microbial pathogens, ant competitors, and to hunt prey. Activities of ant venom include paralytic, cytolytic, haemolytic, allergenic, pro-inflammatory, insecticidal, antimicrobial, and pain-producing pharmacologic activities, while non-toxic functions include roles in chemical communication involving trail and sex pheromones, deterrents, and aggregators. While these diverse activities in ant venoms have until now been largely understudied due to the small venom yield from ants, modern analytical and venomic techniques are beginning to reveal the diversity of toxin structure and function. As such, ant venoms are distinct from other venomous animals, not only rich in linear, dimeric and disulfide-bonded peptides and bioactive proteins, but also other volatile and non-volatile compounds such as alkaloids and hydrocarbons. The present review details the unique structures and pharmacologies of known ant venom proteinaceous and alkaloidal toxins and their potential as a source of novel bioinsecticides and therapeutic agents.

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          Most cited references175

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          Complex cocktails: the evolutionary novelty of venoms.

          Venoms have evolved on numerous occasions throughout the animal kingdom. These 'biochemical weapon systems' typically function to facilitate, or protect the producing animal from, predation. Most venomous animals remain unstudied despite venoms providing model systems for investigating predator-prey interactions, molecular evolution, functional convergence, and novel targets for pharmaceutical discovery. Through advances in 'omic' technologies, venom composition data have recently become available for several venomous lineages, revealing considerable complexity in the processes responsible for generating the genetic and functional diversity observed in many venoms. Here, we review these recent advances and highlight the ecological and evolutionary novelty of venom systems. Copyright © 2012 Elsevier Ltd. All rights reserved.
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            Social immunity.

            Social insect colonies have evolved collective immune defences against parasites. These 'social immune systems' result from the cooperation of the individual group members to combat the increased risk of disease transmission that arises from sociality and group living. In this review we illustrate the pathways that parasites can take to infect a social insect colony and use these pathways as a framework to predict colony defence mechanisms and present the existing evidence. We find that the collective defences can be both prophylactic and activated on demand and consist of behavioural, physiological and organisational adaptations of the colony that prevent parasite entrance, establishment and spread. We discuss the regulation of collective immunity, which requires complex integration of information about both the parasites and the internal status of the insect colony. Our review concludes with an examination of the evolution of social immunity, which is based on the consequences of selection at both the individual and the colony level.
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              Evaluating alternative hypotheses for the early evolution and diversification of ants.

              Ants are the world's most diverse and ecologically dominant eusocial organisms. Resolving the phylogeny and timescale for major ant lineages is vital to understanding how they achieved this success. Morphological, molecular, and paleontological studies, however, have presented conflicting views on early ant evolution. To address these issues, we generated the largest ant molecular phylogenetic data set published to date, containing approximately 6 kb of DNA sequence from 162 species representing all 20 ant subfamilies and 10 aculeate outgroup families. When these data were analyzed with and without outgroups, which are all distantly related to ants and hence long-branched, we obtained conflicting ingroup topologies for some early ant lineages. This result casts strong doubt on the existence of a poneroid clade as currently defined. We compare alternate attachments of the outgroups to the ingroup tree by using likelihood tests, and find that several alternative rootings cannot be rejected by the data. These alternatives imply fundamentally different scenarios for the early evolution of ant morphology and behavior. Our data strongly support several notable relationships within the more derived formicoid ants, including placement of the enigmatic subfamily Aenictogitoninae as sister to Dorylus army ants. We use the molecular data to estimate divergence times, employing a strategy distinct from previous work by incorporating the extensive fossil record of other aculeate Hymenoptera as well as that of ants. Our age estimates for the most recent common ancestor of extant ants range from approximately 115 to 135 million years ago, indicating that a Jurassic origin is highly unlikely.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                Toxins (Basel)
                Toxins (Basel)
                toxins
                Toxins
                MDPI
                2072-6651
                20 January 2016
                January 2016
                : 8
                : 1
                : 30
                Affiliations
                [1 ]CNRS, UMR Écologie des Forêts de Guyane (AgroParisTech, CIRAD, CNRS, INRA, Université de Guyane, Université des Antilles), Campus Agronomique, BP 316, Kourou Cedex 97379, France; Jerome.Orivel@ 123456ecofog.gf (J.O.); alain.dejean@ 123456wanadoo.fr (A.D.)
                [2 ]BTSB (Biochimie et Toxicologie des Substances Bioactives) Université de Champollion, Place de Verdun, Albi 81012, France
                [3 ]Neurotoxin Research Group, School of Medical & Molecular Biosciences, University of Technology Sydney, Broadway, Sydney, NSW 2007, Australia; samira.aili@ 123456uts.edu.au (S.R.A.); graham.nicholson@ 123456uts.edu.au (G.M.N.)
                [4 ]Red Imported Fire Ant Research Center, South China Agricultural University, Guangzhou 510642, China; ofoxofox@ 123456gmail.com
                [5 ]VenomeTech, 473 Route des Dolines—Villa 3, Valbonne 06560, France; escoubas@ 123456venometech.com
                [6 ]Laboratoire Écologie Fonctionnelle et Environnement, 118 Route de Narbonne, Toulouse 31062, France
                Author notes
                [* ]Correspondence: t.axel@ 123456hotmail.fr ; Tel.: +33-5-6348-1997; Fax: +33-5-6348-6432
                [†]

                These authors contributed equally to this work.

                Article
                toxins-08-00030
                10.3390/toxins8010030
                4728552
                26805882
                7a4f0e48-c9da-4843-a9dc-e28c31698147
                © 2016 by the authors; licensee MDPI, Basel, Switzerland.

                This article is an open access article distributed under the terms and conditions of the Creative Commons by Attribution (CC-BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 22 December 2015
                : 08 January 2016
                Categories
                Review

                Molecular medicine
                ant venom,toxins,venom biochemistry,alkaloids,formic acid,peptides,enzymes
                Molecular medicine
                ant venom, toxins, venom biochemistry, alkaloids, formic acid, peptides, enzymes

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