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Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela Sabater, Beatriz; Van Ham, Roeland C. H. J.; Martínez, David; Silva, Francisco; Latorre, Amparo; Moya, Andrés Molecular evolution of aphids and their primary (buchnera SP.) and secondary endosymbionts: implications for the role of symbiosis in insect evolution Interciencia, vol. 26, núm. 10, octubre, 2001, pp. 508-512 Asociación Interciencia Caracas, Venezuela Available in: http://www.redalyc.org/articulo.oa?id=33906115 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative MOLECULAR EVOLUTION OF APHIDS AND THEIR PRIMARY (BUCHNERA SP.) AND SECONDARY ENDOSYMBIONTS: IMPLICATIONS FOR THE ROLE OF SYMBIOSIS IN INSECT EVOLUTION BEATRIZ SABATER, ROELAND C.H.J. VAN HAM, DAVID MARTÍNEZ-TORRES, FRANCISCO SILVA, AMPARO LATORRE and ANDRÉS MOYA he term symbiosis (from One special case of sym- With respect to the role the Greek simbios or liv- biosis is endosymbiosis, where the prokary- played by symbiosis in evolution, there are ing together) was first ote is literally sequestered within an eu- two prevailing views. The first acknowl- introduced by Anton de Bary in 1879. karyotic cell. The paradigm of endosym- edges that symbiosis is an important com- This author explicitly included parasitism biosis is the origin of the eukaryotic cell, ponent in the biology of many organisms, as a type of symbiosis and excluded in which different bacteria successively but yet does not consider it to be a major short-term associations. Some authors do entered a protoeukaryotic cell giving rise evolutionary force per se, because many not accept Bary’s definition and hold that to mitochondria first, and chloroplasts mutualistic associations have limited short-term interactions should be consid- later (Margulis, 1970; Fisher, 1989; Gray, chances of promoting significant evolu- ered true symbiosis and parasitic associa- 1989). Insects are particularly receptive to tionary innovation (Maynard Smith, 1989). tions must be rejected as such. Most re- endosymbiotic processes. It has been esti- Margulis (1991) holds a completely oppo- searchers consider, in a more restrictive mated than more than 10% of the extant site view and broadly argues against the meaning, that there is symbiosis only insect species harbor endosymbionts at Neodarwinian theory as an incomplete the- when both partners benefit from the different stages of accommodation to their ory of evolution. Her argument is based assocation. Douglas (1994) narrows the host. Some of them are recent and casual, on the scarcity of cases of observed spe- term even further and confines symbiosis but others are well established associations ciation and she maintains that the major to associations in which at least one part- that are as relevant to the insect and its taxonomic groups (i.e. phyla, kingdoms) ner bestows the other with some sort of physiology as true organelles are for an have evolved through engagements in novel metabolic capability. In most of the eukaryotic cell (Buchner, 1965). symbiotic associations. According to cases one member of the association is Empirical research on Charlesworth (1991) Margulis’ view is an eukaryote. Contrary to most prokary- symbiosis, specially at the molecular level, rather radical. Although it is possible to otes, eukaryotes have rather limited meta- is a growing and promising field. The im- admit evolutionary accommodations after a bolic capabilities and hence, symbiosis pact of symbiosis on active speciation symbiotic event between two species, has provided and continues to provide an processes, on the genomic transformations there is not an a priori reason to discard evolutionary strategy through which eu- of both partners, and on the evolutionary compatibility between this fact and the karyotes have access to a wider range of success of many taxonomic lineages is be- presence of natural selection as a driving metabolic resources. ginning to be unveiled. force promoting the evolution of the sym- KEYWORDS / Aphids / Buchnera sp. / Secondary Endosymbionts / Phylogenetic Analysis / Genome Reduction / Recibido: 26/03/2001: Aceptado: 20/09/2001 Beatriz Sabater Muñoz. Bachelor in Biology. University of Valencia, Spain. e-mail: [email protected]. Roeland C.H.J. van Ham. Ph.D. in Biology, University of Utrecht, The Netherlands. Postdoctoral researcher, Centro de Astrobiología (INTA-CSIC), Spain. e-mail: [email protected] David Martínez Torres. Ph.D. in Biology. Assistant Professor, University of Valencia, Spain. e-mail: [email protected] Francisco Silva Moreno. Ph.D. in Biology. Associate Professor, University of Valencia, Spain. e-mail: [email protected] Amparo Latorre Castillo. Ph.D. in Biology. Associate Professor, University of Valencia, Spain. e-mail: [email protected] Andrés Moya Simarro. Ph.D. in Biology, Ph.D. in Philosophy and Full Professor, University of Valencia, Spain. Address: Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Departamento de Genética, Universidad de Va- lencia, Spain, Apartado de Correos 2085, 46071, Valencia, Spain. e-mail: andré[email protected] 508 0378-1844/01/10/508-05 $ 3.00/0 OCT 2001, VOL. 26 Nº 10 biotic association. Moreover, the relevance TABLE I of symbiotic events determining the ap- SUMMARY OF THE MAJOR METABOLIC CAPABILITIES ACQUIRED BY THE pearance of major evolutionary lineages or HOST AS A BY PRODUCT OF THE SYMBIOTIC ASSOCIATION** more precisely, the role played by symbio- sis in traits that define higher taxa, should Metabolic novelty Symbiont Host be evaluated. Photosynthesis Algae and Cyanobacteria Several protists, invertebrates, lichenized fungi Endosymbiosis: A Classification Chimiosynthesis Gamma-proteobacteria Several invertebrates In most, if not all, endo- N2 fixation Rhizobium, Frankia Several plants symbiotic associations one of the two part- and cyanobacteria ners is eukaryotic (Table I). Although they Methanogenesis Methanogenic bacteria Some protists display great diversity and morphological Celulases Bacteria, ciliated protists Herbivore vertebrates complexity, eukaryotes show limited meta- and phycomicetes fungi and termites bolic capabilities, are rarely anaerobic, Luminiscence Vibrio and Photobacterium Teleosts, cephalopds, lack photosynthesis (except for plants and some protists), cannot fix nitrogen, and Synthesis of Bacteria Some insects, protists some groups have lost the ability to syn- essential nutrients thesize essential amino-acids and coen- **Modified from Douglas, 1994. zymes necessary for their basic metabo- lism. Some eukaryotes solve these limita- “telescopic generations” is often observed, Comparative Phylogenetics tions by means of a symbiotic association in which embryogenesis starts in yet un- of Buchnera sp. and Aphids with another eukaryotic or prokaryotic or- born daughters, resulting in the enclosure ganism. The examples shown in Table I of up to three generations developing Analysis of Buchnera should be considered as recent endosymbi- within an adult individual. These high re- spp. 16S rDNA sequences from different otic events compared with respiration and productive rates make of aphids an impor- aphid species supported their monophyly photosynthesis carried out by eukaryotic tant agricultural pest, promoting in their within the γ3 subdivision of the class cells, where mitochondria and chloroplasts hosts the loss of nutrients, sheet ruffling, proteobacteria, having Escherichia coli and are endosymbionts derived from ancestral galls, and other forms of structural dam- related members of the enterobacteriaceae free living proteo- and cyanobacteria, re- age. In addition, they are vectors of im- as their closest known relatives (Moran et spectively. portant plant viral diseases. al., 1993). In addition, the 16S rDNA The phloem which aphids based phylogeny of representatives of Aphids and their Endosymbionts feed upon is rich in sugars but poor in ni- Buchnera from four aphid families showed trogen compounds. In particular, the diet is complete concordance with the morphol- Within insects, the Ho- deficient in essential amino acids, vitamins ogy-based phylogeny of their aphid hosts moptera are a highly specious group, with and several lipids that are also essential (Moran and Baumann, 1994). These re- more than 30000 extant species (Remau- (Dixon, 1975; Houk and Griffiths, 1980; sults pointed to a single original infection dière and Remaudière, 1997). The most Raven, 1983; Sasaki et al., 1991; Douglas, in a common ancestor of all modern Aphi- relevant superfamilies within this order are 1993). doidea ocurred aproximately 100-250 MY Phylloseroidea, Aphidoidea, Psylloidea, Species of the genus followed by co-speciation of aphids and Aleurodoidea, and Coccoidea. Buchnera are the primary endosymbionts Buchnera (Moran et al., 1993). With more than 4400 ex- of aphid species and they are required for Several molecular phylo- tant species, the superfamily Aphidoidea is its hosts’ normal development and fecun- genetic studies using different genes from one of the most diversified and widely dity. These bacteria are located in spe- Buchnera have also shown a congruence distributed groups of Homoptera (Black- cialized, polyploid cells, called bacterio- with the morphology-based phylogeny of man and Eastop, 1994). Representatives cytes that form an organ (bacteryome)
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  • Hamiltonella Defensa</Em>

    Hamiltonella Defensa</Em>

    University of Kentucky UKnowledge Entomology Faculty Publications Entomology 9-2014 Factors Limiting the Spread of the Protective Symbiont Hamiltonella defensa in Aphis craccivora Aphids Hannah R. Dykstra University of Georgia Stephanie R. Weldon University of Georgia Adam J. Martinez University of Georgia Jennifer A. White University of Kentucky, [email protected] Keith R. Hopper US Department of Agriculture See next page for additional authors Right click to open a feedback form in a new tab to let us know how this document benefits oy u. Follow this and additional works at: https://uknowledge.uky.edu/entomology_facpub Part of the Entomology Commons Repository Citation Dykstra, Hannah R.; Weldon, Stephanie R.; Martinez, Adam J.; White, Jennifer A.; Hopper, Keith R.; Heimpel, George E.; Asplen, Mark K.; and Oliver, Kerry M., "Factors Limiting the Spread of the Protective Symbiont Hamiltonella defensa in Aphis craccivora Aphids" (2014). Entomology Faculty Publications. 72. https://uknowledge.uky.edu/entomology_facpub/72 This Article is brought to you for free and open access by the Entomology at UKnowledge. It has been accepted for inclusion in Entomology Faculty Publications by an authorized administrator of UKnowledge. For more information, please contact [email protected]. Authors Hannah R. Dykstra, Stephanie R. Weldon, Adam J. Martinez, Jennifer A. White, Keith R. Hopper, George E. Heimpel, Mark K. Asplen, and Kerry M. Oliver Factors Limiting the Spread of the Protective Symbiont Hamiltonella defensa in Aphis craccivora Aphids Notes/Citation Information Published in Applied and Environmental Microbiology, v. 80, no. 18, p. 5818-5827. Copyright © 2014, American Society for Microbiology. All Rights Reserved. The opc yright holder has granted permission for posting the article here.