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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. Digital Object Identifier (DOI) http://dx.doi.org/10.1128/AEM.01775-14 This article is available at UKnowledge: https://uknowledge.uky.edu/entomology_facpub/72 Factors Limiting the Spread of the Protective Symbiont Hamiltonella defensa in Aphis craccivora Aphids Hannah R. Dykstra,a Stephanie R. Weldon,a Adam J. Martinez,a Jennifer A. White,b Keith R. Hopper,c George E. Heimpel,d Mark K. Asplen,d Kerry M. Olivera Department of Entomology, University of Georgia, Athens, Georgia, USAa; Department of Entomology, University of Kentucky, Lexington, Kentucky, USAb; USDA, ARS, Newark, Delaware, USAc; Department of Entomology, University of Minnesota, St. Paul, Minnesota, USAd Downloaded from Many insects are associated with heritable symbionts that mediate ecological interactions, including host protection against nat- ural enemies. The cowpea aphid, Aphis craccivora, is a polyphagous pest that harbors Hamiltonella defensa, which defends against parasitic wasps. Despite this protective benefit, this symbiont occurs only at intermediate frequencies in field popula- tions. To identify factors constraining H. defensa invasion in Ap. craccivora, we estimated symbiont transmission rates, per- formed fitness assays, and measured infection dynamics in population cages to evaluate effects of infection. Similar to results with the pea aphid, Acyrthosiphon pisum, we found no consistent costs to infection using component fitness assays, but we did identify clear costs to infection in population cages when no enemies were present. Maternal transmission rates of H. defensa in Ap. craccivora were high (ca. 99%) but not perfect. Transmission failures and infection costs likely limit the spread of protective http://aem.asm.org/ H. defensa in Ap. craccivora. We also characterized several parameters of H. defensa infection potentially relevant to the protec- tive phenotype. We confirmed the presence of H. defensa in aphid hemolymph, where it potentially interacts with endoparasites, and performed real-time quantitative PCR (qPCR) to estimate symbiont and phage abundance during aphid development. We also examined strain variation of H. defensa and its bacteriophage at multiple loci, and despite our lines being collected in differ- ent regions of North America, they were infected with a nearly identical strains of H. defensa and APSE4 phage. The limited strain diversity observed for these defensive elements may result in relatively static protection profile for this defensive symbiosis. on October 30, 2015 by UNIV OF KENTUCKY any, if not most, insect species are infected with maternally reported infection frequencies ranging from ca. 30 to 60% in three Mtransmitted bacterial symbionts capable of exerting major North American Medicago populations (27). In laboratory-reared effects on host biology (1–5). While some heritable symbiont in- Ac. pisum, vertical transmission rates of the common gammapro- fections are required for their insect host’s survival and reproduc- teobacterial facultative symbionts approach 100% (32–34). Inher- tion, e.g., the bacteriocyte-associated nutritional symbionts found itance failures under natural conditions and during the overwin- in sap-feeding insects (6), the majority represent facultative infec- tering egg stage potentially influence symbiont frequencies, but tions (4). Many facultative symbionts mediate important ecolog- rates of loss are unknown. Clear costs to infections with protective ical interactions, and there is an emerging awareness that infection bacteria, including Hamiltonella defensa, have been difficult to can protect hosts from a range of environmental threats (3, 7–9). identify for particular symbionts in Ac. pisum (9). Studies of stan- Both theory and experimental evidence indicate that protective dard fitness parameters (e.g., fecundity and development time) benefits likely contribute to the spread of heritable symbionts comparing aphids of the same genotype with and without H. de- within host populations (10–13). Heritable facultative symbiont fensa, which protects against parasitoids, find no consistent costs infections, however, are often found at intermediate frequencies to infection and in fact often report benefits (for examples, see in natural populations, and infection costs and transmission fail- references 13 and 18). Population cage studies, however, identify ures are potentially important in limiting their spread (9). benefits to infection in the presence of parasitoid wasps but costs The heritable symbionts of the pea aphid Acyrthosiphon pisum in control cages lacking enemies (13), suggesting that fitness are among the best studied (14). All Ac. pisum aphids possess the tradeoffs contribute to the maintenance of H. defensa at interme- obligate nutritional symbiont Buchnera aphidicola (1, 15), and diate frequencies in natural populations. many harbor one or more facultative symbionts (14). Aphids are Many of the symbionts infecting Ac. pisum are found in other ideal for studying the effects of heritable infections, because fac- aphid species and in other insects more generally, yet their roles in ultative symbionts can be manipulated among clonal lineages, re- sulting in experimental aphid lines that, for example, share the same genetic background but vary in terms of infection by partic- Received 29 May 2014 Accepted 9 July 2014 ular symbionts (14). Such experimental studies with Ac. pisum Published ahead of print 11 July 2014 have identified diverse benefits to infection with common facul- Editor: H. Goodrich-Blair tative symbionts, including protection against heat stress (16–18), Address correspondence to Kerry M. Oliver, [email protected]. fungal pathogens (19–21), and parasitoid wasps (22–24). Despite Supplemental material for this article may be found at http://dx.doi.org/10.1128 these benefits, the heritable protective symbionts of Ac. pisum typ- /AEM.01775-14. ically remain at intermediate frequencies among surveyed popu- Copyright © 2014, American Society for Microbiology. All Rights Reserved. lations (for examples, see references 25 to 31). For example, a doi:10.1128/AEM.01775-14 survey of Hamiltonella defensa, which defends against parasitoids, 5818 aem.asm.org Applied and Environmental Microbiology p. 5818–5827 September 2014 Volume 80 Number 18 Factors Limiting Symbiont Spread in Aphis craccivora other hosts are less well known. H. defensa, for example, is esti- TABLE 1 Collection data for Ap. craccivora clones used in the present mated to occur in 14% of aphid species (14). Recent work has studya shown that this symbiont confers protection against parasitoids in Clone Location Year two other aphid hosts: the black bean aphid, Aphis fabae (35), with AC1 Lexington, KY 2010 which costs to infection have also been found (36), and the cowpea AC17 Tucson, AZ 2009 aphid, Aphis craccivora (37, 38). Interestingly, in Ap. craccivora, H. AC21 Tucson, AZ 2009 defensa protects only against some parasitoid species, completely LL1 Lexington, KY 2011 eliminating parasitism by two Binodoxys species but having no SV1 Harrodsburg, KY 2011 effect on two other aphidiine braconids, Aphidius colemani and a The host plant in all cases was Medicago sativa. DGGE confirmed the presence of H. Lysiphlebus orientalis (37). These findings, together with results defensa only in all clones. from Ac. pisum, indicate that host protection may be a common Downloaded from phenotype associated with H. defensa, although there have been strains identified in both the grain aphid, Sitobion avenae (39), and plant pot) in biological incubators (Percival Scientific, Inc., Perry, IA) at possibly Ac. pisum (40) that do not confer host protection. both 20 and 25°C with a 16-h:8-h light-dark cycle. The long-day condi- Although the mechanisms underlying
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