Abstract
Herbivorous insects show varying levels of diet specialization. Hemipterans usually feed on nutritionally poor diets, and harbor symbionts that supply the host with essential nutrients. Here, we investigate the effects of host plant suitability on the biology of the oligophagous aphid Aphis citricidus (Hemiptera: Aphididae) and the polyphagous Aphis aurantii (Hemiptera: Aphididae), and on their obligate symbiont Buchnera aphidicola. We investigated aphids development when restricted to host plants with different nutritional qualities, e.g. sweet orange (Citrus sinensis) and orange jasmine (Murraya paniculata) and when alternating host plant quality during the immature and adult stages. Sweet orange was the most adequate host for both aphid species, while orange jasmine had a much stronger impact on fitness for the oligophagous than for the polyphagous aphid. The growth pattern of Buchnera differed between aphids and host plants. Buchnera density increased as A. citricidus developed on sweet orange, but decreased in A. citricidus feeding on orange jasmine. Buchnera increased in density in A. aurantii on both host plants. Finally, these fluctuations in Buchnera density reflect the contribution of food source, and we provide arguments on the dynamics of the interactions among aphids, Buchnera and host plant suitability, considering the oligophagous-polyphagous dichotomy.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302. https://doi.org/10.1016/j.tplants.2012.02.006
Andrewartha HG, Birch LC (1954) The innate capacity for increase in numbers. University of Chicago Press, Chicago
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. https://doi.org/10.1146/annurev.ento.47.091201.145300
Baumann L, Baumann P (2005) Cospeciation between the primary endosymbionts of mealybugs and their hosts. Curr Microbiol 50:84–87. https://doi.org/10.1007/s00284-004-4437-x
Buchner P (1965) Endosymbiosis of animals with plant microorganisms. John Wiley, New Jersey
Carver M (1978) The black citrus aphids, Toxoptera citricidus (Kirkaldy) and T. aurantii (Boyer de Fonscolombe) (Homoptera: Aphididae). Aust J Entomol 17:263–270. https://doi.org/10.1111/j.1440-6055.1978.tb00156.x
Cassone BJ, Redinbaugh MG, Dorrance AE, Michel AP (2015) Shifts in Buchnera aphidicola density in soybean aphids (Aphis glycines) feeding on virus-infected soybean. Insect Mol Biol 24:422–431. https://doi.org/10.1111/imb.12170
Chandler SM, Wilkinson TL, Douglas AE (2008) Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria. Proc R Soc B 275:565–570. https://doi.org/10.1098/rspb.2007.1478
Colasurdo N, Gelinas Y, Despland E (2009) Larval nutrition affects life history traits in a capital breeding moth. J Exp Bio 212:1794–1800. https://doi.org/10.1242/jeb.027417
Czerniewicz P, Leszczynski B, Chrzanowski G, Sempruch C, Sytykiewicz H (2011) Effects of host plant phenolics on spring migration of bird cherry-oat aphid (Rhopalosiphum padi L.). Allelopathy J 27:309–316. https://doi.org/10.1016/j.jip.2004.05.003
Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37. https://doi.org/10.1146/annurev.ento.43.1.17
Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754. https://doi.org/10.1093/jxb/erj067
Du Plessis H, Byrne M, Van Den Berg J (2015) The effect of different host plants on development and survival of Nysius natalensis (Hemiptera: Orsillidae). Environ Entomol 44:122–127.https://doi.org/10.1093/ee/nvu009
Fuentealba A, Bauce E (2012) Carry-over effect of host nutritional quality on performance of spruce budworm progeny. Bull Entomol Res 102:275–284. https://doi.org/10.1017/s0007485311000617
Gunduz AE, Douglas AE (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc R Soc B 276:987-991.https://doi.org/10.1098/rspb.2008.1476
Gutbrodt B, Dorn S, Unsicker SB, Mody K (2012) Species-specific responses of herbivores to within-plant and environmentally mediated between-plant variability in plant chemistry. Chemoecology 22:101–111. https://doi.org/10.1007/s00049-012-0102-1
Halbert SE, Brown LG (2011) Brown Citrus aphid, Toxoptera citricida (Kirkaldy) (Insecta: Hemiptera: Aphididae). University of Florida IFAS Extension, Florida
Hansen AK, Moran NA (2011) Aphid genome expression reveals host–symbiont cooperation in the production of amino acids. Proc Natl Acad Sci U S A 108:2849–2854. https://doi.org/10.1073/pnas.1013465108
Hansen AK, Moran NA (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol 23:1473–1496. https://doi.org/10.1111/mec.12421
Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T (2006) Strict host symbiont cospeciation and reductive genome evolution in insect gut bacteria. Plos Bio 4:1841–1851. https://doi.org/10.1371/journal.pbio.0040337
House HL (1961) Insect nutrition. Annu Rev Entomol 6:13–26. https://doi.org/10.1146/annurev.en.06.010161.000305
Humphreys NJ, Douglas AE (1997) Partitioning of symbiotic bacteria between generations of insect: a quantitative study of a Buchnera sp in the pea aphid (Acyrthosiphon pisum) reared at different temperatures. Appl Environ Microb 63:3294–3296
Joern A, Provin T, Behmer ST (2012) Not just the usual suspects: insect herbivore populations and communities are associeted with multiple plant nutrients. Ecology 93:1002–1015. https://doi.org/10.1890/11-1142.1
Johns RC, Tobita H, Hara H, Ozaki K (2015) Adaptive advantages of dietary mixing different-aged foliage within conifers for a generalist defoliator. Ecol Res 30:793–802. https://doi.org/10.1007/s11284-015-1280-4
Katsir L, Chung HS, Koo AJK, Howe GA (2008) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Bio 11:428–435. https://doi.org/10.1016/j.pbi.2008.05.004
Killiny N (2017) Metabolite signature of the phloem sap of fourteen citrus varieties with different degrees of tolerance to Candidatus Liberibacter asiaticus. Physiol Mol Plant Pathol 97:20–29. https://doi.org/10.1016/j.pmpp.2016.11.004
Knuttel H, Fiedler K (2001) Host-plant-derived variation in ultraviolet wing patterns influences mate selection by male butterflies. J Exp Biol 204:2447–2459
Koga R, Tsuchida T, Fukatsu T (2003) Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc R Soc B 270:2543–2550. https://doi.org/10.1098/rspb.2003.2537
Komaki K, Ishikawa H (2000) Genomic copy number of intracellular bacterial symbionts of aphids varies in response to developmental stage and morph of their host. Insect Biochem Molec Biol 30:253–258. https://doi.org/10.1016/s0965-1748(99)00125-3
Lu WN, Chiu MC, Kuo MH (2014) Host life stage- and temperature-dependent density of the symbiont Buchnera aphidicola in a subtropical pea aphid (Acyrthosiphon pisum) population. J Asia Pac Entomol 17:537–541. https://doi.org/10.1016/j.aspen.2014.03.012
Maia ADHN, Luiz AJB (2006) Programa SAS para análise de tabelas de vida e fertilidade de artrópodes: o método Jackknife. EMBRAPA, Jaguariúna
McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nature Rev Microbiol 10:13–26. https://doi.org/10.1038/nrmicro2670
Milanović S, Janković-Tomanić M, Kostić I, Kostić M, Morina F, Živanović B, Lazarević J (2016) Behavioural and physiological plasticity of gypsy moth larvae to host plant switching. Entomol Exp Appl (2):152–158. https://doi.org/10.1111/eea.12388
Mody K, Unsicker SB, Linsenmair KE (2007) Fitness related dietmixing by intraspecific host-plant-switching of specialist insect herbivores. Ecology 88:1012–1020. https://doi.org/10.1890/06-1338
Moore PJ, Attisano A (2011) Oosorption in response to poor food: complexity in the trade-off between reproduction and survival. Ecol Evol 1:37–45. https://doi.org/10.1002/ece3.4
Moran NA, Yun Y (2015) Experimental replacement of an obligate insect symbiont. Proc Natl Acad Sci U S A 112:2093–2096. https://doi.org/10.1073/pnas.1420037112
Muller K, Vogelweith F, Thiery D, Moret Y, Moreau J (2015) Immune benefits from alternative host plants could maintain polyphagy in a phytophagous insect. Oecologia 177:467–475. https://doi.org/10.1007/s00442-014-3097-1
Nakabachi A, Ishida K, Hongoh Y, Ohkuma M, Miyagishima SY (2014) Aphid gene of bacterial origin encodes a protein transported to an obligate endosymbiont. Curr Biol 24:640–641. https://doi.org/10.1016/j.cub.2014.06.038
Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci U S A 102:12795–12800. https://doi.org/10.1073/pnas.0506131102
Oliver KM, Moran NA, Hunter MS (2006) Costs and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc B 273:1273–1280. https://doi.org/10.1098/rspb.2005.3436
Pennacchio F, Caccia S, Digilio MC (2014) Host regulation and nutritional exploitation by parasitic wasp. Curr Opin Insect Sci 6:74–79. https://doi.org/10.1016/j.cois.2014.09.018
Perez-Brocal V, Gil VR, Ramos S, Lamelas A, Postigo M, Michelena JM, Silva FJ, Moya A, Latorre AA (2006) Small microbial genome: the end of a long symbiotic relationship? Science 314:312–313. https://doi.org/10.1126/science.1130441
Prosser WA, Douglas AE (1992) A test of the hypotheses that nitrogen is upgraded and recycled in an aphid (Acyrthosiphon pisum) symbiosis. J Insect Physiol 38:93–99. https://doi.org/10.1016/0022-1910(92)90037-e
R Core Team (2015) R: A language and environment for statistical computing. R Forun data on for Statistical Computing. https://www.R-project.org/. Accessed 15 July 2015
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratoty Press, Cold Spring Harbor
Sandström J, Pettersson J (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J Insect Physiol 40:947–955. https://doi.org/10.1016/0022-1910(94)90133-3
Sandström J, Telang A, Moran NA (2000) Nutritional enhancement of host plants by aphids: a comparison of three aphid species on grasses. J Insect Physiol 46:33–40. https://doi.org/10.1016/s0022-1910(99)00098-0
SAS Institute INC (2015) SAS language v.9. Cary, SAS Institute
Scriber JM, Slansky F Jr (1981) The nutritional ecology of immature insects. Annu Rev Entomol 26:183–211. https://doi.org/10.1146/annurev.en.26.010181.001151
Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp APS. Nature 407:81–86
Simon JC, D’Alençon E, Guy E, Jacquin-Joly E, Jaquiéry J, Nouhaud P, Peccoud J, Sugio A, Streiff R (2015) Genomics of adaptation to host-plants in herbivorous insects. Brief Funct Genomics 14:413–423. https://doi.org/10.1093/bfgp/elv015
Simonet P, Duport G, Gaget K, Weiss-Gayet M, Colella S, Febvay G, Charles H, Vinuelas J, Heddi A, Calevro F (2016). Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis. Sci Rep 6. https://doi.org/10.1038/srep19967
Stam JM, Kroes A, Li Y, Gols R, Van Loon JJA, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713. https://doi.org/10.1146/annurev-arplant-050213-035937
Sugio A, Dubreuil G, Giron D, Simon JC (2015) Plant-insect interactions under bacterial influence: ecological implications and underlying mechanisms. J Exp Bot 66:467–478. https://doi.org/10.1093/jxb/eru435
Sunnucks P, De Barro PJ, Lushai G, Maclean N, Hales D (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Mol Ecol 6:1059–1073. https://doi.org/10.1046/j.1365-294x.1997.00280.x
Tang YQ, Lapointe SL, Brown LG, Hunter WB (1999) Effects of host plant and temperature on the biology of Toxoptera citricida (Homoptera : Aphididae). Environ Entomol 28:895–900. https://doi.org/10.1093/ee/28.5.895
Telang A, Sandström J, Dyreson E, Moran NA (1999) Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomol Exp Appl 91:403–412. https://doi.org/10.1046/j.1570-7458.1999.00508.x
Thao ML, Baumann P (2004) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol 70:3401–3406. https://doi.org/10.1128/aem.70.6.3401-3406.2004
Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P (2000) Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol 66:2898–2905. https://doi.org/10.1128/aem.66.7.2898-2905.2000
Tsai JH (1998) Development, survivorship, and reproduction of Toxoptera citricida (Kirkaldy) (Homoptera : Aphididae) on eight host plants. Environ Entomol 27:1190–1195. https://doi.org/10.1093/ee/27.5.1190
Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, Simon JC, Fukatsu T (2002) Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol Ecol 11:2123–2135. https://doi.org/10.1046/j.1365-294x.2002.01606.x
Van Ham R, Van Ham RCHJ, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, Fernandez JM, Jimenez L, Postigo M, Silva FJ, Tammames J, Viguera E, Latorre A, Valencia A, Moran F, Moya A (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100:581–586. https://doi.org/10.1073/pnas.0235981100
Vogel KJ, Moran NA (2011) Effect of host genotype on symbiont titer in the aphid Buchnera symbiosis. Insects 2:423–434. https://doi.org/10.3390/insects2030423
Wang JJ, Tsai JH (2001) Development, survival and reproduction of black citrus aphid, Toxoptera aurantii (Hemiptera: Aphididae), as a function of temperature. Bull Entomol Res 91:477–487. https://doi.org/10.1079/BER2001120
Whelan JA, Russel NB, Whelan MA (2003) A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 278:261–269. https://doi.org/10.1016/s0022-1759(03)00223-0
Wilkinson TL, Adams D, Minto LB, Douglas AE (2001) The impact of host plant on the abundance and function of symbiotic bacteria in an aphid. J Exp Biol 204:3027–3038
Wilkinson TL, Fukatsu T, Ishikawa H (2003) Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Arthropod Struct Dev 32:241–245. https://doi.org/10.1016/s1467-8039(03)00036-7
Wilkinson TL, Koga R, Fukatsu T (2007) Role of host nutrition in symbiont regulation: impact of dietary nitrogen on proliferation of obligate and facultative bacterial endosymbionts of the pea aphid Acyrthosiphon pisum. Appl Environ Microbiol 73:1362–1366. https://doi.org/10.1128/aem.01211-06
Zar JH (1999) Biostatistical analysis. Pearson Education Inc, New Jersey
Zhang Y, Cao W, HCJ G, Liu X (2016) Host plant determines the population soze of an obligate symbiont (Buchnera aphidicola) in aphids. Appl Environ Microbiol 82:2336–2346. https://doi.org/10.1128/AEM.04131-15
Acknowledgments
Authors thank FAPESP by providing a PhD fellowship to ASG (Grant # 2012/04287-0, São Paulo Research Foundation). Authors also thank CNPq (Grant # 490474/2011-0) and FAPESP (Grant # 2011/50877-0, São Paulo Research Foundation) for providing research funds to the senior author FLC.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Guidolin, A.S., Cônsoli, F.L. Influence of host plant on oligophagous and polyphagous aphids, and on their obligate symbiont titers. Biologia 75, 71–81 (2020). https://doi.org/10.2478/s11756-019-00274-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-019-00274-3