Brady CM, Asplen MK, Desneux N, Heimpel GE, Hopper KR, Linnen CR, Oliver KM, Wulff JA, White JA (2014) Worldwide populations of the aphid Aphis craccivora are infected with diverse facultative bacterial symbionts. Microb Ecol 67(1):195–204. https://doi.org/10.1007/s00248-013-0314-0

Article  PubMed  Google Scholar 

Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S, Stern DL (2003) Developmental origin and evolution of bacteriocytes in the aphid–Buchnera symbiosis. PLoS Biol 1(1):e21. https://doi.org/10.1371/journal.pbio.0000021

Article  PubMed  PubMed Central  Google Scholar 

Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Machler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9(2):378–400. https://doi.org/10.3929/ethz-b-000240890

Article  Google Scholar 

Buckley RC (1987) Interactions involving plants, homoptera, and ants. Annu Rev Ecol Syst 18(1):111–135. https://doi.org/10.1146/annurev.es.18.110187.000551

Article  Google Scholar 

Chen D-Q, Montllor CB, Purcell AH (2000) Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. Kondoi. Entomologia Experimentalis Et Applicata 95(3):315–323. https://doi.org/10.1046/j.1570-7458.2000.00670.x

Article  Google Scholar 

Dugravot S, Brunissen L, Létocart E, Tjallingii WF, Vincent C, Giordanengo P, Cherqui A (2007) Local and systemic responses induced by aphids in Solanum tuberosum plants. Entomol Exp Appl 123(3):271–277. https://doi.org/10.1111/j.1570-7458.2007.00542.x

Article  Google Scholar 

El-Ziady S, Kennedy JS (1956) Beneficial effects of the common garden ant, Lasius niger L., on the black bean aphid, Aphis fabae Scopoli. Proc Royal Entomol Soc London. Ser A, Gen Entomol 31(4–6):61–65. https://doi.org/10.1111/j.1365-3032.1956.tb00208.x

Article  Google Scholar 

Endo S, Itino T (2012) The aphid-tending ant Lasius fuji exhibits reduced aggression toward aphids marked with ant cuticular hydrocarbons. Popul Ecol 54(3):405–410. https://doi.org/10.1007/s10144-012-0314-9

Article  Google Scholar 

Fischer CY, Detrain C, Thonart P, Haubruge E, Francis F, Verheggen FJ, Lognay GC (2017) Bacteria may contribute to distant species recognition in ant-aphid mutualistic relationships : bacteria may help mutualistic species recognition. Insect Sci 24(2):278–284. https://doi.org/10.1111/1744-7917.12302

Article  CAS  PubMed  Google Scholar 

Fischer CY, Lognay GC, Detrain C, Heil M, Grigorescu A, Sabri A, Thonart P, Haubruge E, Verheggen FJ (2015) Bacteria may enhance species association in an ant–aphid mutualistic relationship. Chemoecology 25(5):223–232. https://doi.org/10.1007/s00049-015-0188-3

Article  CAS  Google Scholar 

Flatt T, Weisser WW (2000) The effects of mutualistic ants on aphid life history traits. Ecology 81(12):3522–3529. https://doi.org/10.1890/0012-9658(2000)081[3522:TEOMAO]2.0.CO;2

Article  Google Scholar 

Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3(5):294–299

CAS  Google Scholar 

Foottit RG, Maw HEL, Von Dohlen CD, Hebert PDN (2008) Species identification of aphids (Insecta : Hemiptera: Aphididae) through DNA barcodes. Mol Ecol Resour 8(6):1189–1201. https://doi.org/10.1111/j.1755-0998.2008.02297.x

Article  CAS  PubMed  Google Scholar 

Fukatsu T, Nikoh N (1998) Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl Environ Microbiol 64(10):3599–3606. https://doi.org/10.1128/AEM.64.10.3599-3606.1998

Article  CAS  PubMed  PubMed Central  Google Scholar 

Gehrer L, Vorburger C (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Let 8(4):613–615. https://doi.org/10.1098/rsbl.2012.0144

Article  Google Scholar 

Guo J, Hao G, Hatt S, Wang Z, Francis F (2022) Host plant adaptability and proteomic differences of diverse Rhopalosiphum maidis (Fitch) lineages. Arch Insect Biochem Physiol 109(1):e21853. https://doi.org/10.1002/arch.21853

Article  CAS  PubMed  Google Scholar 

Guo J, Hatt S, He K, Chen J, Francis F, Wang Z (2017) Nine facultative endosymbionts in aphids. A review. J Asia-Pac Entomol 20(3):794–801. https://doi.org/10.1016/j.aspen.2017.03.025

Article  Google Scholar 

Haynes KF (1988) Sublethal effects of neurotoxic insecticides on insect behavior. Annu Rev Entomol 33(1):149–168. https://doi.org/10.1146/annurev.en.33.010188.001053

Article  CAS  PubMed  Google Scholar 

Henry LM, Maiden MCJ, Ferrari J, Godfray HCJ (2015) Insect life history and the evolution of bacterial mutualism. Ecol Lett 18(6):516–525. https://doi.org/10.1111/ele.12425

Article  PubMed  Google Scholar 

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 Royal Soc London. Ser B: Biol Sci 270(1533):2543–2550. https://doi.org/10.1098/rspb.2003.2537

Article  Google Scholar 

Kwon T-S (2010) Effect of the application of an organophosphate pesticide (Fenitrothion) on foraging behavior of ants. J Korean For Soc 99:179–185

Google Scholar 

Lapolla JS, Brady SG, Shattuck SO (2011) Monograph of Nylanderia (Hymenoptera: Formicidae) of the world: an introduction to the systematics and biology of the genus. Zootaxa 3110(1):1. https://doi.org/10.11646/zootaxa.3110.1.1

Article  Google Scholar 

Leroy PD, Sabri A, Heuskin S, Thonart P, Lognay G, Verheggen FJ, Francis F, Brostaux Y, Felton GW, Haubruge E (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat Commun 2:348. https://doi.org/10.1038/ncomms1347

Article  CAS  PubMed  Google Scholar 

Luttenschlager H, Noël G, Carpentier J, Glacet L, Ravelomanana A, Claude Rakotonirina J, Rajaonera T, Francis F (2024) Inventaire préliminaire des relations entre pucerons myrmécophiles et fourmis des parcelles agricoles en périphérie de la ville d’Antananarivo (Madagascar). Entomologie Faunistique - Faunistic Entomology 77:52–60

Article  Google Scholar 

Nielsen C, Agrawal AA, Hajek AE (2009) Ants defend aphids against lethal disease. Biol Let 6(2):205–208. https://doi.org/10.1098/rsbl.2009.0743

Article  Google Scholar 

Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55(1):247–266. https://doi.org/10.1146/annurev-ento-112408-085305

Article  CAS  PubMed  Google Scholar 

Peccoud J, Bonhomme J, Mahéo F, de la Huerta M, Cosson O, Simon J-C (2014) Inheritance patterns of secondary symbionts during sexual reproduction of pea aphid biotypes. Insect Sci 21(3):291–300. https://doi.org/10.1111/1744-7917.12083

Article  CAS  PubMed  Google Scholar 

Pons I, Renoz F, Noël C, Hance T (2019) New insights into the nature of symbiotic associations in aphids : infection process, biological effects, and transmission mode of cultivable Serratia symbiotica bacteria. Appl Environ Microbiol 85(10):e02445-e2518. https://doi.org/10.1128/AEM.02445-18

Article  CAS  PubMed  PubMed Central  Google Scholar 

Pons I, Scieur N, Dhondt L, Renard M-E, Renoz F, Hance T (2022) Pervasiveness of the symbiont Serratia symbiotica in the aphid natural environment: distribution, diversity and evolution at a multitrophic level. FEMS Microbiol Ecol 98(1):fiac012. https://doi.org/10.1093/femsec/fiac012

Article  CAS  PubMed  Google Scholar 

Renoz F, Pons I, Vanderpoorten A, Bataille G, Noël C, Foray V, Pierson V, Hance T (2019) Evidence for gut-associated Serratia symbiotica in wild aphids and ants provides new perspectives on the evolution of bacterial mutualism in insects. Microb Ecol 78(1):159–169. https://doi.org/10.1007/s00248-018-1265-2

Article  CAS  PubMed  Google Scholar 

Rice KB, Eubanks MD (2013) No enemies needed : cotton aphids (Hemiptera: Aphididae) directly benefit from red imported fire ant (Hymenoptera: Formicidae) tending. Fla Entomol 96(3):929–932. https://doi.org/10.1653/024.096.0329

Article  Google Scholar 

Sabri A, Vandermoten S, Leroy PD, Haubruge E, Hance T, Thonart P, De Pauw E, Francis F (2013) Proteomic investigation of aphid honeydew reveals an unexpected diversity of proteins. PLoS ONE 8(9):e74656. https://doi.org/10.1371/journal.pone.0074656

Article  CAS  PubMed  PubMed Central