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All Clone-mates are not Created Equal: Fitness Discounting Theory Predicts Pea Aphid Colony Structure

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Abstract

As many animals form aggregations, group-living is believed to be adaptive. It is not clear, though, if clonal aggregations should have spatial structure, as protecting clone-mates is the genetic equivalent of protecting self. ‘Fitness discounting’ theory states that immediate reproductive opportunities are of greater value than are delayed opportunities. Thus, we hypothesized that spatial structure should exist in colonies of unequal-aged, clonal organisms like aphids. We predicted that, compared to reproductive (5th instar) individuals, young (2nd and 3rd instar) juveniles (i.e., the youngest instars capable of emitting an alarm signal) should occupy the most dangerous feeding positions. As individuals approach reproductive maturity and alarm signals decline (4th instar), they should occupy increasingly safer feeding positions. We tested these predictions by documenting the spatial distribution of two (green and pink) pea aphid, Acyrthosiphon pisum, asexual lineages (“clones”) at 1, 3, 6, 24, 48, 72, 96, and 120 h after host plant colonization. Confirming our hypothesis, we found that early (2nd and 3rd) instar aphids occupied feeding positions with the highest predation risk. Upon reaching the penultimate (4th) instar, individuals dispersed from the colony to colonize other leaves. Thus, pea aphid colonies are not random aggregations; aphid colony structure can be explained by fitness discounting theory.

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References

  • Andersson M, Wiklund CG (1978) Clumping versus spacing out: experiments on nest predation in fieldfares (Turdus pilaris). Anim Behav 26:1207–1212

    Article  Google Scholar 

  • Barta Z, Flynn R, Giraldeau LA (1997) Geometry for a selfish foraging group: a genetic algorithm approach. Proc R Soc B Biol Sci 264:1233–1238

    Article  Google Scholar 

  • Benkmann CW (1988) Flock size, food dispersion and the feeding behaviors of crossbills. Behav Ecol Sociobiol 23:167–175

    Article  Google Scholar 

  • Biesinger Z, Haefner JW (2005) Proximate cues for predator searching: a quantitative analysis of hunger and encounter rate in the ladybird (Coccinella septempuctata). Anim Behav 69:235–244

    Article  Google Scholar 

  • Blackman RL (1979) Stability and variation in aphid clonal lineages. Biol J Linn Soc 11:259–277

    Article  Google Scholar 

  • Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer, Sunderland

    Google Scholar 

  • Braendle C, Weisser WW (2001) Variation in escape behavior of red and green clones in the pea aphid. J Insect Behav 14:497–509

    Article  Google Scholar 

  • Byers JA (2005) A cost of alarm pheromone production in cotton aphids, Aphis gossypii. Naturwissenschaften 92:69–72

    Article  PubMed  CAS  Google Scholar 

  • Caraco T, Pulliam HR (1984) Sociality and survivorship in animals exposed to predation. In: Price PW, Slobodchickoff CN, Gaud WS (eds) A new ecology: Novel approaches to interactive systems. Wiley Interscience, New York, pp 279–309

    Google Scholar 

  • Caro TM (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago

    Google Scholar 

  • Clark CW, Mangel M (1986) The evolutionary advantages of group foraging. Theor Popul Biol 30:45–75

    Article  Google Scholar 

  • Conner JK, Hartl DL (2004) A primer of ecological genetics. Sinauer, Sunderland

    Google Scholar 

  • Costamagna AC, Landis DA, Brewer MJ (2008) The role of natural enemy guilds in Aphis glycines suppression. Biol Control 45:368–379

    Article  Google Scholar 

  • Dawkins R (1982) The extended phenotype: The gene as the unit of selection. W.H. Freeman and Company, Oxford

    Google Scholar 

  • Dehn MM (1990) Vigilance for predators: detection and dilution effects. Behav Ecol Sociobiol 26:337–342

    Google Scholar 

  • Dixon AFG (1958) The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L). Trans R Soc London 110:319–334

    Google Scholar 

  • Dixon AFG (1959) An experimental study of the searching behaviour of the predatory coccinellid beetle Adalia decempunctata (L.). J Anim Ecol 28:259–281

    Article  Google Scholar 

  • Dixon AFG (1977) Aphid ecology: life cycles, polymorphism and population regulation. Annu Rev Ecol Syst 8:329–353

    Article  Google Scholar 

  • Dixon AFG (1985) Aphid ecology. Blackie, Glascow

    Google Scholar 

  • Dixon AFG, Wratten SD (1971) Laboratory studies on aggregation, size, and fecundity in the black bean aphid, Aphis fabae Scop. B Entomol Res 61:97–111

    Article  Google Scholar 

  • Gutierrez AP, Hagen KS, Ellis CK (1990) Evaluating the impact of natural enemies: a multitrophic perspective. In: Mackauer M, Ehler LE, Roland J (eds) Critical issues in biological control. Intercept, Andover, pp 81–109

    Google Scholar 

  • Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef- building corals. Ecology 77:950–963

    Article  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour II. J Theor Biol 7:17–52

    Article  PubMed  CAS  Google Scholar 

  • Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311

    Article  PubMed  CAS  Google Scholar 

  • Harmon JP, Losey JE, Ives AR (1998) The role of vision and color in the close proximity foraging behavior of four coccinellid species. Oecologia 115:287–292

    Article  Google Scholar 

  • Harvell CD, Grosberg RK (1988) The timing of sexual maturity in clonal animals. Ecology 69:1855–1864

    Article  Google Scholar 

  • Houston AI, McNamara JM (1986) The influence of mortality on the behaviour that maximises reproductive success in a patchy environment. Oikos 47:267–274

    Article  Google Scholar 

  • Ide T, Suzuki N, Katayama N (2007) The use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae). Ecol Entomol 32:455–460

    Article  Google Scholar 

  • Inbar M, Eshel A, Wool D (1995) Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology 76:1506–1515

    Article  Google Scholar 

  • Iwasa Y, Suzuki Y, Matsuda H (1984) Theory of oviposition strategy of parasitoids. I. Effect of mortality and limited egg number. Theor Popul Biol 26:205–227

    Article  PubMed  CAS  Google Scholar 

  • Janzen DH (1977) What are dandelions and aphids? Am Nat 111:586–589

    Article  Google Scholar 

  • Johnson PCD, Whitfield JA, Foster WA, Amos W (2002) Clonal mixing in the soldier-producing aphid Pemphigus spyrothecae (Hemiptera: Aphididae). Mol Ecol 11:1525–1531

    Article  PubMed  Google Scholar 

  • Kidd NAC (1977) Factors influencing aggregation between nymphs of the lime aphid, Eucallipterus tiliae (L.). Ecol Entomol 2:273–277

    Article  Google Scholar 

  • Kidd NAC (1982) Predator avoidance as a result of aggregation in the grey pine aphid, Schizolachnus pineti. J Anim Ecol 51:397–412

    Article  Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

    Google Scholar 

  • Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London

    Google Scholar 

  • Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia 88:15–21

    Article  Google Scholar 

  • Libbrecht R, Gwynn DM, Fellowes MDE (2007) Aphidius ervi preferentially attacks the green morph of the pea aphid, Acyrthosiphon pisum. J Insect Behav 20:25–32

    Article  Google Scholar 

  • Lima SL (1995) Back to the basics of anti-predatory vigilance: the group-size effect. Anim Behav 49:11–20

    Article  Google Scholar 

  • Losey JE, Ives AR, Harmon J, Ballantyne F, Brown C (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388:269–272

    Article  CAS  Google Scholar 

  • Loxdale HD (2008) The nature and reality of the aphid clone: genetic variation, adaptation, and evolution. Agric For Entomol 10:81–90

    Article  Google Scholar 

  • Maynard Smith J (1978) Optimization theory in evolution. Annu Rev Ecol Syst 9:31–56

    Article  Google Scholar 

  • McFadden CS (1997) Contributions of sexual and asexual reproduction to population structure in the clonal soft coral, Alcyonium rudyi. Evolution 51:112–126

    Article  Google Scholar 

  • Michaud JP, Jyoti JL, Qureshi JA (2006) Positive correlation of fitness with group size in two biotypes of Russian wheat aphid. J Econ Entomol 99:1214–1224

    Article  PubMed  CAS  Google Scholar 

  • Mondor EB, Roitberg BD (2002) Pea aphid, Acyrthosiphon pisum, cornicle ontogeny as an adaptation to differential predation risk. Can J Zool 80:2131–2136

    Article  Google Scholar 

  • Mondor EB, Roitberg BD (2003) Age-dependent fitness costs of alarm signaling in aphids. Can J Zool 81:757–762

    Article  Google Scholar 

  • Mondor EB, Roitberg BD (2004) Inclusive fitness benefits of scent-marking predators. P Roy Soc B Biol Sci (Supp) 271:S341–S343

    Article  Google Scholar 

  • Mondor EB, Baird DS, Slessor KN, Roitberg BD (2000) Ontogeny of alarm pheromone secretion in pea aphid, Acyrthosiphon pisum. J Chem Ecol 26:2875–2882

    Article  CAS  Google Scholar 

  • Nakamuta K (1985) Mechanism of the switchover from extensive to area-concentrated search behaviour of the ladybird beetle Coccinella septempunctata bruckii. J Insect Physiol 31:849–856

    Article  Google Scholar 

  • Nault LR, Edwards LJ, Styer WE (1973) Aphid alarm pheromones: secretion and reception. Environ Entomol 2:101–105

    CAS  Google Scholar 

  • Nelson EH (2007) Predator avoidance behavior in the pea aphid: costs, frequency, and population consequences. Oecologia 151:22–32

    Article  PubMed  Google Scholar 

  • Obata S (1986) Mechanisms of prey finding in the aphidophagous ladybird beetle Harmonia axyridis (Col., Coccinellidae). Entomophaga 31:303–311

    Article  Google Scholar 

  • Obrycki JJ, Tauber MJ, Tingey WM (1983) Predator and parasitoid interaction with aphid-resistant potatoes to reduce aphid densities: a two-year field study. J Econ Entomol 76:456–462

    Google Scholar 

  • Orpwood JE, Magurran AE, Armstrong JD, Griffiths SW (2008) Minnows and the selfish herd: effects of predation risk on shoaling behavior are dependent on habitat complexity. Anim Behav 76:143–152

    Article  Google Scholar 

  • Pickett JA, Wadham LJ, Woodcock CM, Hardie J (1992) The chemical ecology of aphids. Annu Rev Entomol 37:67–90

    Article  CAS  Google Scholar 

  • Pike N, Manica A (2006) The optimal balance of defence investment strategies in clonal colonies of social aphids. Behav Ecol Sociobiol 60:803–814

    Article  Google Scholar 

  • Prasad RP, Kabaluk JT, Meberg HP, Bevon DA, Henderson DE (2009) Seasonal and spatial occurrence of aphid natural enemies in organic Brassica fields: diversity, phenology, and reproduction. J Sustain Agr 33:336–348

    Article  Google Scholar 

  • Pulliam HR, Caraco T (1984) Living in groups: is there an optimal group size? In: Krebs JR, Davies NB (eds) Behavioral ecology: An evolutionary approach. Sinauer, Sunderland, pp 122–147

    Google Scholar 

  • Ritz DA (1994) Social aggregation in pelagic invertebrates. Adv Mar Biol 30:155–216

    Article  Google Scholar 

  • Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086

    Article  Google Scholar 

  • Romey WL, Walston AR, Watt PJ (2008) Do 3-D predators attack the margins of 2-D selfish herds? Behav Ecol 19:74–78

    Article  Google Scholar 

  • SAS Institute Inc (2008) JMP 8.0—statistical discovery from SAS. SAS Institute, Cary

    Google Scholar 

  • Schmidt MH, Lauer A, Purtauf T, Thies C, Schaefer M, Tscharntke T (2003) Relative importance of predators and parasitoids for cereal aphid control. P Roy Soc B Biol Sci 270:1905–1909

    Article  Google Scholar 

  • Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton

    Google Scholar 

  • Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biological control. Ecology 84:91–107

    Article  Google Scholar 

  • Sozou PD, Seymour RM (2003) Augmented discounting: Interaction between ageing and time-preference behaviour. P Roy Soc B Biol Sci 270:1047–1053

    Article  Google Scholar 

  • Stadler B, Weisser WW, Houston AI (1994) Defence reactions in aphids: the influence of state and future reproductive success. J Anim Ecol 63:419–430

    Article  Google Scholar 

  • Sumpter DJT (2006) The principles of collective animal behaviour. Philos T Roy Soc B 361:5–22

    Article  CAS  Google Scholar 

  • Taylor LR, Woiwod IP, Perry JN (1978) The density-dependence of spatial behavior and the rarity of randomness. J Anim Ecol 47:383–406

    Article  Google Scholar 

  • Tomiuk J, Wohrmann K (1982) Comments on the stability of aphid clones. Experientia 38:320–321

    Article  Google Scholar 

  • Turchin P, Kareiva P (1989) Aggregation in Aphis varians: an effective strategy for reducing predation risk. Ecology 70:1008–1016

    Article  Google Scholar 

  • van Veen FJF, Müller CB, Pell JK, Godfray HCJ (2008) Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. J Anim Ecol 77:191–200

    Article  PubMed  Google Scholar 

  • Villagra CA, Ramirez CC, Niemeyer HM (2002) Antipredator responses of aphids to parasitoids change as a function of aphid physiological state. Anim Behav 64:677–683

    Article  Google Scholar 

  • Viscido SV, Wethey DS (2002) Quantitative analysis of fiddler crab movement: evidence for ‘selfish herd’ behaviour. Anim Behav 63:735–741

    Article  Google Scholar 

  • Volkl W, Stadler B (1996) Colony orientation and successful defence behaviour in the conifer aphid, Schizolachnus pineti. Entomol Exp Appl 78:197–200

    Article  Google Scholar 

  • Watt DJ, Mock DW (1987) A selfish herd of martins. Auk 104:342–343

    Google Scholar 

  • Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton

    Google Scholar 

  • Wilson DS (1975) A theory of group selection. P Natl Acad Sci USA 72:143–146

    Article  CAS  Google Scholar 

  • Wynne-Edwards VC (1962) Animal dispersion in relation to social behaviour. Oliver & Boyd, Edinburgh

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, Englewood Cliffs

    Google Scholar 

Download references

Acknowledgements

Laboratory assistance was provided by A. Shepard. Funding for this project was provided by the Department of Biology and Georgia Southern University.

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Correspondence to Edward B. Mondor.

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Duff, K.M., Mondor, E.B. All Clone-mates are not Created Equal: Fitness Discounting Theory Predicts Pea Aphid Colony Structure. J Insect Behav 25, 48–59 (2012). https://doi.org/10.1007/s10905-011-9275-7

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