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Disengtangling the evolution of weak warning signals: high detection risk and low production costs of chemical defences in gregarious pine sawfly larvae

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Abstract

Evolution of costly secondary defences for a cryptic prey is puzzling, if the prey is already well protected by camouflage. However, if the chemical defence is not sufficient to deter all predators, selection can favour low signal intensity in defended prey. Alternatively, if the costs of chemical defence are low or cost-free, chemical defences can be expected to evolve also for non-signalling prey, particularly if conspicuous signalling is costly. We tested these assumptions with pine sawfly larvae (Neodiprion sertifer and Diprion pini) that are cryptically coloured and chemically defended with resin acids sequestered from their host plant (Pinus sp.). Larvae feed in large aggregations, which we hypothesise could function as a signal of unprofitability. Our results show that even though the birds found N. sertifer larvae unprofitable in the controlled laboratory assays, they continued attacking and consuming them in the wild. When we tested the signal value of aggregation we found that a large group size did not offer protection for a defended larva: the survival was higher in groups of 10 individuals compared to groups of 50, suggesting increased detectability costs for individuals in larger groups. Finally, we tested how costly the production and maintenance of a chemical defence is for D. pini larvae by manipulating the resin acid content of the diet. We did not find any life history or immunological costs of the chemical defence for the larvae. In contrast, pupal weights were higher on the high resin diet than on the low resin diet. Also, larvae were able to produce higher amounts of defence fluids on the high diet than on the low diet. Thus, our result suggests high detectability costs and low production costs of defences could explain why some unprofitable species have not evolved conspicuous signals.

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References

  • Alatalo R, Mappes J (1996) Tracking the evolution of warning signals. Nature 382:708–710

    Article  CAS  Google Scholar 

  • Aldrich JR, Blum MS (1978) Aposematic aggregation of a bug (Hemiptera: Coreidae): The defensive display and formation of aggregations. Biotropica 10:58–61

    Article  Google Scholar 

  • Aukema BH, Raffa KF (2004) Does aggregation benefit bark beetles by diluting predation? Links between a group-colonisation strategy and the absence of emergent multiple predator effects. Ecol Entomol 29:129–138

    Article  Google Scholar 

  • Barnett CA, Bateson M, Rowe C (2007) State-dependent decision making: educated predators strategically trade off the costs and benefits of consuming aposematic prey. Behav Ecol 18:645–651

    Article  Google Scholar 

  • Beatty CD, Roderick SB, Sherratt TN (2005) The evolution of aggregation in profitable and unprofitable prey. Anim Behav 70:199–208

    Article  Google Scholar 

  • Björkman C, Larsson S (1991) Pine sawfly defence and variation in host plant resin acids: a trade-off with growth. Ecol Entomol 16:283–289

    Article  Google Scholar 

  • Björkman C, Larsson S, Gref R (1991) Effects of nitrogen fertilization on pine needle chemistry and sawfly performance. Oecologia 86:202–209

    Article  Google Scholar 

  • Björkman C, Larsson S, Bommarco R (1997) Oviposition preferences in pine sawflies: a trade-off between larval growth and defence against natural enemies. Oikos 79:45–52

    Article  Google Scholar 

  • Blount JD, Speed MP, Ruxton G, Stephens PA (2009) Warning displays may function as honest signals of toxicity. Proc R Soc Lond B 276:871–877

    Article  Google Scholar 

  • Camara MD (1997) Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hübner (Nymphalidae): a gravimetric and quantitative genetic analysis. Evol Ecol 11:451–469

    Article  Google Scholar 

  • Casey TM, Knapp R (1987) Caterpillar thermal adaptation: behavioural differences reflect metabolic thermal sensitivities. Comp Biochem Physiol 86A:679–682

    Article  Google Scholar 

  • Codella SG, Raffa KF (1995a) Host plant influence on chemical defense in conifer sawflies (Hymenoptera: Diprionidae). Oecologia 104:1–11

    Article  Google Scholar 

  • Codella SG, Raffa KF (1995b) Contributions of female oviposition patterns and larval behaviour to group defense in conifer sawflies (Hymenoptera: Diprionidae). Oecologia 103:24–33

    Article  Google Scholar 

  • Codella SG, Raffa KF (1996) Individual and social components of wood ant response to conifer sawfly defence (Hymenoptera: Formicidae, Diprionidae). Anim Behav 52:801–811

    Article  Google Scholar 

  • Cook JM (1997) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421–435

    Article  Google Scholar 

  • Cott HB (1940) Adaptive colouration in animals. Methuen, London

    Google Scholar 

  • Cotter SC, Hails RS, Cory JS, Wilson K (2004) Density-dependent prophylaxis and condition-dependent immune function in Lepidopteran larvae: a multivariate approach. J Anim Ecol 73:283–293

    Article  Google Scholar 

  • Darst CR, Cummings ME, Cannatella DC (2006) A mechanism for diversity in warning signals: conspicuousness versus toxicity in poison frogs. PNAS 103:5852–5857

    Article  PubMed  CAS  Google Scholar 

  • Del Campo M, Smedley SR, Eisner T (2005) Reproductive benefits derived from defensive plant alkaloid possession in an Arctiid moth (Utetheisa ornatrix). PNAS 102:13508–13512

    Article  PubMed  CAS  Google Scholar 

  • Eisner T, Johnessee JS, Carrel J (1974) Defensive use by an insect of a plant resin. Science 184:996–999

    Article  PubMed  CAS  Google Scholar 

  • Endler JA (1991) Interactions between predators and prey. In: Krebs JR, Davies NB (eds) Behavioural ecology. An evolutionary approach. Blackwell Science, Cambridge, pp 169–196

    Google Scholar 

  • Endler JA, Mappes J (2004) Predator mixes and the conspicuousness of aposematic signals. Am Nat 163:532–547

    Article  PubMed  Google Scholar 

  • Exnerová A, Svadová K, Štys P, Barcalová S, Landová E, Prokopová M, Fuchs R, Socha R (2006) Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera). Biol J Linn Soc 88:143–153

    Article  Google Scholar 

  • Fischer S, Samietz J, Wäckers FL, Dorn S (2001) Interaction of vibrational and visual cues in parasitoid host location. J Comp Physiol A 187:785–791

    Article  PubMed  CAS  Google Scholar 

  • Forsman A, Merilaita S (1999) Fearful symmetry: pattern size and asymmetry affects aposematic signal efficacy. Evol Ecol 13:131–140

    Article  Google Scholar 

  • Friman V, Lindstedt C, Hiltunen T, Laakso J, Mappes J (2009) Predation on multiple trophic levels shapes the evolution of pathogen virulence. PLoS ONE 4(8):e6761

    Article  PubMed  Google Scholar 

  • Gagliardo A, Guilford T (1993) Why do warning coloured prey live gregariously? Proc R Soc Lond Ser B 286:149–150

    Google Scholar 

  • Gamberale-Stille G (2000) Decision time and prey gregariousness influence attack probability in naive and experienced predators. Anim Behav 60:95–99

    Google Scholar 

  • Gamberale G, Sillén-Tullberg B (1998) Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence. Proc R Soc Lond B 265:889–894

    Article  Google Scholar 

  • Gamberale G, Tullberg BS (1996) Evidence for a more effective signal in aggregated aposematic prey. Anim Behav 52:597–601

    Article  Google Scholar 

  • Gamberale-Stille G, Tullberg B (1999) Experienced chicks show biased avoidance of stronger signals: an experiment with natural colour variation in live aposematic prey. Evol Ecol 13:579–589

    Article  Google Scholar 

  • Gentry GL, Dyer LA (2002) On the conditional nature of Neotropical caterpillar defences against their natural enemies. Ecology 83:3108–3119

    Article  Google Scholar 

  • Grill CP, Moore AJ (1998) Effects of a larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle. Oecologia 114:274–282

    Article  Google Scholar 

  • Hagman M, Forsman A (2003) Correlated evolution of conspicuous colouration and body size in poison frogs (Dendrobatidae). Evolution 57:2904–2910

    PubMed  Google Scholar 

  • Ham AD, Ihalainen E, Lindström L, Mappes J (2006) Does colour matter? The importance of colour in avoidance learning, memorability and generalisation. Behav Ecol Sociobiol 60:482–491

    Article  Google Scholar 

  • Harvey JA, van Nouhuys S, Biere A (2005) Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. J Chem Ecol 31:287–302

    Article  PubMed  CAS  Google Scholar 

  • Hedlund K, Vet LEM, Dicke M (1996) Generalist and specialist parasitoid strategies of using odours of adult drosophilid flies when searching for larval hosts. Oikos 77:390–398

    Article  Google Scholar 

  • Heimpel GE, de Boer JG (2008) Sex determination in Hymenoptera. Annu Rev Entomol 53:209–230

    Article  PubMed  CAS  Google Scholar 

  • Herz A, Heitland W (1999) Larval parasitism of a forest pest, the common pine sawfly Diprion pini (L.) (HYM., Diprionidae), during an endemic density phase. J Appl Ent 123:129–137

    Article  Google Scholar 

  • Holloway GJ, de Jong P, Brakefield PM, de Vos H (1991) Chemical defence in ladybird beetles (Coccinellidae). I. Distribution of coccinelline and individual variation in defence in 7-spot ladybirds (Coccinella septempunctata). Chemoecology 2:7–14

    Article  CAS  Google Scholar 

  • Holloway GJ, de Jong PW, Ottenheim M (1993) The genetics and cost of chemical defence in the 2-spot ladybird (Adalia bipunctata L.). Evolution 47:1229–1239

    Article  Google Scholar 

  • Holloway GJ, Gilbert F, Brandt A (2001) The relationship between mimetic imperfection and phenotypic variation in insect colour patterns. Proc R Soc Lond B 269:411–416

    Article  Google Scholar 

  • Hunter AF (2000) Gregariousness and repellent defences in the survival of phytophagous insects. Oikos 91:213–224

    Article  Google Scholar 

  • Kalin M, Knerer G (1977) Group and mass effects in diprionid sawflies. Nature 267:427–429

    Article  Google Scholar 

  • Klemola N, Klemola T, Rantala MJ, Ruuhola T (2007) Natural host-plant quality affects immune defence of an insect herbivore. Entomol Exp Appl 123:167–176

    Article  CAS  Google Scholar 

  • Koskimäki J, Rantala MJ, Taskinen J, Tynkkynen K, Suhonen J (2004) Immunocompetence and resource holding potential in the damselfly, Calopteryx virgo L. Behav Ecol 15:169–173

    Article  Google Scholar 

  • Larsson S, Björkman C, Gref R (1986) Responses of Neodiprion sertifer (Hym., Diprionidae) larvae to variation in needle resin acid concentration in Scots pine. Oecologia 70:77–84

    Article  Google Scholar 

  • Larsson S, Lundgren L, Ohmart CP, Gref R (1992) Weak responses of pine sawfly larvae to high needle flavonoid concentrations in scots pine. J Chem Ecol 18:271–282

    Article  CAS  Google Scholar 

  • Larsson S, Ekbom B, Björkman C (2000) Influence of plant quality on pine sawfly population dynamics. Oikos 89:440–450

    Article  Google Scholar 

  • Lawrence WS (1990) The efects of group size and host species on development and survivorship of a gregarious caterpillar Halisidota caryae (Lepidoptera: Arctiidae). Eco Entomol 15:53–62

    Article  Google Scholar 

  • Leimar O, Enquist M, Sillén-Tullberg B (1986) Evolutionary stability of aposematic coloration and prey unprofitability: a theoretical analysis. Am Nat 128:469–490

    Article  Google Scholar 

  • Lindstedt C, Mappes J, Päivinen J, Varama M (2006) Effects of group size and pine defence chemicals on Diprionid sawfly survival against ant predation. Oecologia 150:519–526

    Article  PubMed  Google Scholar 

  • Lindstedt C, Lindström L, Mappes J (2008) Hairiness and warning colours as components of antipredator defence: additive or interactive benefits? Anim Behav 75:1703–1713

    Article  Google Scholar 

  • Lindstedt C, Lindström L, Mappes J (2009a) Thermoregulation constrains effective warning signal expression. Evolution 63:469–478

    Article  PubMed  Google Scholar 

  • Lindstedt C, Reudler Talsma J, Ihalainen E, Lindström L, Mappes J (2009b) Diet quality affects coloration indirectly: excretion costs in a generalist herbivore. Evolution 64:68–78

    Article  PubMed  Google Scholar 

  • Lindström L, Alatalo R, Mappes J, Riipi M, Vertainen L (1999) Can aposematic signals evolve by gradual change? Nature 397:249–251

    Article  Google Scholar 

  • Lindström L, Alatalo R, Lyytinen A, Mappes J (2001) Strong antiapostatic selection against novel rare aposematic prey. PNAS 98:9181–9184

    Article  PubMed  Google Scholar 

  • Lindström L, Alatalo RV, Lyytinen A, Mappes J (2004) The effect of alternative prey on the dynamics of Batesian and Müllerian mimicries. Evolution 58:1294–1302

    PubMed  Google Scholar 

  • Longson CG, Joss JMP (2006) Optimal toxicity in animals: predicting the optimal level of chemical defences. Func Ecol 20:731–735

    Article  Google Scholar 

  • Mappes J, Alatalo RV (1997) Effect of novelty and gregariousness in survival of aposematic prey. Behav Ecol 8:174–177

    Article  Google Scholar 

  • Mappes J, Marples N, Endler J (2005) The complex business of survival by aposematism. TREE 20:598–603

    PubMed  Google Scholar 

  • Marshall NJ (2000) Communication and camouflage with the same ‘bright’ colours in reef fishes. Phil Trans R Soc B 355:1243–1248

    Article  PubMed  CAS  Google Scholar 

  • Mattiacci L, Hütter E, Schoch D, Scascighini N, Dorn S (2000) Plant-odour mediates parasitoid host handling and oviposition in an endophytic tritrophic system. Chemoecology 10:185–192

    Article  Google Scholar 

  • Merilaita S, Kaitala V (2002) Community structure and the evolution of aposematic colouration. Ecol Lett 5:495–501

    Article  Google Scholar 

  • Merilaita S, Ruxton G (2007) Aposematic signals and the relationship between conspicuousness and distinctiveness. J Theor Biol 245:268–287

    Article  PubMed  Google Scholar 

  • Mopper S, Whitham TG, Price PW (1990) Plant phenotype and interspecific competition between insects determine sawfly performance and density. Ecology 71(6):2135–2144

    Article  Google Scholar 

  • Nilsson M, Forsman A (2003) Evolution of conspicuous colouration, body size and gregariousness: a comparative analysis of Lepidopteran larvae. Evol Ecol 17:51–66

    Article  Google Scholar 

  • Ojala K, Julkunen-Tiitto R, Lindström L, Mappes J (2005) Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evol Ecol Res 7:1153–1170

    Google Scholar 

  • Ojala K, Lindström L, Mappes J (2007) Life history constraints and warning signal expression in arctiid moth. Func Ecol 21:1162–1167

    Article  Google Scholar 

  • Poulton EB (1890) The colours of animals: their meaning and use especially considered in the case of insects (Edn 2), xiii, Kegan Paul, Trench, Trubner and co., London

  • Powell W, Pennacchio F, Poppy GM, Tremblay E (1998) Strategies involved in the location of hosts by the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae). Biol Control 11:104–112

    Article  Google Scholar 

  • Prop N (1960) Protection against birds and parasites in some species of tenthredinid larvae. Arch Neerl Zool 13:380–447

    Article  Google Scholar 

  • Rantala MJ, Koskimäki J, Taskinen J, Tynkkynen K (2000) Immunocompetence developmental stability and wing spot size in Calopteryx splendens L. Proc R Soc Lond B 267:2453–2457

    Article  CAS  Google Scholar 

  • Reader T, Hochuli DF (2003) Understanding gregariousnees in a larval lepidoteran: the roles of host plant, predation and microclimate. Ecol Ent 28(6):729–737

    Article  Google Scholar 

  • Riipi M, Alatalo R, Lindström L, Mappes J (2001) Multiple benefits of gregariousness cover detectability costs in aposematic aggregations. Nature 413:512–514

    Article  PubMed  CAS  Google Scholar 

  • Roque-Albelo L, Schroeder FC, Conner WE, Bezzerides A, Hoebeke ER, Meinwald J, Eisner T (2002) Chemical defence and aposematism: the case of Utetheisa galapagensis. Chemoecology 12:153–157

    Article  CAS  Google Scholar 

  • Rowe C, Lindström L, Lyytinen A (2004) The importance of pattern similarity between Müllerian mimics in predator avoidance learning. Proc R Soc Lond B 271:407–413

    Article  Google Scholar 

  • Rowland HM, Ihalainen E, Lindström L, Mappes J, Speed MP (2007) Co-mimics have a mutualistic relationship despite unequal defence levels. Nature 448:64–66

    Article  PubMed  CAS  Google Scholar 

  • Ruxton GD, Sherrat TN (2006) Aggregation, defence and warning signals: the evolutionary relationship. Proc R Soc Lond B 273:2417–2424

    Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. Evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, New York

    Google Scholar 

  • Ruxton GD, Speed MP, Broom M (2009) Identifying the ecological conditions that select for intermediate levels of aposematic signalling. Evol Ecol 23:491–501

    Article  Google Scholar 

  • Ryder JJ, Siva-Jothy MT (2000) Male calling song provides a reliable signal of immune function in a cricket. Proc R Soc Lond B 267:1171–1175

    Article  CAS  Google Scholar 

  • Saastamoinen M, van Nouhuys S, Nieminen M, O’Hara B, Suomi J (2007) Development and survival of a specialist herbivore, Melitaea cinxia, on host plants producing high and low concentrations of iridoid glycosides. Ann Zool Fenn 44:70–80

    Google Scholar 

  • Sandre SL, Stevens M, Mappes J (2010) The effect of predator appetite, prey warning coloration and luminance on predator foraging decisions. Behaviour 147:1121–1143

    Article  Google Scholar 

  • Seymour RS (1979) Convective and evaporative cooling in sawfly larvae. J Insect Physiol 20:2447–2457

    Article  Google Scholar 

  • Sherratt TN, Beatty CD (2003) The evolution of warning signals as reliable indicators of prey defence. Am Nat 162:377–389

    Article  PubMed  Google Scholar 

  • Sillén-Tullberg B (1985) Higher survival of an aposematic than of a cryptic form of a distasteful bug. Oecologia 67:411–415

    Article  Google Scholar 

  • Sillén-Tullberg B (1990) Do predators avoid groups of aposematic prey? An experimental test. Anim Behav 40:856–860

    Article  Google Scholar 

  • Sillén-Tullberg B, Leimar O (1988) The evolution of gregariousness in distasteful insects as a defence against predators. Am Nat 132:723–734

    Article  Google Scholar 

  • Skelhorn J, Rowe C (2006a) Prey palatability influences predator learning and memory. Anim Behav 71:1111–1118

    Article  Google Scholar 

  • Skelhorn J, Rowe C (2006b) Predator avoidance learning of prey with secreted or stored defences and the evolution of insect defences. Anim Behav 72:827–834

    Article  Google Scholar 

  • Skelhorn J, Ruxton GD (2006) Avian predators attack aposematic prey more forcefully when they are part of an aggregation. Biol Lett 2:488–490

    Article  PubMed  Google Scholar 

  • Skelhorn J, Griksaitis D, Rowe C (2008) Colour biases are more than a question of taste. Anim Behav 75:827–835

    Article  Google Scholar 

  • Speed M, Ruxton G (2007) How bright and how nasty: explaining diversity in warning signal strength. Evolution 61:623–635

    Article  PubMed  Google Scholar 

  • Speed M, Brockhurst MA, Ruxton GD (2010) Dual benefits of aposematism: predator avoidance and enhanced resource collection. Evolution 23:207–211

    Google Scholar 

  • Stevens M, Merilaita S (2009) Defining disruptive coloration and distinguishing its functions. Phil Trans R Soc B 364:481–488

    Article  PubMed  Google Scholar 

  • Tullberg B, Leimar O, Gamberale-Stille G (2000) Did aggregation favour the initial evolution of warning coloration? A novel world revisited. Anim Beh 59:281–287

    Article  Google Scholar 

  • Tullberg BS, Merilaita S, Wiklund C (2005) Aposematism and crypsis combined as a result of distance dependence: functional versatility of the colour pattern in the swallowtail butterfly larva. Proc R Soc Lond B 272:1315–1321

    Article  Google Scholar 

  • Turner JRG, Speed MP (1999) How weird can mimicry get? Evol Ecol 13:807–827

    Article  Google Scholar 

  • Wilson K, Reeson AS (1998) Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions? Ecol Entomol 23:100–101

    Article  Google Scholar 

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Acknowledgments

We thank UPM Kymmene, Stora Enso and landowners in Konnevesi-area for provision of study areas. We also thank Sheena Cotter who kindly commented the text and Ville Friman for helping with analyses. This study was financed by the Academy of Finland (Finnish Centres of Excellence in Evolutionary Ecology and Evolutionary Research), Societas Biologica Fennica Vanamo 2002 and Luonnon Ystäväin Yhdistys ry of Kuopio.

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Lindstedt, C., Huttunen, H., Kakko, M. et al. Disengtangling the evolution of weak warning signals: high detection risk and low production costs of chemical defences in gregarious pine sawfly larvae. Evol Ecol 25, 1029–1046 (2011). https://doi.org/10.1007/s10682-010-9456-4

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