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Is phenotypic plasticity a key mechanism for responding to thermal stress in ants?

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Abstract

Unlike natural selection, phenotypic plasticity allows organisms to respond quickly to changing environmental conditions. However, plasticity may not always be adaptive. In insects, body size and other morphological measurements have been shown to decrease as temperature increases. This relationship may lead to a physiological conflict in ants, where larger body size and longer legs often confer better thermal resistance. Here, we tested the effect of developmental temperature (20, 24, 28 or 32 °C) on adult thermal resistance in the thermophilic ant species Aphaenogaster senilis. We found that no larval development occurred at 20 °C. However, at higher temperatures, developmental speed increased as expected and smaller adults were produced. In thermal resistance tests, we found that ants reared at 28 and 32 °C had half-lethal temperatures that were 2 °C higher than those of ants reared at 24 °C. Thus, although ants reared at higher temperatures were smaller in size, they were nonetheless more thermoresistant. These results show that A. senilis can exploit phenotypic plasticity to quickly adjust its thermal resistance to local conditions and that this process is independent of morphological adaptations. This mechanism may be particularly relevant given current rapid climate warming.

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References

  • Abril S, Oliveras J, Gómez C (2010) Effect of temperature on the development and survival of the Argentine ant, Linepithema humile. J Insect Sci 10:1–13

    Article  Google Scholar 

  • Amor F, Ortega P, Cerdá X, Boulay R (2011) Solar elevation triggers foraging activity in a thermophilic ant. Ethology 117:1031–1039

    Article  Google Scholar 

  • Andersen AN (1995) A classification of Australian ant communities, based on functional groups which parallel plant life-forms in relation to stress and disturbance. J Biogeogr 22:15–29

    Article  Google Scholar 

  • Anderson K, Munger J (2003) Effect of temperature on brood relocation in Pogonomyrmex salinus (Hymenopteria: Formicidae). Western North American Naturalist 63

  • Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268

    Article  Google Scholar 

  • Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58

    Article  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using {lme4}. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Berg MP, Kiers ET, Driessen G, van der Heijden M, Kooi BW, Kuenen F et al (2010) Adapt or disperse: understanding species persistence in a changing world. Glob Chang Biol 16:587–598

    Article  Google Scholar 

  • Bestelmeyer BT (2000) The trade-off between thermal tolerance and behavioural dominance in a subtropical South American ant community. J Anim Ecol 69:998–1009

    Article  Google Scholar 

  • Boulay R, Aron S, Cerdá X, Doums C, Graham P, Hefetz A et al (2017) Social life in arid environments: the case study of Cataglyphis ants. Annu Rev Entomol 62:13–21

    Article  Google Scholar 

  • Boulay R, Carro F, Soriguer RC, Cerdá X (2007a) Synchrony between fruit maturation and effective dispersers’ foraging activity increases seed protection against seed predators. Proc R Soc B Biol Sci 274:2515–2522

    Article  Google Scholar 

  • Boulay R, Carro F, Soriguer RC, Cerdá X (2009a) Small-scale indirect effects determine the outcome of a tripartite plant–disperser–granivore interaction. Oecologia 161:529–537

    Article  PubMed  Google Scholar 

  • Boulay R, Cerdá X, Fertin A, Ichinose K, Lenoir A (2009b) Brood development into sexual females depends on the presence of a queen but not on temperature in an ant dispersing by colony fission, Aphaenogaster senilis. Ecological Entomology 34:595–602

    Article  Google Scholar 

  • Boulay R, Galarza JA, Chéron B, Hefetz A, Lenoir A, van Oudenhove L et al (2010) Intraspecific competition affects population size and resource allocation in an ant dispersing by colony fission. Ecology 91:3312–3321

    Article  PubMed  Google Scholar 

  • Boulay R, Hefetz A, Cerdá X, Devers S, Francke W, Twele R et al (2007b) Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size. Behav Ecol Sociobiol 61:1531–1541

    Article  Google Scholar 

  • Brian MV (1973) Temperature choice and its relevance to brood survival and caste determination in the ant Myrmica rubra. Physiol Zool 46:245–252

    Article  Google Scholar 

  • Cagniant H, Ledoux A (1974) Nouvelle description d’Aphaenogaster senilis sur des exemplaires de la région de Banyuls-sur-Mer (P.-O.), France. Vie Milieu Série C 24:97–110

    Google Scholar 

  • Calabi P, Porter SD (1989) Worker longevity in the fire ant Solenopsis invicta: ergonomic considerations of correlations between temperature, size and metabolic rates. J Insect Physiol 35:643–649

    Article  Google Scholar 

  • Cerdá X, Retana J (1997) Links between worker polymorphism and thermal biology in a thermophilic ant species. Oikos 78:467–474

    Article  Google Scholar 

  • Cerdá X, Retana J (2000) Alternative strategies by thermophilic ants to cope with extreme heat: individual versus colony level traits. Oikos 89:155–163

    Article  Google Scholar 

  • Cerdá X, Retana J, Cros S (1998) Critical thermal limits in Mediterranean ant species: trade-off between mortality risk and foraging performance. Funct Ecol 12:45–55

    Article  Google Scholar 

  • Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

    Article  CAS  PubMed  Google Scholar 

  • Chown SL, Slabber S, McGeoch MA, Janion C, Leinaas HP (2007) Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proc R Soc Lond B Biol Sci 274:2531–2537

    Article  Google Scholar 

  • Clémencet J, Cournault L, Odent A, Doums C (2010) Worker thermal tolerance in the thermophilic ant Cataglyphis cursor (Hymenoptera, Formicidae). Insect Soc 57:11–15

    Article  Google Scholar 

  • Fernández-Escudero I, Tinaut A (1998) Heat-cold dialectic in the activity of Proformica longiseta, a thermophilous ant inhabiting a high mountain (Sierra Nevada, Spain). Int J Biometeorol 41:175–182

    Article  Google Scholar 

  • Forster J, Hirst AG (2012) The temperature-size rule emerges from ontogenetic differences between growth and development rates. Funct Ecol 26:483–492

    Article  Google Scholar 

  • Gehring WJ, Wehner R (1995) Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. Proc Natl Acad Sci U S A 92:2994–2998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghalambor C, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Article  Google Scholar 

  • Gibbs A, Pomonis JG (1995) Physical properties of insect cuticular hydrocarbons: the effects of chain length, methyl-branching and unsaturation. Comp Biochem Physiol B: Biochem Mol Biol 112:243–249

    Article  Google Scholar 

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    Article  CAS  PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Blackwell Science Ltd

  • Hood GW, Tschinkel WR (1990) Desiccation resistance in arboreal and terrestrial ants. Physiol Entomol 15:23–35

    Article  Google Scholar 

  • Huey RB, Stevenson R (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366

    Article  Google Scholar 

  • Hurlbert AH, Ballantyne F, Powell S (2008) Shaking a leg and hot to trot: the effects of body size and temperature on running speed in ants. Ecological Entomology 33:144–154

    Article  Google Scholar 

  • Jayatilaka P, Narendra A, Reid SF, Cooper P, Zeil J (2011) Different effects of temperature on foraging activity schedules in sympatric Myrmecia ants. J Exp Biol 214:2730–2738

    Article  PubMed  Google Scholar 

  • Kaspari M (1993) Body size and microclimate use in Neotropical granivorous ants. Oecologia 96:500–507

    Article  PubMed  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2015) Tests in linear mixed effects model. R package version 2.0–29

  • Lighton JRB, Feener DH (1989) Water-loss rate and cuticular permeability in foragers of the desert ant Pogonomyrmex rugosus. Physiol Zool 62:1232–1256

    Article  Google Scholar 

  • Lighton JRB, Quinlan MC, Feener DH (1994) Is bigger better? Water balance in the polymorphic desert harvester ant Messor pergandei. Physiol Entomol 19:325–334

    Article  Google Scholar 

  • Littell R, Milliken G, Stroup W, Wolfinger R (1996) SAS system for mixed models. SAS Institute, Cary Mehdiabadi

    Google Scholar 

  • Marsh A (1985) Thermal responses and temperature tolerance in a diurnal desert ant, Ocymyrmex barbiger. Physiol Zool 58:629–636

    Article  Google Scholar 

  • Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14

    Article  PubMed  PubMed Central  Google Scholar 

  • Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H et al (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583

    Article  CAS  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity. Beyond nature and nurture. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Porter SD (1988) Impact of temperature on colony growth and developmental rates of the ant, Solenopsis invicta. J Insect Physiol 34:1127–1133

    Article  Google Scholar 

  • Porter SD, Tschinkel WR (1993) Fire ant thermal preferences: behavioral control of growth and metabolism. Behav Ecol Sociobiol 32:321–329

    Article  Google Scholar 

  • Purcell J, Pirogan D, Avril A, Bouyarden F, Chapuisat M (2016) Environmental influence on the phenotype of ant workers revealed by common garden experiment. Behav Ecol Sociobiol 70:357–367

    Article  Google Scholar 

  • RCore-Team (2015) R: a language and environment for statistical computing

  • Retana J, Cerdá X (2000) Patterns of diversity and composition of Mediterranean ground ant communities tracking spatial and temporal variability in the thermal environment. Oecologia 123:436–444

    Article  CAS  PubMed  Google Scholar 

  • Rissing SW, Pollok GB (1984) Worker size variability and foraging efficiency in Veromessor pergandei (Hymenoptera: Formicidae). Behav Ecol Sociobiol 15:121–126

    Article  Google Scholar 

  • Roces F, Núñez J (1989) Brood translocation and circadian variation of temperature preference in the ant Camponotus mus. Oecologia 81:33–37

    Article  PubMed  Google Scholar 

  • Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60

    Article  CAS  PubMed  Google Scholar 

  • RStudio-Team (2016) RStudio: integrated development environment for R

  • Ruel C, Cerdá X, Boulay R (2012) Behaviour-mediated group size effect constrains reproductive decisions in a social insect. Anim Behav 84:853–860

    Article  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  Google Scholar 

  • Ślipiński P, Pomorski JJ, Kowalewska K (2015) Heat shock proteins expression during thermal risk exposure in the temperate xerothermic ant Formica cinerea. Sociobiology 62:457

    Article  Google Scholar 

  • Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers.”. J Exp Biol 213:912–920

    Article  CAS  PubMed  Google Scholar 

  • Sommer S, Wehner R (2012) Leg allometry in ants: extreme long-leggedness in thermophilic species. Arthropod Structure & Development 41:71–77

    Article  Google Scholar 

  • Southerland MT (1988) The effects of temperature and food on the growth of laboratory colonies of Aphaenogaster rudis Emery (Hymenoptera: Formicidae). Insect Soc 35:304–309

    Article  Google Scholar 

  • Traniello JFA, Fujita MS, Bowen RV (1984) Ant foraging behavior: ambient temperature influences prey selection. Behav Ecol Sociobiol 15:65–68

    Article  Google Scholar 

  • van Oudenhove L, Billoir E, Boulay R, Bernstein C, Cerdá X (2011) Temperature limits trail following behaviour through pheromone decay in ants. Naturwissenschaften 98:1009–1017

    Article  CAS  PubMed  Google Scholar 

  • van Oudenhove L, Boulay R, Lenoir A, Bernstein C, Cerdá X (2012) Substrate temperature constrains recruitment and trail following behavior in ants. J Chem Ecol 38:802–809

    Article  PubMed  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, for the MASS package

  • Villalta I, Angulo E, Devers S, Cerdá X, Boulay R (2015) Regulation of worker egg laying by larvae in a fission-performing ant. Anim Behav 106:149–156

    Article  Google Scholar 

  • Waddington C (1953) Genetic assimilation of an acquired character. Evolution 7:118–126

    Article  Google Scholar 

  • Weidenmüller A, Mayr C, Kleineidam CJ, Roces F (2009) Preimaginal and adult experience modulates the thermal response behavior of ants. Curr Biol 19:1897–1902

    Article  PubMed  Google Scholar 

  • West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. Proc Natl Acad Sci U S A 102:6543–6549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wittman SE, Sanders NJ, Ellison AM, Jules ES, Ratchford JS, Gotelli NJ (2010) Species interactions and thermal constraints on ant community structure. Oikos 119:551–559

    Article  Google Scholar 

  • Zeilstra I, Fischer C (2005) Cold tolerance in relation to developmental and adult temperature in a butterfly. Physiol Entomol 30:92–95

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Acknowledgements

Cristela Sanchez Oms was supported by a PhD grant co-funded by the Centre regional government and the French Ministry of Higher Education and Research. Part of this work was supported by CNRS funds (PICS: 24698).

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Authors and Affiliations

  1. Estación Biologica de Doñana, CSIC, Avenida Americo Vespucio 26, 41092, Sevilla, Spain

    Cristela Sánchez Oms & Xim Cerdá

  2. Institute of Insect Biology, Parc de Grandmont, 37200, Tours, France

    Cristela Sánchez Oms & Raphaël Boulay

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  1. Cristela Sánchez Oms
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  2. Xim Cerdá
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Correspondence to Raphaël Boulay.

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Communicated by: Alain Dejean

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Oms, C.S., Cerdá, X. & Boulay, R. Is phenotypic plasticity a key mechanism for responding to thermal stress in ants?. Sci Nat 104, 42 (2017). https://doi.org/10.1007/s00114-017-1464-6

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