Is Phenotypic Plasticity a Key Mechanism for Responding to Thermal Stress in Ants?
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Sci Nat (2017) 104:42 DOI 10.1007/s00114-017-1464-6 ORIGINAL PAPER Is phenotypic plasticity a key mechanism for responding to thermal stress in ants? Cristela Sánchez Oms1,2 & Xim Cerdá1 & Raphaël Boulay2 Received: 24 February 2017 /Revised: 12 April 2017 /Accepted: 21 April 2017 # Springer-Verlag Berlin Heidelberg 2017 Abstract Unlike natural selection, phenotypic plasticity al- Keywords Phenotypic plasticity . Ants . Aphaenogaster lows organisms to respond quickly to changing environmental senilis . Rearing temperature . Thermal resistance . Body size 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 Introduction relationship may lead to a physiological conflict in ants, where larger body size and longer legs often confer better thermal Predicting species’ responses to global warming is one of the resistance. Here, we tested the effect of developmental tem- major challenges in ecology and evolutionary biology. Under perature (20, 24, 28 or 32 °C) on adult thermal resistance in climate change, species are expected to either modify their the thermophilic ant species Aphaenogaster senilis.Wefound distributions (Parmesan et al. 1999), acclimate (Somero that no larval development occurred at 20 °C. However, at 2010) or adapt to new environmental conditions through nat- higher temperatures, developmental speed increased as ex- ural selection (Hoffmann and Sgrò 2011). If species cannot pected and smaller adults were produced. In thermal resistance adopt one of these solutions, they are likely to rapidly go tests, we found that ants reared at 28 and 32 °C had half-lethal extinct. There are numerous examples in the literature of nat- temperatures that were 2 °C higher than those of ants reared at ural populations responding to global warming with pheno- 24 °C. Thus, although ants reared at higher temperatures were typic changes, but debate exists over whether such changes smaller in size, they were nonetheless more thermoresistant. are caused by natural selection or phenotypic plasticity These results show that A. senilis can exploit phenotypic plas- (Merilä and Hendry 2014). Unlike natural selection, which ticity to quickly adjust its thermal resistance to local condi- acts over long time spans, phenotypic plasticity allows an tions and that this process is independent of morphological organism to quickly respond to environmental conditions adaptations. This mechanism may be particularly relevant giv- without relying on genotypic modifications. Phenotypic plas- en current rapid climate warming. ticity may therefore be particularly relevant in the context of rapid global warming (Chown et al. 2007;Bergetal.2010). However, its utilisation by non-model organisms is largely Communicated by: Alain Dejean unknown and probably underestimated. Ants abound in almost all terrestrial ecosystems, where Electronic supplementary material The online version of this article they serve important ecological functions. As ectotherms, (doi:10.1007/s00114-017-1464-6) contains supplementary material, which is available to authorized users. their physiological performance is directly dependent on en- vironmental temperatures, and they may be among the species * Raphaël Boulay with the greatest sensitivity to global warming. Temperature [email protected] strongly affects many features of ant behaviour, ontogeny and ecology. For example, when faced with extreme temperatures, 1 Estación Biologica de Doñana, CSIC, Avenida Americo Vespucio ants alter daily and seasonal foraging activity as well as prey 26, 41092 Sevilla, Spain choice (Traniello et al. 1984;Marsh1985; Fernández- 2 Institute of Insect Biology, Parc de Grandmont, 37200 Tours, France Escudero and Tinaut 1998;Amoretal.2011; Jayatilaka 42 Page 2 of 7 Sci Nat (2017) 104:42 et al. 2011). Moreover, in hot habitats, there is a shift towards larvae and then measured the size and thermal resistance of the solitary foraging since high temperatures limit the efficacy of resulting adults. trail pheromones (van Oudenhove et al. 2011, 2012). Temperature is also a major structuring factor at the commu- nity level (Andersen 1995; Bestelmeyer 2000; Retana and Materials and methods Cerdá 2000; Wittman et al. 2010). In particular, in Mediterranean regions, behaviourally dominant species are Model system often heat intolerant and risk averse, while behaviourally sub- ordinate species tend to be heat tolerant and risk prone (Cerdá Aphaenogaster senilis is a thermophilic ant found in the west- et al. 1998). Thus, species-specific differences in thermotoler- ern Mediterranean basin (Cagniant and Ledoux 1974). It is ance allow local coexistence via temporal niche partitioning: strictly monogynous (Boulay et al. 2007b), and its nests con- dominant species are active at dawn and dusk, whereas sub- tain an average of 1260 ± 69 monomorphic workers (Boulay ordinate species are active around midday. In turn, this pattern et al. 2010). Fifty-seven colonies were collected in Doñana has major consequences for ant interactions with other taxa, National Park (37° 1′ N, 6° 33′ W, Huelva Province, SW including plants (Boulay et al. 2007a, 2009a). Spain) from November 2009 to March 2014. They were all Thermophilic ants have numerous adaptations that allow maintained in the same rearing room at 23 ± 2 °C, given ad them to cope with elevated temperatures (Boulay et al. libitum access to water and fed twice a week with sliced meal- 2017), including the enhanced synthesis of heat-shock pro- worms (Tenebrio molitor). teins (Gehring and Wehner 1995; Ślipiński et al. 2015), low metabolic rates and limited cuticular transpiration (Gibbs and Pomonis 1995; Cerdá and Retana 2000). In addition, in- Experimental design creased body size may greatly improve heat resistance (Cerdá and Retana 1997; Clémencet et al. 2010). First, since A total of 72 experimental groups were created; each larger insects tend to have lower surface area-to-volume ratios, contained 150 workers and 20 first-instar larvae. Forty-two larger workers have lower desiccation rates than do small of the field-collected colonies were used to create one exper- workers (Lighton and Feener 1989; Hood and Tschinkel imental group each. The other 15 colonies were large enough 1990;Kaspari1993). Second, Lighton et al. (1994)reported to create two experimental groups each. The experimental that larger ants can store more water. Third, body size is pos- groups were kept in artificial nests in glass tubes (diameter x itively associated with maximum foraging time (Lighton and length 2 × 20 cm) half-filled with water behind a cotton plug. Feener 1989) and foraging temperature (Rissing and Pollok The nests were connected to foraging arenas (length x width x 1984). Long-legged ants can distance their bodies from hot height 18 × 11.5 × 7.5 cm), whose walls were covered in surfaces and can run faster, which enhances convective Fluon to prevent the ants from escaping. The experimental cooling (Hurlbert et al. 2008; Sommer and Wehner 2012). groups were kept in environmental chambers at 20, 24, 28 In this study, we analysed how the temperatures experi- or 32 °C (18 experimental groups per condition). They were enced by larvae and pupae affected thermal resistance in maintained in complete darkness and fed a diced mealworm adults in the thermophilic species Aphaenogaster senilis twice weekly. Experimental groups created from the same (Hymenoptera: Formicidae). To date, this question has re- colonies were assigned to different treatments. ceived little attention in ants. In Camponotus rufipes, Weidenmüller et al. (2009) showed that pre-imagos exposed Data measurements to warmer temperatures had higher temperature response thresholds and temperature preferences as adult brood- The number of larvae that reached the pupal stage and the tending workers. However, insect developmental time is number of pupae of each caste (worker, male or queen) were known to be shorter when temperatures are higher and the recorded every 3 days for 103 days. A picture of each pupa result is smaller adults (Atkinson 1994; Forster and Hirst was taken, and its body length was measured to the nearest 2012). In ants, morphological traits present a high degree of 0.005 mm using ImageJ software (Schneider et al. 2012). New phenotypic plasticity (Purcell et al. 2016) and high tempera- pupae were transferred into round plastic containers (diameter tures have also been reported to reduce developmental time x height 8.5 × 4 cm); they were cared for by ten workers, (Brian 1973;Porter1988; Southerland 1988; Abril et al. which were marked with a dot of paint on their gasters to 2010). This situation could lead to a physiological conflict, distinguish them from newly emerged workers. The boxes in which warmer developmental temperatures actually reduce were connected to a glass tube (diameter x length adult thermal resistance by decreasing the average adult body 2 × 20 cm) half-filled with water behind a cotton plug. The size or by increasing its variance. To test this hypothesis, we number of pupal eclosions and the survival of the callows over examined how temperature affected developmental speed in their first 2 weeks of life were recorded. Pupae and callows Sci Nat (2017) 104:42 Page 3 of 7 42 were kept at the same treatment temperature as larvae (20, 24, dose.p function in the MASS package (Venables and Ripley 28 or 32 °C). 2002). We also determined, for each developmental tempera- The thermal resistance of the callows was estimated using ture, whether the probability of death at a given temperature half-lethal temperatures (hereafter, LT50). Randomly chosen depended on mesosoma length, leg length or the mesosoma/ ants from the same colony and temperature treatment were leg length ratio (models 9 to 11, binomial link function). placed in groups of four on an electric Plactronic Selecta hot Unless otherwise mentioned, model-adjusted means were ob- plate set to 48 °C; they remained on the hot plate for 10 min. tained and standard errors were calculated from the parameter The number of ants that died was recorded. Then, the hot plate estimates (Littell et al.