Elsevier

Journal of Insect Physiology

Volume 98, April 2017, Pages 108-116
Journal of Insect Physiology

Thermal preference and performance in a sub-Antarctic caterpillar: A test of the coadaptation hypothesis and its alternatives

https://doi.org/10.1016/j.jinsphys.2016.12.006Get rights and content

Highlights

  • Pringleophaga marioni larvae move optimally between 20 and 25 °C.

  • Larvae Tpref is significantly lower between 4 and 5 °C.

  • Larvae survive better at lower temperatures of 5 °C compared to 10 or 15 °C.

  • We conclude that preference is rather aligned to a trait directly affecting fitness.

Abstract

Physiological ecologists have long assumed that thermoregulatory behaviour will evolve to optimise physiological performance. The coadaptation hypothesis predicts that an animal’s preferred body temperature will correspond to the temperature at which its performance is optimal. Here we use a strong inference approach to examine the relationship between thermal preference and locomotor performance in the caterpillars of a wingless sub-Antarctic moth, Pringleophaga marioni Viette (Tineidae). The coadaptation hypothesis and its alternatives (suboptimal is optimal, thermodynamic effect, trait variation) are tested. Compared to the optimal movement temperature (22.5 °C for field-fresh caterpillars and 25, 20, 22.5, 25 and 20 °C following seven day acclimations to 0, 5, 10, 15 and 5–15 °C respectively), caterpillar thermal preference was significantly lower (9.2 °C for field-fresh individuals and 9.4, 8.8, 8.1, 5.2 and 4.6 °C following acclimation to 0, 5, 10, 15 and 5–15 °C, respectively). Together with the low degree of asymmetry observed in the performance curves, and the finding that acclimation to high temperatures did not result in maximal performance, all, but one of the above hypotheses (i.e. ‘trait variation’) was rejected. The thermal preference of P. marioni caterpillars more closely resembles temperatures at which survival is high (5–10 °C), or where feeding is optimal (10 °C), than where locomotion speed is maximal, suggesting that thermal preference may be optimised for overall fitness rather than for a given trait.

Introduction

Because temperature determines the rate of most biological processes, ectotherms are usually assumed to select body temperatures that optimise performance. If fitness is positively related to performance, organisms that prefer optimum temperatures should have an advantage over those that do not (Huey and Bennett, 1987, Angilletta et al., 2002, Huey et al., 2003). In consequence, natural selection should result in similarity between the optimum and preferred temperatures because this should maximise Darwinian fitness (Martin and Huey, 2008, Anderson et al., 2011), resulting in thermal coadaptation.

Thermal coadaptation has been reported in many ectotherm taxa, including reptiles (Van Berkum, 1986, Huey and Bennett, 1987, Garland et al., 1991, Kubisch et al., 2011), insects (Sanford and Tschinkel, 1993, Forsman, 1999, Calabria et al., 2012), nematodes (Anderson et al., 2011), and fish (Khan and Herbert, 2012). Nonetheless, mismatches between thermoregulatory behaviour and thermal physiology are common. For example, in lizards, optimal locomotor performance is achieved at a higher temperature than preferred body temperatures (reviewed in Martin and Huey, 2008, Fernández et al., 2011). Similar findings for population growth have been reported for insects (Smith, 1965, Langer and Young, 1976, Allsopp et al., 1980, Allsopp, 1981, White, 1987, Jian et al., 2002) and other ectotherms (Åkesson, 1976, Zhang and Lefcort, 1991, Prevedelli and Simonini, 2001, Jia et al., 2002, Tepler et al., 2011).

Several hypotheses have been proposed to explain this departure from coadaptation, particularly when optimum temperatures are higher than preferred temperatures. First, Martin and Huey (2008) suggested that preferred temperatures should be lower than optimum temperatures (hereafter the ‘suboptimal is optimal’ hypothesis) because asymmetric performance curves mean that performance decreases rapidly above the optimum temperature (Huey and Stevenson, 1979, Huey and Kingsolver, 1989). Thus, preference should be for lower temperatures to minimise the risk of reduced performance (and possibly death) when thermoregulation is imperfect (Martin and Huey, 2008).

Second, Asbury and Angilletta (2010) hypothesised that the thermodynamic effect (i.e. poorer performance at low temperatures because biochemical reactions proceed more slowly, (Frazier et al., 2006, Angilletta et al., 2010)) means that natural selection should favour a thermal optimum that is higher than body temperature. On the basis of this thermodynamic effect, it is argued that adaptation or acclimation to warm environments should therefore confer greater performance compared to colder environments (i.e. “hotter is better”) (Angilletta, 2009, Angilletta et al., 2010). Asbury and Angilletta (2010) argued that selection driven by a thermodynamic effect could explain differences between thermoregulatory behaviour and thermal physiology. This is particularly true for the large differences between preferred temperature and the thermal optimum found in some studies (e.g. c. 8 °C for geckos (Angilletta et al., 1999) and 17 °C for marine invertebrates (Tepler et al., 2011)). We term this the ‘thermodynamic effect’ hypothesis.

We term a third hypothesis as the ‘trait variation’ hypothesis. According to this hypothesis, if optimum temperatures vary among physiological processes, then no single thermal preference will be optimal for all systems (Huey and Stevenson, 1979). In consequence, thermal preference may depend on where the major constraints for fitness lie under a given set of conditions. For example, when nutrients are plentiful, preference for high temperature in migratory locusts favours maximal growth rather than efficient utilization of nutrients, but when nutrients are limited, the preferred temperature is lowered to maximise efficiency (Miller et al., 2009, Coggan et al., 2011, Clissold et al., 2013). This hypothesis reflects the more general one that there may be differential effects of temperature on individual traits and on overall fitness, and that understanding the relationships between the adaptive value of particular traits and overall fitness is important (Kingsolver and Woods, 1997, Woods and Harrison, 2002). Moreover, these effects may take different forms depending on whether environmental temperatures are relatively constant or variable (Williams et al., 2012, Colinet et al., 2015, Kingsolver et al., 2015).

Although all of these hypotheses enjoy some empirical support, they have rarely been examined simultaneously. The strong inference approach (Platt, 1964) adopts joint exploration of alternative explanations for variations in thermal performance (Huey et al., 1999). Here, we apply this approach to caterpillars of the flightless sub-Antarctic moth, Pringleophaga marioni, for which the thermal biology is well-known (Klok and Chown, 1997, Sinclair and Chown, 2003, Sinclair et al., 2004, Sinclair and Chown, 2005, Sinclair and Chown, 2006, Haupt et al., 2014a, Haupt et al., 2014b, Haupt et al., 2016, Chown et al., 2016). Specifically, we examine the relationship between thermal preference (Tpref) and the thermal optimum (Topt) for locomotion. First, we compare Topt and Tpref. If these traits are similar, the coadaptation hypothesis cannot be rejected. If they are different, and the magnitude of this difference is relatively small and the performance curve asymmetric, the ‘suboptimal is optimal’ hypothesis cannot be rejected. Alternatively, we determine whether variation in performance curves following exposure to different acclimation regimes accords with the expectations of a thermodynamic effect (i.e. is hotter better?), thus testing the ‘thermodynamic effect’ hypothesis. Finally, we determine whether or not thermal preference aligns with performance measures other than locomotion, and specifically those that may be significant for a relatively long-lived (ca 1 year) detritivorous caterpillar (Haupt et al., 2014a). If so, and all other hypotheses are rejected, the ‘trait variation’ hypothesis cannot be rejected.

Section snippets

Study site and species

Pringleophaga marioni Viette (Tineidae) is a flightless moth, the caterpillars of which occur in virtually all habitats on the sub-Antarctic Marion and Prince Edward islands (46.9°S, 36.7°E) (Crafford et al., 1986, Haupt et al., 2014a, Haupt et al., 2016). The caterpillars are detritivores and take nearly a year to progress through this stage (Haupt et al., 2014a). Field collected caterpillars have a critical thermal minimum (CTmin) between −1.6 and 0.1 °C, and a critical thermal maximum (CTmax)

Results

The distribution of caterpillars under a constant temperature of c. 10 °C showed that caterpillars were unlikely to favour a particular end of the gradient because a similar number of individuals were found at either end, compared to the distribution of caterpillars on the c. 0–30 °C gradient where more individuals were found at one end (Fig. S5).

Excluding preferred temperatures below the upper bound we set (0.2 °C), increased the median Tpref slightly, significantly so in 0 °C acclimated

Discussion

In this study, we simultaneously tested the hypothesis of coadaptation of optimal and preferred body temperatures (Huey and Bennett, 1987, Angilletta et al., 2002, Huey et al., 2003, Angilletta, 2009), and several of its alternatives (Huey and Stevenson, 1979, Kingsolver and Woods, 1997, Martin and Huey, 2008, Asbury and Angilletta, 2010). Before doing so, we first took into account the possibility that animals may have been trapped at the low temperature end of the thermal gradient, resulting

Acknowledgments

Jennifer Lee, Justine Shaw, Asanda Phiri, Kersti Hickley and Mashudu Mashau assisted with field work. Two reviewers provided helpful comments on a previous version of the manuscript. This study was supported by National Research Foundation of South Africa Grant SNA14071475789 and the South African National Antarctic Programme.

References (75)

  • S. Slabber et al.

    Acclimation effects on the thermal tolerances of springtails from sub-Antarctic Marion Island: indigenous and invasive species

    J. Insect Physiol.

    (2007)
  • L.B. Smith

    The intrinsic rate of natural increase of Cryptolestes ferrugineus (Stephens) (Coleoptera, Cucujidae)

    J. Stored Prod. Res.

    (1965)
  • C.W. Weldon et al.

    Time-course for attainment and reversal of acclimation to constant temperature in two Ceratitis species

    J. Therm. Biol.

    (2011)
  • B. Åkesson

    Temperature and life cycle in Ophryotrocha labronica (Polychaeta, Dorvilleidae)

    Ophelia

    (1976)
  • P.G. Allsopp

    Development, longevity and fecundity of the false wireworms Pterohelaeus darlingensis and P. alternatus (Coleoptera: Tenebrionidae). I. Effect of constant temperature

    Aust. J. Zool.

    (1981)
  • P.G. Allsopp et al.

    Response of larvae of Pterohelaeus darlingensis Carter (Coleoptera: Tenebrionidae) to moisture, temperature and gravity

    Aust. J. Entomol.

    (1980)
  • J.L. Anderson et al.

    Does thermoregulatory behavior maximize reproductive fitness of natural isolates of Caenorhabditis elegans?

    BMC Evol. Biol.

    (2011)
  • J.L. Anderson et al.

    Thermal preference of Caenorhabditis elegans: a null model and empirical tests

    J. Exp. Biol.

    (2007)
  • M.J. Angilletta

    Thermal Adaptation: A Theoretical and Empirical Synthesis

    (2009)
  • M.J. Angilletta et al.

    Coadaptation: a unifying principle in evolutionary thermal biology

    Physiol. Biochem. Zool.

    (2006)
  • M.J. Angilletta et al.

    Thermodynamic effects on organismal performance: is hotter better?

    Physiol. Biochem. Zool.

    (2010)
  • M.J. Angilletta et al.

    Temperature preference in geckos: diel variation in juveniles and adults

    Herpetologica

    (1999)
  • D.A. Asbury et al.

    Thermodynamic effects on the evolution of performance curves

    Am. Nat.

    (2010)
  • G. Calabria et al.

    Hsp70 protein levels and thermotolerance in Drosophila subobscura: a reassessment of the thermal co-adaptation hypothesis

    J. Evol. Biol.

    (2012)
  • S.L. Chown et al.

    Microhabitat temperatures at Marion Island (46°54’S 37°45’E)

    S. Afr. J. Antarct. Res.

    (1992)
  • F.J. Clissold et al.

    Insect herbivores can choose microclimates to achieve nutritional homeostatis

    J. Exp. Biol.

    (2013)
  • N. Coggan et al.

    Locusts use dynamic thermoregulatory behaviour to optimize nutritional outcomes

    Proceedings of the Royal Society B

    (2011)
  • H. Colinet et al.

    Insects in fluctuating thermal environments

    Ann. Rev. Entomol.

    (2015)
  • J.E. Crafford

    Patterns of energy flow in populations of the dominant insect consumers on Marion Island

    (1990)
  • J.E. Crafford et al.

    The insects of sub-Antarctic Marion and Prince Edward Islands, with a bibliography of entomology of the Kerguelen Biogeographical Province

    S. Afr. J. Antarct. Res.

    (1986)
  • M.J. Crawley

    The R book

    (2007)
  • C.A. Darveau et al.

    Allometric cascade as a unifying principle of body mass effects on metabolism

    Nature

    (2002)
  • J.A. Deere et al.

    Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance

    Am. Nat.

    (2006)
  • W.W. Dowd et al.

    Thermal variation, thermal extremes and the physiological performance of individuals

    J. Exp. Biol.

    (2015)
  • A. Forsman

    Variation in thermal sensitivity of performance among colour morphs of a pygmy grasshopper

    J. Evol. Biol.

    (1999)
  • M.R. Frazier et al.

    Thermodynamics constraints the evolution of insect population growth rates: “Warmer is Better”

    Am. Nat.

    (2006)
  • D.D. French et al.

    A note on the feeding of Pringleophaga marioni Viette larvae at Marion Island

    S. Afr. J. Antarct. Res.

    (1983)
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