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