John S. Terblanche

Physiological Diversity in Insects: Ecological and Evolutionary Contexts.

Publisher Summary This chapter discusses the modern ecological and evolutionary contexts of the evolutionary physiology in insects and provides a survey of sources of environmental variability and their effects on insect populations. The chapter explores environmental variation and the various ways in which it may be quantified. Some environmental variables are relatively simple and straightforward, both to measure and to control, whereas others pose substantially greater problems from both perspectives. Even variables that are seemingly easy to measure might act in ways that are difficult to identify. The chapter examines insect responses to the thermal environment over a variety of spatial and temporal scales, focusing on recent developments in the field. The importance of water availability for insect survival and the determination of distribution and abundance patterns have been widely demonstrated. The chapter considers the question of what lessons insect evolutionary physiologists might have to offer ecology and conservation biology. In particular, how evolutionary physiology can offer ecologists a set of useful general rules in some cases and can unveil the nature of local contingency in others.

Critical thermal limits depend on methodological context

A full-factorial study of the effects of rates of temperature change and start temperatures was undertaken for both upper and lower critical thermal limits (CTLs) using the tsetse fly, Glossina pallidipes. Results show that rates of temperature change and start temperatures have highly significant effects on CTLs, although the duration of the experiment also has a major effect. Contrary to a widely held expectation, slower rates of temperature change (i.e. longer experimental duration) resulted in poorer thermal tolerance at both high and low temperatures. Thus, across treatments, a negative relationship existed between duration and upper CTL while a positive relationship existed between duration and lower CTL. Most importantly, for predicting tsetse distribution, G. pallidipes suffer loss of function at less severe temperatures under the most ecologically relevant experimental conditions for upper (0.06°C min−1; 35°C start temperature) and lower CTL (0.06°C min−1; 24°C start temperature). This suggests that the functional thermal range of G. pallidipes in the wild may be much narrower than previously suspected, approximately 20–40°C, and highlights their sensitivity to even moderate temperature variation. These effects are explained by limited plasticity of CTLs in this species over short time scales. The results of the present study have broad implications for understanding temperature tolerance in these and other terrestrial arthropods.

Ecologically relevant measures of tolerance to potentially lethal temperatures

Summary The acute thermal tolerance of ectotherms has been measured in a variety of ways; these include assays where organisms are shifted abruptly to stressful temperatures and assays where organisms experience temperatures that are ramped more slowly to stressful levels. Ramping assays are thought to be more relevant to natural conditions where sudden abrupt shifts are unlikely to occur often, but it has been argued that thermal limits established under ramping conditions are underestimates of true thermal limits because stresses due to starvation and/or desiccation can arise under ramping. These confounding effects might also impact the variance and heritability of thermal tolerance. We argue here that ramping assays are useful in capturing aspects of ecological relevance even though there is potential for confounding effects of other stresses that can also influence thermal limits in nature. Moreover, we show that the levels of desiccation and starvation experienced by ectotherms in ramping assays will often be minor unless the assays involve small animals and last for many hours. Empirical data illustrate that the combined effects of food and humidity on thermal limits under ramping and sudden shifts to stressful conditions are unpredictable; in Drosophila melanogaster the presence of food decreased rather than increased thermal limits, whereas in Ceratitis capitata they had little impact. The literature provides examples where thermal limits are increased under ramping presumably because of the potential for physiological changes leading to acclimation. It is unclear whether heritabilities and population differentiation will necessarily be lower under ramping because of confounding effects. Although it is important to clearly define experimental methods, particularly when undertaking comparative assessments, and to understand potential confounding effects, thermotolerance assays based on ramping remain an important tool for understanding and predicting species responses to environmental change. An important area for further development is to identify the impact of rates of temperature change under field and laboratory conditions.

Insect thermal tolerance: what is the role of ontogeny, ageing and senescence?

Temperature has dramatic evolutionary fitness consequences and is therefore a major factor determining the geographic distribution and abundance of ectotherms. However, the role that age might have on insect thermal tolerance is often overlooked in studies of behaviour, ecology, physiology and evolutionary biology. Here, we review the evidence for ontogenetic and ageing effects on traits of high‐ and low‐temperature tolerance in insects and show that these effects are typically pronounced for most taxa in which data are available. We therefore argue that basal thermal tolerance and acclimation responses (i.e. phenotypic plasticity) are strongly influenced by age and/or ontogeny and may confound studies of temperature responses if unaccounted for. We outline three alternative hypotheses which can be distinguished to propose why development affects thermal tolerance in insects. At present no studies have been undertaken to directly address these options. The implications of these age‐related changes in thermal biology are discussed and, most significantly, suggest that the temperature tolerance of insects should be defined within the age‐demographics of a particular population or species. Although we conclude that age is a source of variation that should be carefully controlled for in thermal biology, we also suggest that it can be used as a valuable tool for testing evolutionary theories of ageing and the cellular and genetic basis of thermal tolerance.

Macrophysiology: A Conceptual Reunification

Widespread recognition of the importance of biological studies at large spatial and temporal scales, particularly in the face of many of the most pressing issues facing humanity, has fueled the argument that there is a need to reinvigorate such studies in physiological ecology through the establishment of a macrophysiology. Following a period when the fields of ecology and physiological ecology had been regarded as largely synonymous, studies of this kind were relatively commonplace in the first half of the twentieth century. However, such large‐scale work subsequently became rather scarce as physiological studies concentrated on the biochemical and molecular mechanisms underlying the capacities and tolerances of species. In some sense, macrophysiology is thus an attempt at a conceptual reunification. In this article, we provide a conceptual framework for the continued development of macrophysiology. We subdivide this framework into three major components: the establishment of macrophysiological patterns, determining the form of those patterns (the very general ways in which they are shaped), and understanding the mechanisms that give rise to them. We suggest ways in which each of these components could be developed usefully.

Water loss in insects: An environmental change perspective

In the context of global environmental change much of the focus has been on changing temperatures. However, patterns of rainfall and water availability have also been changing and are expected to continue doing so. In consequence, understanding the responses of insects to water availability is important, especially because it has a pronounced influence on insect activity, distribution patterns, and species richness. Here we therefore provide a critical review of key questions that either are being or need to be addressed in this field. First, an overview of insect behavioural responses to changing humidity conditions and the mechanisms underlying sensing of humidity variation is provided. The primary sensors in insects belong to the temperature receptor protein superfamily of cation channels. Temperature-activated transient receptor potential ion channels, or thermoTRPs, respond to a diverse range of stimuli and may be a primary integrator of sensory information, such as environmental temperature and moisture. Next we touch briefly on the components of water loss, drawing attention to a new, universal model of the water costs of gas exchange and its implications for responses to a warming, and in places drying, world. We also provide an overview of new understanding of the role of the sub-elytral chamber for water conservation, and developments in understanding of the role of cuticular hydrocarbons in preventing water loss. Because of an increasing focus on the molecular basis of responses to dehydration stress we touch briefly on this area, drawing attention to the role of sugars, heat shock proteins, aquaporins, and LEA proteins. Next we consider phenotypic plasticity or acclimation responses in insect water balance after initial exposures to altered humidity, temperature or nutrition. Although beneficial acclimation has been demonstrated in several instances, this is not always the case. Laboratory studies show that responses to selection for enhanced ability to survive water stress do evolve and that genetic variation for traits underlying such responses does exist in many species. However, in others, especially tropical, typically narrowly distributed species, this appears not to be the case. Using the above information we then demonstrate that habitat alteration, climate change, biological invasions, pollution and overexploitation are likely to be having considerable effects on insect populations mediated through physiological responses (or the lack thereof) to water stress, and that these effects may often be non-intuitive.

Insect Rate‐Temperature Relationships: Environmental Variation and the Metabolic Theory of Ecology

Much of the recent discussion concerning the form and underlying mechanistic basis of metabolic rate–temperature and development rate–temperature relationships has been precipitated by the development of the metabolic theory of ecology (MTE). Empirical tests of the theory’s fundamental equation are an essential component of establishing its validity. Here, we test the temperature component of the fundamental equation of the MTE as it applies to metabolic rate and development rate, using insects as model organisms. Specifically, we test (i) whether mean activation energies, E, approximate the 0.65 eV value proposed by the proponents of the MTE and whether the range of values is tightly constrained between 0.6 and 0.7 eV, as they have argued; (ii) whether phylogenetic signal is apparent in the rate‐temperature relationships; (iii) whether the slopes of the rate‐temperature relationships show consistent, directional variation associated with environmental variables; and (iv) whether intra‐ and interspecific rate‐temperature relationships differ significantly. Because the majority of activation energy values fell outside the predicted range and rate‐temperature relationships showed consistent directional variation correlated with large‐scale climatic variation, we conclude that data from insects provide only limited support for the MTE. In consequence, we consider alternative explanations for variation in rate‐temperature relationships.

Insect gas exchange patterns: A phylogenetic perspective

SUMMARY Most investigations of insect gas exchange patterns and the hypotheses proposed to account for their evolution have been based either on small-scale, manipulative experiments, or comparisons of a few closely related species. Despite their potential utility, no explicit, phylogeny-based, broad-scale comparative studies of the evolution of gas exchange in insects have been undertaken. This may be due partly to the preponderance of information for the endopterygotes, and its scarcity for the apterygotes and exopterygotes. Here we undertake such a broad-scale study. Information on gas exchange patterns for the large majority of insects examined to date (eight orders, 99 species) is compiled, and new information on 19 exemplar species from a further ten orders, not previously represented in the literature (Archaeognatha, Zygentoma, Ephemeroptera, Odonata, Mantodea, Mantophasmatodea, Phasmatodea, Dermaptera, Neuroptera, Trichoptera), is provided. These data are then used in a formal, phylogeny-based parsimony analysis of the evolution of gas exchange patterns at the order level. Cyclic gas exchange is likely to be the ancestral gas exchange pattern at rest (recognizing that active individuals typically show continuous gas exchange), and discontinuous gas exchange probably originated independently a minimum of five times in the Insecta.

Evolutionary responses of discontinuous gas exchange in insects

The discontinuous gas-exchange cycles (DGCs) observed in many quiescent insects have been a cause of debate for decades, but no consensus on their evolutionary origin or adaptive significance has been achieved. Nevertheless, three main adaptive hypotheses have emerged: (i) the hygric hypothesis suggests that DGCs reduce respiratory water loss; (ii) the chthonic hypothesis suggests that DGCs facilitate gas exchange during environmental hypoxia, hypercapnia, or both; and (iii) the oxidative-damage hypothesis suggests that DGCs minimize oxidative tissue damage. However, most work conducted to date has been based on single-species investigations or nonphylogenetic comparative analyses of few species, despite calls for a strong-inference, phylogenetic approach. Here, we adopt such an approach by using 76 measurements of 40 wild-caught species to examine macrophysiological variation in DGC duration in insects. Potential patterns of trait variation are first identified on the basis of the explicit a priori predictions of each hypothesis, and the best phylogenetic generalized least-squares fit of the candidate models to the data is selected on the basis of Akaikes information criterion. We find a significant positive relationship between DGC duration and habitat temperature and an important interaction between habitat temperature and precipitation. This result supports the hygric hypothesis. We conclude that the DGCs of insects reduce respiratory water loss while ensuring adequate gas exchange.

The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae)

SUMMARY Recent reviews of the adaptive hypotheses for animal responses to acclimation have highlighted the importance of distinguishing between developmental and adult (non-developmental) phenotypic plasticity. There has been little work, however, on separating the effects of developmental plasticity from adult acclimation on physiological traits. Therefore, we investigated the relative contributions of these two distinct forms of plasticity to the environmental physiology of adult tsetse flies by exposing developing pupae or adult flies to different temperatures and comparing their responses. We also exposed flies to different temperatures during development and re-exposed them as adults to the same temperatures, to investigate possible cumulative effects. Critical thermal maxima were relatively inflexible in response to acclimation temperatures (21, 25, 29°C) with plasticity type accounting for the majority of the variation (49–67%, nested ANOVA). By contrast, acclimation had a larger effect on critical thermal minima with treatment temperature accounting for most of the variance (84–92%). Surprisingly little of the variance in desiccation rate could be explained by plasticity type (30–47%). The only significant effect of acclimation temperature on standard (resting) metabolic rate of adult flies was at 21°C, resulting in treatment temperature, rather than plasticity type, accounting for the majority of the variance (30–76%). This study demonstrates that the stage at which acclimation takes place has significant, though often different, effects on several adult physiological traits in G. pallidipes, and therefore that it is not only important to consider the form of plasticity but also the direction of the response and its significance from a life-history perspective.