Evolutionary Adaptations to Poikilothermy and Its Ecological Implications

Evolutionary adaptations of poikilotherms are dictated by the necessity to withstand a substantial variation in body temperature. Across the animal kingdom, different species of poikilotherms have evolved to operate at body temperatures from —1.86 °C (e.g., some polar fish and invertebrates) to up to 44-45 ° C in certain tropical fish, desert insects, and reptiles, while dormant or quiescent life stages of some animals (such as some rotifers and tardigrades) can survive temperatures spanning from nearly —273 to over 100°C. Within each species of poi-kilotherms, the range of tolerated body temperatures is smaller, but can still be very appreciable. Thus, in temperate and subpolar poikilotherms, seasonal temperature changes may lead to a gradual change in Tb by 15-30 °C. On a short-term basis, some land insects and reptiles from temperate climates and marine intertidal invertebrates may experience rapid variations of Tb in excess of 20-30 °C during diurnal or tidal cycles. Behavioral escape mechanisms (such as migration or habitat choice) may reduce thermal stress but are rarely sufficient to completely prevent a change in Tb. As a result, physiological and biochemical functions of poiki-lotherms have evolved to withstand a wide range of

Figure 1 Poikilothermie animals: (a) a reef fish Anthias squampinnis; (b) a nudibranch mollusk Coryphella on a bryozoan colony; (c) a lion mane jellyfish Cyanea capillata; (d) a freshwater crustacean Daphnia (water flea), (e) a spring frog Rana; (f) a tiger swallowtail Papilio glaucus on honeysuckle. Photos: (a)-(e) Mikhail Fedyuk, (f) Inna Sokolova.

Figure 1 Poikilothermie animals: (a) a reef fish Anthias squampinnis; (b) a nudibranch mollusk Coryphella on a bryozoan colony; (c) a lion mane jellyfish Cyanea capillata; (d) a freshwater crustacean Daphnia (water flea), (e) a spring frog Rana; (f) a tiger swallowtail Papilio glaucus on honeysuckle. Photos: (a)-(e) Mikhail Fedyuk, (f) Inna Sokolova.

fluctuations in Tb which would be immediately lethal for most active homeotherms.

Temperature change directly affects the rates of all biological processes as well as stability of macromole-cules and membrane structures. At high temperatures, increasing molecular motion may lead to structural desta-bilization and eventually damage. At low temperatures, a decrease in kinetic energy of the molecules results in low rates of biochemical reactions and the loss of membrane fluidity incompatible with sustaining active life. If the temperature drops further, below the freezing point of intracellular fluids, water crystallization and resulting mechanical damage to the cells becomes a problem. Therefore, a major challenge of poikilothermy is to maintain cellular and systemic homeostasis in the face of temperature-induced functional and structural alterations in their cells. Poikilotherms have evolved multiple ways to achieve this homeostasis, which include profound alterations of intracellular milieu, membrane composition and properties, enzyme activities, and concentrations of molecular chaperones and cryoprotectants.

Biological membranes are among the most temperature-sensitive cellular sites in poikilotherms. Changes in Tb strongly affect membrane fluidity, which in turn may affect its integrity and permeability, as well as signal transduction and function of membrane-associated proteins and cytoskeleton. A suite of biochemical mechanisms known as homeoviscous adaptation allows poikilotherms to maintain optimal levels of membrane fluidity in the face of temperature change. These mechanisms involve adaptive changes in the degree of acyl chain saturation of the membrane phospholipids, changes in the cholesterol content and ratio of different phospholipid classes (phosphatidyl choline to phosphatidyl ethanolamine) in the membrane. In different poikilotherms, homeoviscous adaptation may be brought about by the de novo synthesis of certain lipid classes, biochemical modification of existing membrane lipids, cholesterol synthesis or breakdown, as well as by seasonal changes in the diet. Some mammalian hibernators selectively feed on plants rich in polyunsaturated fatty acids before entering into hibernation. This leads to an increase of the unsaturated lipid content in their membranes and fat depots, lower temperature set points during hibernation, and improved winter survival rates. Interestingly, diet can also affect temperature preference of an organism resulting in modified behavior. For example, Australian shingleback skinks select cooler environments when fed diets artificially enriched in polyunsaturated fatty acids, and this diet-induced shift in the preferred body temperature may reach 5 °C.

Another key aspect of the variable Tb in poikilotherms is variation in the rates of enzymatic reactions, which has profound 'ripple' effects on the rates of all integrative processes, from metabolism and growth to neurotransmission and behavior. Decrease in body temperature results in slowing down the rates of enzymatic reactions, which may in turn result in reduced rates of growth and reproduction, as well as impaired locomotion and ability to escape predators or to find food. On the short-term scale, homeostasis of enzymatic reaction rates may be achieved by changing concentrations of reaction substrates and products, or variation in intracellular levels of allosteric regulators of enzyme activity. During a prolonged decrease in Tb (e.g., during seasonal cold acclimatization), decreasing reaction rates can be compensated by elevated enzyme concentrations, expression of less-temperature-sensitive isoforms of enzymes, or both. However, this compensation is often incomplete, and in most poikilotherms a decrease in body temperature is associated with a decreased activity and growth rate.

Although elevated temperatures enhance rates of enzymatic processes (and thus, 'the rate of living') in poikilotherms, an excessive increase in Tb is damaging and potentially lethal due to the destabilization and eventual denaturation of cellular proteins. In order to protect against such denaturation, poikilotherms may express molecular chaperones (particularly so-called heat shock proteins, or HSPs), which assist in proper folding of partially denatured proteins and stabilization of their native conformation. Expression of HSPs is almost universal response to heat stress in the animal kingdom and found in all poikilotherms, as well as most homeotherms. The only known exception is some extremely stenother-mal and cold-adapted Antarctic fish species which have lost the ability to induce HSPs in response to heat stress. Increasing Tb also results in a decline in intracellular pH in poikilotherms, which helps to support normal folding and function of intracellular proteins through the maintenance of constant levels of protonation of their critical a-imidazol groups. Taken together, these changes in intracellular milieu help to maintain structural integrity and cellular homeostasis in poikilotherms facing a change in Tb.

Preventing ice formation is a significant challenge for poikilotherms living in habitats where environmental temperatures fall below the freezing point of intracellular fluids. Many poikilothermic species such as Arctic and Antarctic fishes, terrestrial arthropods and amphibians, plants and fungi are known to seasonally synthesize and accumulate antifreeze agents such as glycerol, sorbitol (and other polyols), trimethylamine-A^-oxide (TMAO), as well as specialized antifreeze proteins and glycopro-teins. These compounds decrease the freezing point of intracellular fluids and some ofthem also provide thermal hysteresis (lowering of the temperature required for crystal growth beyond that needed for crystal melting), thus preventing formation and growth of intracellular ice crystals. Owing to these mechanisms, some glycerol-rich insects may supercool to —60 °C without freezing. Caterpillars of the butterflies Aporia crataegi can survive several months with body temperature as low as —50 °C; to achieve such remarkable hardiness, 14% of their body weight is composed of cryoprotectants. In hibernating land frogs, high tissue levels of glucose serve as cryopro-tectants. Synthesis of the cryoprotectants in poikilotherms is regulated by hormonal systems, which in turn are typically activated by photoperiod rather than temperature. This allows animals to accumulate sufficient levels of cryoprotectants in their tissues before the environmental temperature actually drops below freezing.

It is worth noting that most of the above-described adaptive changes to maintain homeostasis in the face of changing Tb require considerable times to be accomplished (e.g., days to weeks) and are typically associated with long-term acclimation or acclimatization of poikilotherms to the changed thermal environment, for example, during seasonal temperature changes or evolutionary adaptation to different climates. During short-term temperature fluctuations, poikilotherms have to put up with temporary disturbances of cellular homeostasis and must depend on the robustness of their intracellular systems to survive those disturbances. Due to the inevitable constraints on structure and function of macromolecules (and thus on the range of the temperatures to which the organisms may be successfully adapted), there is no species that 'could take it all' and could survive the changes of Tb spanning over the whole range of temperatures consistent with active life. Due to the varying Tb as a function of ambient temperature and the high temperature sensitivity of their physiology, distribution patterns of poikilotherms often closely follow gradients or discontinuities in environmental temperature. It is perhaps no wonder that the most striking examples of the temperature-induced shifts in species distribution come from poikilotherm species. The threshold effects of temperature (i.e., the minimum amount of the temperature change which is sufficient to result in a significant shift of the species distribution limits) may be quite sublime, and a change of the mean temperature by 1-2 °C can strongly shift the geographical distribution of poikilotherms. This high temperature dependence of poikilotherm biogeography is evidenced not only by paleontological record but also by the recent observations of major distribution shifts in aquatic and terrestrial poi-kilotherms which are correlated with (and likely caused by) increases in ambient temperature of about 1.2-2.2 °C in the last century. A less-than-exhaustive list of recent climate-driven changes in poikilotherm distribution include major faunal shifts in shallow-water marine habitats, local extinctions of poikilotherm populations at the southern limits of the distribution range, declines in zooplankton abundance, extensive bleaching of coral reefs, increases in mosquito-born diseases in highlands, and the northward shift of ranges of nonmigratory insects. With the global climate change, more research will be needed to improve our understanding of physiological and biochemical mechanisms underlying the distribution shifts of poiki-lotherm populations and to analyze the profound ecosystem-level effects of these shifts.

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