Thyroid Hormones Correlate with Basal Metabolic Rate but Not Field Metabolic Rate in a Wild Bird Species

Thyroid hormones (TH) are known to stimulate in vitro oxygen consumption of tissues in mammals and birds. Hence, in many laboratory studies a positive relationship between TH concentrations and basal metabolic rate (BMR) has been demonstrated whereas evidence from species in the wild is scarce. Even though basal and field metabolic rates (FMR) are often thought to be intrinsically linked it is still unknown whether a relationship between TH and FMR exists. Here we determine the relationship between the primary thyroid hormone triiodothyronine (T3) with both BMR and FMR in a wild bird species, the black-legged kittiwake (Rissa tridactyla). As predicted we found a strong and positive relationship between plasma concentrations of T3 and both BMR and mass-independent BMR with coefficients of determination ranging from 0.36 to 0.60. In contrast there was no association of T3 levels with either whole-body or mass-independent FMR (R² = 0.06 and 0.02, respectively). In accordance with in vitro studies our data suggests that TH play an important role in modulating BMR and may serve as a proxy for basal metabolism in wild birds. However, the lack of a relationship between TH and FMR indicates that levels of physical activity in kittiwakes are largely independent of TH concentrations and support recent studies that cast doubt on a direct linkage between BMR and FMR.     

Does low daily energy expenditure drive low metabolic capacity in the tropical robin, Turdus grayi?

Temperate and tropical birds possess divergent life history strategies. Physiological parameters including energy metabolism correlate with the life history such that tropical species with a slower ‘pace of life’ have lower resting and maximal metabolic rates than temperate congeners. To better understand the physiological mechanisms underlying these differences, we investigated the relationship of metabolic capacity, muscle oxidative capacity and activity patterns to variation in life history patterns in American robins (Turdus migratorius), while resident in central North America and Clay-colored robins (Turdus grayi) resident in Panama. We measured summit metabolism $ \left( {\dot{V}{\text{O}_{2\text{summit}}}} \right) $ in birds from both tropical and temperate habitats and found that the temperate robins have a 60 % higher metabolic capacity. We also measured the field metabolic rate (FMR) of free-living birds using heart rate (HR) telemetry and found that temperate robins’ daily energy expenditure was also 60 % higher. Thus, $\dot{V}{\text{O}_{2\text{summit}}} $ and FMR both reflect life history differences between the species. Further, both species operate at a nearly identical ~50 % of their thermogenic capacity throughout a given day. As a potential mechanism to explain differences in activity and metabolic capacity, we ask whether oxidative properties of flight muscle are altered in accordance with life history variation and found minimal differences in oxidative capacity of skeletal muscle. These data demonstrate a close relationship between thermogenic capacity and daily activity in free-living birds. Further, they suggest that the slow pace of life in tropical birds may be related to the maintenance of low activity rather than functional capacity of the muscle tissue.     

光照条件、植株冠层结构和枝条寿命的关系——以桂花和水杉为例

根据衰老理论的代谢率假说,生物寿命与其代谢率有关,个体大小相同的生物体,在质量较好的微生境中通常比较差生境中具有更高的代谢速率。因此,生物体在资源供给较差的生境中通常比资源供给较充足的生境中具有更长的寿命。枝条是木本植物植冠构建的基本单元之一,如果枝条遵循代谢率假说,则可推测在光照较好环境下的植物枝条或小枝将比其在遮荫环境下具有更短的寿命,即枝条寿命与光照条件成反比。以常绿物种桂花(Osmanthus fragrans)和落叶物种水杉(Metasequoiaglyptostroboides)为研究对象,通过测量不同光照环境下,植株大小(株高和胸径)、冠层深度、冠层轮廓(冠层深度/冠层宽度)、相对冠层宽度(冠层宽度/植株高度)以及植株凋落枝条寿命等性状,探讨了光照条件对成年植株冠层形态结构和植株枝条寿命的影响。调查发现:1)枝条的寿命在遮荫条件下显著高于全光照条件下,与理论预测吻合;2)随遮荫程度增加,植株冠层深度和冠层轮廓增加,相对冠层宽度减小;3)枝条的平均寿命与植株冠层深度和冠层轮廓成正比,与植株相对冠层宽度成反比。这表明光照条件可能通过改变植株冠层结构来影响枝条寿命。未来需要进一步研究枝条生物量分配、叶片光合能力和呼吸速率在不同生活型物种之间的差异,以便更全面的理解枝条寿命与生境质量之间的关系。     

Xantusiid lizards have low energy, water, and food requirements

Lizards in the family Xantusiidae (the night lizards) are known to have resting metabolic rates that are only half those of other lizards of comparable size. We evaluated whether xantusiids also have low field metabolic rates (FMR) and food requirements by measuring FMR and water flux rates with doubly labeled water in three xantusiid species in their natural habitats. Free-living Xantusia vigilis, Xantusia henshawi, and Xantusia riversiana processed energy and water very slowly, about one-third as fast as do other reptiles of similar size. Xantusiid lizards have a distinctive life history that is characterized by very slow growth and low reproductive rates, and they are intensely reclusive. This general lifestyle is also found in some species that live in environments with scarce food resources, such as in caves and in arid habitats, and these species may also have relatively low energy requirements.     

Are summit metabolism and thermogenic endurance correlated in winter-acclimatized passerine birds?

Small birds exhibiting marked winter improvement of cold tolerance also show elevated summit metabolic rates (maximum cold-induced metabolic rate) in winter relative to summer. However, relatively large increases in cold tolerance can occur with only minor increments of maximum cold-induced metabolic rate and geographic variation in cold tolerance is not always positively correlated with variation in maximum cold-induced metabolic rate. Thus, it is uncertain whether maximum cold-induced metabolic rate and cold tolerance are phenotypically correlated in small birds and no previous study has directly examined this relationship. I measured maximum cold-induced metabolic rate and cold tolerance (i.e., thermogenic endurance) over three winters in black-capped chickadees Poecile atricapillus, American tree sparrows Spizella arborea, and dark-eyed juncos Junco hyemalis. For raw thermogenic endurance data, residuals of maximum cold-induced metabolic rate and thermogenic endurance from mass regressions were significantly and positively correlated in juncos and tree sparrows, and their correlation approached significance for chickadees. Log10 transformation of thermogenic endurance and mass data gave similar results. These data provide the first direct evidence for a phenotypic correlation between maximum cold-induced metabolic rate and thermogenic endurance in small birds, although much of the variance in thermogenic endurance is explained by factors other than maximum cold-induced metabolic rate and the degree of correlation differs among species. Nevertheless, these data suggest that physiological adjustments producing elevated thermogenic endurance also produce elevated maximum cold-induced metabolic rate in small birds.     

Relationships Among Powered Flight,Metabolic Rate,Body Mass,Genome Size,and the Retrotransposon Complement of Volant Birds

Avian genomes are of interest because the rapid metabolic rate associated with powered flight requires small cells which constrain genome size. Consequently, flying birds tend to have small genomes relative to other vertebrates such as mammals. It thus stands to reason that flying birds should have smaller genomes than ground-dwelling birds with lower metabolic rates. Small genomes could be condensed but uncompromised in a number of ways, including smaller intergenic intervals, shorter introns, and/or a reduced transposable element (TE) complement. We evaluated genome size in light of the orthologous TE complement among 41 flying (FY) and seven ground-dwelling (GD) bird species to determine if a preponderance of deletions in orthologous TEs might explain the compact genomes of flying birds with high metabolic rates. We measured, across multiple loci in all 48 species, the lengths of 50 contemporary orthologous chicken repeat 1 (CR1, a non-LTR retrotransposon) copies relative to inferred ancestral CR1 sequences. We found genome sizes in GD birds were not different than those in FY birds, but the mean lengths of orthologous CR1 loci were significantly shorter in FY birds than in GD birds. Moreover, we observed a negative correlation between basal metabolic rate and length of orthologous CR1 loci. Finally, we observed positive correlations between body mass and both genome sizes as well as length of orthologous CR1 loci, which we expected given that body mass correlates negatively with metabolic rates. Our results support the contention that metabolism helps shape the avian TE complement and thus indirectly contributes to the compact genomes of birds.     

Field metabolic rates of black-browed albatrosses Thalassarche melanophrys during the incubation stage

Field metabolic rates (FMR) and activity patterns of black-browed albatrosses Thalassarche melanophrys were measured while at sea and on nest during the incubation stage at Kerguelen Island, southwestern Indian Ocean. Activity-specific metabolic rates of five albatrosses at sea (FMR_at-sea) were measured using doubly labeled water (DLW), and by equipping birds with wet-dry activity data loggers that determined when birds were in flight or on the water. The metabolic rates of four birds incubating their eggs (FMR_on-nest) were also measured using DLW. The mean±SD FMR_at-sea of albatrosses was 611±96 kJ kg⁻¹ d⁻¹ compared to FMR_on-nest of 196±52 kJ kg⁻¹ d⁻¹. While at sea, albatrosses spent 52.9±8.2% (N=3) of their time in flight and they landed on the water 41.2±13.9 times per day. The FMR of black-browed albatrosses appear to be intermediate to that of three other albatross species. Based on at-sea activity, the power requirement of flight was estimated to be 8.7 W kg⁻¹ (or 4.0×predicted BMR), which is high compared to other albatross species, but may be explained by the high activity levels of the birds when at sea. The FMR_at-sea of albatrosses, when scaled with body mass, are lower than other seabirds of similar body size, which probably reflects the economical nature of their soaring flight.     

The erratic mitochondrial clock: variations of mutation rate, not population size, affect mtDNA diversity across birds and mammals

Background  

During the last ten years, major advances have been made in characterizing and understanding the evolution of mitochondrial DNA, the most popular marker of molecular biodiversity. Several important results were recently reported using mammals as model organisms, including (i) the absence of relationship between mitochondrial DNA diversity and life-history or ecological variables, (ii) the absence of prominent adaptive selection, contrary to what was found in invertebrates, and (iii) the unexpectedly large variation in neutral substitution rate among lineages, revealing a possible link with species maximal longevity. We propose to challenge these results thanks to the bird/mammal comparison. Direct estimates of population size are available in birds, and this group presents striking life-history trait differences with mammals (higher mass-specific metabolic rate and longevity). These properties make birds the ideal model to directly test for population size effects, and to discriminate between competing hypotheses about the causes of substitution rate variation.     

Energetic cost of foraging in free-diving emperor penguins.

Hypothesizing that emperor penguins (Aptenodytes forsteri) would have higher daily energy expenditures when foraging for their food than when being hand-fed and that the increased expenditure could represent their foraging cost, we measured field metabolic rates (FMR; using doubly labeled water) over 4-d periods when 10 penguins either foraged under sea ice or were not allowed to dive but were fed fish by hand. Surprisingly, penguins did not have higher rates of energy expenditure when they dove and captured their own food than when they did not forage but were given food. Analysis of time-activity and energy budgets indicated that FMR was about 1.7 x BMR (basal metabolic rate) during the 12 h d(-1) that penguins were lying on sea ice. During the remaining 12 h d(-1), which we termed their "foraging period" of the day, the birds were alert and active (standing, preening, walking, and either free diving or being hand-fed), and their FMR was about 4.1 x BMR. This is the lowest cost of foraging estimated to date among the eight penguin species studied. The calculated aerobic diving limit (ADL(C)), determined with the foraging period metabolic rate of 4.1 x BMR and known O(2) stores, was only 2.6 min, which is far less than the 6-min ADL previously measured with postdive lactate analyses in emperors diving under similar conditions. This indicates that calculating ADL(C) from an at-sea or foraging-period metabolic rate in penguins is not appropriate. The relatively low foraging cost for emperor penguins contributes to their relatively low total daily FMR (2.9 x BMR). The allometric relationship for FMR in eight penguin species, including the smallest and largest living representatives, is kJ d(-1)=1,185 kg(0.705).     

The extreme longevity of Arctica islandica is associated with increased peroxidation resistance in mitochondrial membranes

The deleterious reactive carbonyls released upon oxidation of polyunsaturated fatty acids in biological membranes are believed to foster cellular aging. Comparative studies in mammals and birds have shown that the susceptibility to peroxidation of membrane lipids peroxidation index (PI) is negatively correlated with longevity. Long‐living marine molluscs are increasingly studied as longevity models, and the presence of different types of lipids in the membranes of these organisms raises questions on the existence of a PI–longevity relationship. We address this question by comparing the longest living metazoan species, the mud clam Arctica islandica (maximum reported longevity = 507 year) to four other sympatric bivalve molluscs greatly differing in longevity (28, 37, 92, and 106 year). We contrasted the acyl and alkenyl chain composition of phospholipids from the mitochondrial membranes of these species. The analysis was reproduced in parallel for a mix of other cell membranes to investigate whether a different PI–longevity relationship would be found. The mitochondrial membrane PI was found to have an exponential decrease with increasing longevity among species and is significantly lower for A. islandica. The PI of other cell membranes showed a linear decrease with increasing longevity among species and was also significantly lower for A. islandica. These results clearly demonstrate that the PI also decreases with increasing longevity in marine bivalves and that it decreases faster in the mitochondrial membrane than in other membranes in general. Furthermore, the particularly low PI values for A. islandica can partly explain this species’ extreme longevity.     

The maximum oxygen consumption and aerobic scope of birds and mammals: getting to the heart of the matter

Resting or basal metabolic rates, compared across a wide range of organisms, scale with respect to body mass as approximately the 0.75 power. This relationship has recently been linked to the fractal geometry of the appropriate transport system or, in the case of birds and mammals, the blood vascular system. However, the structural features of the blood vascular system should more closely reflect maximal aerobic metabolic rates rather than submaximal function. Thus, the maximal aerobic metabolic rates of birds and mammals should also scale as approximately the 0.75 power. A review of the literature on maximal oxygen consumption and factorial aerobic scope (maximum oxygen consumption divided by basal metabolic rate) suggests that body mass influences the capacity of the cardiovascular system to raise metabolic rates above those at rest. The results show that the maximum sustainable metabolic rates of both birds and mammals are similar and scale as approximately the 0.88 +/- 0.02 power of body mass (and aerobic scope as approximately the 0.15 +/- 0.05 power), when the measurements are standardized with respect to the differences in relative heart mass and haemoglobin concentration between species. The maximum heart beat frequency of birds and mammals is predicted to scale as the -0.12 +/- 0.02 power of body mass, while that at rest should scale as -0.27 +/- 0.04.     

Metabolism and longevity: is there a role for membrane fatty acids?

More than 100 years ago, Max Rubner combined the fact that both metabolic rate and longevity of mammals varies with body size to calculate that "life energy potential" (lifetime energy turnover per kilogram) was relatively constant. This calculation linked longevity to aerobic metabolism which in turn led to the "rate-of-living" and ultimately the "oxidative stress" theories of aging. However, the link between metabolic rate and longevity is imperfect. Although unknown in Rubner's time, one aspect of body composition of mammals also varies with body size, namely the fatty acid composition of membranes. Fatty acids vary dramatically in their susceptibility to peroxidation and the products of lipid peroxidation are very powerful reactive molecules that damage other cellular molecules. The "membrane pacemaker" modification of the "oxidative stress" theory of aging proposes that fatty acid composition of membranes, via its influence on peroxidation of lipids, is an important determinant of lifespan (and a link between metabolism and longevity). The relationship between membrane fatty acid composition and longevity is discussed for (1) mammals of different body size, (2) birds of different body size, (3) mammals and birds that are exceptionally long-living for their size, (4) strains of mice that vary in longevity, (5) calorie-restriction extension of longevity in rodents, (6) differences in longevity between queen and worker honeybees, and (7) variation in longevity among humans. Most of these comparisons support an important role for membrane fatty acid composition in the determination of longevity. It is apparent that membrane composition is regulated for each species. Provided the diet is not deficient in polyunsaturated fat, it has minimal influence on a species' membrane fatty acid composition and likely also on it's maximum longevity. The exceptional longevity of Homo sapiens combined with the limited knowledge of the fatty acid composition of human tissues support the potential importance of mitochondrial membranes in determination of longevity.     

Living at the physiological limits: field and maximum metabolic rates of the common shrew (Sorex araneus)

Shrews (genus Sorex, small insectivorous mammals) are well known for their extremely high basal metabolic rates (BMRs) even when corrected for their small body size. We measured energy expenditure of the common shrew (Sorex araneus) under natural conditions (field metabolic rate [FMR]) by doubly labeled water method to test whether FMR is proportional to high BMR in this species. The study was performed in summer in northeastern Poland. In addition to the FMR, we also measured maximum metabolic rates induced by cold exposure and by intense activity (MMRCOLD and MMRRUN, respectively) to evaluate the aerobic reserve (MMR-FMR) in S. araneus. This aerobic reserve was used as an indicator of the potential for metabolic constraints. The FMR averaged 2.31+/-0.32 L CO2 d(-1) (+/-SD) or 58.1+/-8.0 kJ d(-1) in 8.2-g animals. This figure constituted 216%-258% of a value predicted for a "standard" mammal of the same body mass and was the highest mass-specific field metabolic rate in mammals. Because of the high BMR level in S. araneus, the FMR to BMR ratio (2.4) was not far off mammalian standards (median value of 3.1). The rate of water efflux determined in S. araneus (20.2 mL H2O d(-1) or 2.46 mL H2O g(-1) d(-1)) exceeded all figures reported to date in other mammals and was apparently linked to the high FMR level and relatively high water content of shrews' food. Maximal metabolic rates (MMRRUN of 18.1+/-1.6 mL O2 g(-1) h(-1) and MMRCOLD of 23.5+/-1.9 mL O2 g(-1) h(-1)) were not high in proportion to BMR or FMR that resulted in relatively narrow aerobic reserve in S. araneus: 20% when calculated against the MMRRUN and 39% when compared with the MMRCOLD. Our study reveals that S. araneus has high energy costs of living and operates close to its physiological limits.     

Energetics of the smallest: Do bacteria breathe at the same rate as whales?

Power laws describing the dependence of metabolic rate on body mass have been established for many taxa, but not for prokaryotes, despite the ecological dominance of the smallest living beings. Our analysis of 80 prokaryote species with cell volumes ranging more than 1,000,000-fold revealed no significant relationship between mass-specific metabolic rate q and cell mass. By absolute values, mean endogenous mass-specific metabolic rates of non-growing bacteria are similar to basal rates of eukaryote unicells, terrestrial arthropods and mammals. Maximum mass-specific metabolic rates displayed by growing bacteria are close to the record tissue-specific metabolic rates of insects, amphibia, birds and mammals. Minimum mass-specific metabolic rates of prokaryotes coincide with those of larger organisms in various energy-saving regimes: sit-and-wait strategists in arthropods, poikilotherms surviving anoxia, hibernating mammals. These observations suggest a size-independent value around which the mass-specific metabolic rates vary bounded by universal upper and lower limits in all body size intervals.     

The determinants of the molecular substitution process in turtles

Neutral rates of molecular evolution vary across species, and this variation has been shown to be related to biological traits. One of the first patterns to be observed in vertebrates has been an inverse relationship between body mass (BM) and substitution rates. The effects of three major life‐history traits (LHT) that covary with BM – metabolic rate, generation time and longevity (LON) – have been invoked to explain this relationship. However, most of the theoretical and empirical evidence supporting this relationship comes from endothermic vertebrates, that is, mammals and birds, in which the environmental conditions, especially temperature, do not have a direct impact on cellular and molecular biology. We analysed the variations in mitochondrial and nuclear rates of synonymous substitution across 224 turtle species and examined their correlation with two LHT (LON and BM) and two environmental variables [latitude (LAT) and habitat]. Our analyses indicate that in turtles, neutral rates of molecular evolution are hardly correlated with LON or BM. Rather, both the mitochondrial and nuclear substitution rates are significantly correlated with LAT – faster evolution in the tropics – and especially so for aquatic species. These results question the generality of the relationships reported in mammals and birds and suggest that environmental factors might be the strongest determinants of the mutation rate in ectotherms.     

Metabolic rate is negatively linked to adult survival but does not explain latitudinal differences in songbirds

Survival rates vary dramatically among species and predictably across latitudes, but causes of this variation are unclear. The rate‐of‐living hypothesis posits that physiological damage from metabolism causes species with faster metabolic rates to exhibit lower survival rates. However, whether increased survival commonly observed in tropical and south temperate latitudes is associated with slower metabolic rate remains unclear. We compared metabolic rates and annual survival rates that we measured across 46 species, and from literature data across 147 species of birds in northern, southern and tropical latitudes. High metabolic rates were associated with lower survival but survival varied substantially among latitudinal regions independent of metabolism. The inability of metabolic rate to explain latitudinal variation in survival suggests (1) species may evolve physiological mechanisms that mitigate physiological damage from cellular metabolism and (2) extrinsic rather than intrinsic sources of mortality are the primary causes of latitudinal differences in survival.     

The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach

The relationship of oxidative stress with maximum life span (MLSP) in different vertebrate species is reviewed. In all animal groups the endogenous levels of enzymatic and non-enzymatic antioxidants in tissues negatively correlate with MLSP and the most longevous animals studied in each group, pigeon or man, show the minimum levels of antioxidants. A possible evolutionary reason for this is that longevous animals produce oxygen radicals at a low rate. This has been analysed at the place where more than 90% of oxygen is consumed in the cell, the mitochondria. All available work agrees that, across species, the longer the life span, the lower the rate of mitochondrial oxygen radical production. This is true even in animal groups that do not conform to the rate of living theory of aging, such as birds. Birds have low rates of mitochondrial oxygen radical production, frequently due to a low free radical leak in their respiratory chain. Possibly the low rate of mitochondrial oxygen radical production of longevous species can decrease oxidative damage at targets important for aging (like mitochondrial DNA) that are situated near the places of free radical generation. A low rate of free radical production can contribute to a low aging rate both in animals that conform to the rate of living (metabolic) theory of aging and in animals with exceptional longevities, like birds and primates. Available research indicates there are at least two main characteristics of longevous species: a high rate of DNA repair together with a low rate of free radical production near DNA. Simultaneous consideration of these two characteristics can explain part of the quantitative differences in longevity between animal species. Accepted: 12 December 1997     

Testing the "rate of living" model: further evidence that longevity and metabolic rate are not inversely correlated in Drosophila melanogaster.

In a recent study examining the relationship between longevity and metabolism in a large number of recombinant inbred Drosophila melanogaster lines, we found no indication of the inverse relationship between longevity and metabolic rate that one would expect under the classical "rate of living" model. A potential limitation in generalizing from that study is that it was conducted on experimental material derived from a single set of parental strains originally developed over 20 years ago. To determine whether the observations made with those lines are characteristic of the species, we studied metabolic rates and longevities in a second, independently derived set of recombinant inbred lines. We found no correlation in these lines between metabolic rate and longevity, indicating that the ability to both maintain a normal metabolic rate and have extended longevity may apply to D. melanogaster in general. To determine how closely our measurements reflect metabolic rates of flies maintained under conditions of life span assays, we used long-term, flow-through metabolic rate measurements and closed system respirometry to examine the effects of variables such as time of day, feeding state, fly density, mobility of the flies, and nitrogen knockout on D. melanogaster metabolic rate. We found that CO2 production estimated in individual flies accurately reflects metabolic rates of flies under the conditions used for longevity assays.     

Longevity of animals in units of intrinsic time

We propose two different approaches to defining variable units of intrinsic time (physiological time units in a strict sense, or PTU). For continuously growing animals, we suggest the use of specific mass growth rates; and for animals that cease to grow at some point, we recommend specific metabolic rates. Longevity of animals in terms of PTU is equal to the total specific rate (per lifetime) of the respective processes. A method is proposed to describe age-related changes in respect of specific metabolic rates of non-growing constant-mass adult birds. Maximum PTU longevity values have been estimated for certain fish species (continuously growing animals), and birds (that cease growth). Estimates of the maximum PTU longevity across both passerine and non-passerine groups differ slightly and are actually estimates of the Rubner constant for birds.     

Phenotypic flexibility in basal metabolic rate is associated with rainfall variability among populations of rufous-collared sparrow

Phenotypic flexibility in metabolic rates allows organisms to reversibly adjust their energy flow to meet challenges imposed by a variable environment. In turn, the food habits hypothesis (FHH) predicts that species or populations adjust their basal metabolic rate (BMR) according to the diet attributes such as food abundance or predictability. Desert ecosystems represent a temporally heterogeneous environment because of low rain pulse predictability, which is also associated with temporal variation in food resources. In the present study, we investigated the relationship between the magnitude of BMR flexibility in response to dietary acclimation and the inter-annual rainfall variability in three populations of rufous-collared sparrows. Specifically we addressed the question of whether birds from a desert environment are more flexible in BMR than those from non-desert habitats. We found a positive trend between BMR flexibility and the inter-annual rainfall variability. In fact, dietary treatments had a significant effect only in desert birds, a result that also supported the FHH. Our study confirms the existence of phenotypic variation in response to environmental conditions among populations, and also highlights the importance of considering the circumstances in which phenotypic flexibility evolves and the specific environmental cues that induce their expression.