Differences in the physiological responses to temperature among stonechats from three populations reared in a common environment

The physiological response to variation in air temperature (T(a)) can provide insights into how animals are adapted to different environments. I measured metabolic rate, total evaporative water loss (TEWL) and body temperature (T(b)) as a function of T(a) in stonechats from equatorial Kenya, temperate central Europe and continental Kazakhstan, environments where stonechats have evolved different life histories. All birds were raised and kept under identical captive conditions to highlight genetically based differences and to exclude phenotypic plasticity as explanatory factor. The slope relating metabolic rate to T(a) was steepest in Kazakh stonechats and lowest for birds from Kenya, indicating that, counterintuitively, the tropical stonechats were best insulated. Taking into account variation in T(b) in response to T(a), the lower critical temperature for the three populations fell between 32.0 and 34.9 degrees C, values higher than previously assumed. Whole organism BMR did not differ among populations, but because body mass was significantly higher in the Kenyan stonechats, their mass-specific BMR was lower compared with conspecifics from higher latitude. Whole organism or mass-specific TEWL did not differ among populations. Possibly, Kenyan birds are better insulated to compensate for their limited capacity to elevate metabolic rate.     

Quantitative genetics parameters show partial independent evolutionary potential for body mass and metabolism in stonechats from different populations

Phenotypic variation in physiological traits, such as energy metabolism, is commonly subjected to adaptive interpretations, but little is known about the heritable basis or genetic correlations among physiological traits in non-domesticated species. Basal metabolic rate (BMR) and body mass are related in complex ways. We studied the quantitative genetics of BMR, residual BMR (on body mass), mass-specific BMR and body mass of stonechats originating from four different populations and bred in captivity. Heritabilities ranged from 0.2 to 0.7. The genetic variance–covariance structure implied that BMR, mass-specific BMR and body mass can in part evolve independently of each other, because we found genetic correlations deviating significantly from one and minus one. BMR, mass-specific BMR and body mass further differed among populations at the phenotypic level; differences in the genetic correlation among populations are discussed.     

Physiological responses in rufous-collared sparrows to thermal acclimation and seasonal acclimatization

A large number of physiological acclimation studies assume that flexibility in a certain trait is both adaptive and functionally important for organisms in their natural environment; however, it is not clear how an organism’s capacity for temperature acclimation translates to the seasonal acclimatization that these organisms must accomplish. To elucidate this relationship, we measured BMR and TEWL rates in both field-acclimatized and laboratory-acclimated adult rufous-collared sparrows (Zonotrichia capensis). Measurements in field-acclimatized birds were taken during the winter and summer seasons; in the laboratory-acclimated birds, we took our measurements following 4 weeks at either 15 or 30°C. Although BMR and TEWL rates did not differ between winter and summer in the field-acclimatized birds, laboratory-acclimated birds exposed to 15°C exhibited both a higher BMR and TEWL rate when compared to the birds acclimated to 30°C and the field-acclimatized birds. Because organ masses seem to be similar between field and cold-acclimated birds whereas BMR is higher in cold-acclimated birds, the variability in BMR cannot be explained completely by adjustments in organ masses. Our findings suggest that, although rufous-collared sparrows can exhibit thermal acclimation of physiological traits, sparrows do not use this capacity to cope with minor to moderate fluctuations in environmental conditions. Our data support the hypothesis that physiological flexibility in energetic traits is a common feature of avian metabolism.     

Estimation of heritability and repeatability of resting metabolic rate in birds, with free-living pied flycatchers Ficedula hypoleuca (Aves: Passeriformes) as an example

Estimates of a trait heritability and repeatability can get at an idea of its usefulness for being an individual characteristic and its ability to change under selection pressure. Heritability and repeatability of energetic parameters still poorly studied in birds. The most important physiological characteristic of homoiotherms is resting metabolic rate (RMR), which, in the absence of productive processes, does not exceed basal metabolic rate (BMR). We estimated BMR repeatability in free-living pied flycatchers in Moscow Region (55 degrees 44' N, 36 degrees 51' E; 1992-2008) and Tomsk (56 degrees 20' N, 84 degrees 56' E; 2008-2009) populations over intervals from 40 days to 3 years. In Moscow Region population, BMR repeatability amounted to tau = 0.34 +/- 0.10 (n=80) if measured over 1 year interval, tau = 0.60 +/- 0.15 (n=19) if measured over 2 years interval, and tau = 0.85 +/- 0.13 (n=6) if measured over 3 years interval providing that consecutive BMR measurements were done in the same period of reproductive season. In Tomsk population, BMR repeatability, measured over 1 year interval, amounted to tau = 0.49 +/- 0.11 (n=50). Repeatability is a measure of a trait constancy and sets the upper limit of its heritability. To estimate RMR heritability, cross-fostering experiments have been conducted in 2003-2005 with flycatchers of Moscow Region population. RMR of chicks positively correlated with BMR of their biological fathers, whereas such correlation in metabolic rates between chicks and their foster fathers was absent. The RMR heritability estimate turned out to be h2 = 0.43 +/- 0.17 (n=210). The obtained estimates of heritability and repeatability of fundamental energetic traits are rather high for physiological features. This suggests the existence of a potential for direct selection on BMR and evolutionary stable diversity of avian populations with regard to basal metabolic rate.     

Moult and basal metabolic costs in males of two subspecies of stonechats: the European Saxicola torquata rubicula and the East African S. t. axillaris

The circannual patterns in resting metabolic rate (RMR) of males of two subspecies of stonechats, the European Saxicola torquata rubicula and the East African S. t. axillaris, are compared. As the birds from the two subspecies were raised and kept under comparable laboratory conditions, differences in metabolic rate between the two subspecies had to be genetically determined. RMR peaked during moult in both subspecies. During the rest of the year RMR was fairly constant in both subspecies and assumed to reflect basal metabolic rate (BMR). African stonechats had a 22% lower mass specific BMR than European stonechats, which is thought to reflect a genetical physiological adaptation to the differences in environmental circumstances they experience in the field. A low BMR makes an animal more susceptible to cold. Hence, the relatively high plumage mass in the African compared to the European stonechat may be functionally linked to its relatively low BMR. Moult costs, calculated from the plumage masses and the differences in RMR inside and outside the moult period, tended to be higher in the European compared to the African stonechats. These data and an interspecific comparison of moult costs over various species of birds support the earlier notion by Lindström et al. (1993) that moult costs are more closely linked with BMR than with body mass or rate of moult. The relation between moult costs and BMR and the fact that the efficiency of moult is extremely low (3.8 and 6.4% for European and African stonechats, respectively) suggest that the maintenance of specific tissues necessary for moult is a large cost factor. Alternatively, impaired insulation during moult may necessitate an increased metabolic capacity which may be associated with an increased RMR.     

Individual variation and repeatability of basal metabolism in the bank vole, Clethrionomys glareolus

Basal metabolic rate (BMR) is a fundamental energetic trait and has been measured in hundreds of birds and mammals. Nevertheless, little is known about the consistency of the population-average BMR or its repeatability at the level of individual variation. Here, we report that average mass-independent BMR did not differ between two generations of bank voles or between two trials separated by one month. Individual differences in BMR were highly repeatable across the one month interval: the coefficient of intraclass correlation was 0.70 for absolute log-transformed values and 0.56 for mass-independent values. Thus, BMR can be a meaningful measure of an individual physiological characteristic and can be used to test hypotheses concerning relationships between BMR and other traits. On the other hand, mass-independent BMR did not differ significantly across families, and the coefficient of intraclass correlation for full sibs did not differ from zero, which suggests that heritability of BMR in voles is not high.     

Adaptation of metabolism and evaporative water loss along an aridity gradient

Broad-scale comparisons of birds indicate the possibility of adaptive modification of basal metabolic rate (BMR) and total evaporative water loss (TEWL) in species from desert environments, but these might be confounded by phylogeny or phenotypic plasticity. This study relates variation in avian BMR and TEWL to a continuously varying measure of environment, aridity. We test the hypotheses that BMR and TEWL are reduced along an aridity gradient within the lark family (Alaudidae), and investigate the role of phylogenetic inertia. For 12 species of lark, BMR and TEWL decreased along a gradient of increasing aridity, a finding consistent with our proposals. We constructed a phylogeny for 22 species of lark based on sequences of two mitochondrial genes, and investigated whether phylogenetic affinity played a part in the correlation of phenotype and environment. A test for serial independence of the data for mass-corrected TEWL and aridity showed no influence of phylogeny on our findings. However, we did discover a significant phylogenetic effect in mass-corrected data for BMR, a result attributable to common phylogenetic history or to common ecological factors. A test of the relationship between BMR and aridity using phylogenetic independent constrasts was consistent with our previous analysis: BMR decreased with increasing aridity.     

Repeatability of basal metabolism in breeding female kittiwakes Rissa tridactyla

We studied kittiwakes (Rissa tridactyla) breeding near Ny-Ålesund (79° N, 12° E) on Svalbard. In 1997, the basal metabolic rates (BMRs) of 17 breeding females were measured during the incubation and chick-rearing periods. The mean body mass of the kittiwakes decreased significantly (by 10%) between the incubation and chick-rearing periods. At the same time, both the whole-body and mass-specific BMRs decreased significantly. There was a positive and significant relationship between the BMR residuals from the incubation period and those from the chick-rearing period. Thus, the BMR of incubating female kittiwakes is a significant predictor of their BMR during the chick-rearing period. New BMR data were collected in 1998 from ten of these females, measured around the chick-hatching date. Repeatability values were calculated using either (i) the data for eight individuals for which three BMR measurements existed, or (ii) all the data from both years, yielding significant repeatabilities of 0.52 and 0.35, respectively. These values indicate that between 48 and 65% of the observed variation in BMR is due to intraindividual variability, while between-individual variability accounts for 35 to 52% of the variation in the BMR. This is the first report of a significant repeatability of the BMR of an endothermic organism across an elapsed time of more than one day.     

Scombroid Fishes Provide Novel Insights into the Trait/Rate Associations of Molecular Evolution

The study of which life history traits primarily affect molecular evolutionary rates is often confounded by the covariance of these traits. Scombroid fishes (billfishes, tunas, barracudas, and their relatives) are unusual in that their mass-specific metabolic rate is positively associated with body size. This study exploits this atypical pattern of trait variation, which allows for direct tests of whether mass-specific metabolic rate or body size is the more important factor of molecular evolutionary rates. We inferred a phylogeny for scombroids from a supermatrix of molecular and morphological characters and used new phylogenetic comparative approaches to assess the associations of body size and mass-specific metabolic rate with substitution rate. As predicted by the body size hypothesis, there is a negative correlation between body size and substitution rate. However, unexpectedly, we also find a negative association between mass-specific metabolic and substitution rates. These relationships are supported by analyses of the total molecular data, separate mitochondrial and nuclear genes, and individual loci, and they are robust to phylogenetic uncertainty. The molecular evolutionary rates of scombroids are primarily tied to body size. This study demonstrates that groups with novel patterns of trait variation can be particularly informative for identifying which life history traits are the primary factors of molecular evolutionary rates.     

Basal metabolic rate can evolve independently of morphological and behavioural traits

Quantitative genetic analyses of basal metabolic rate (BMR) can inform us about the evolvability of the trait by providing estimates of heritability, and also of genetic correlations with other traits that may constrain the ability of BMR to respond to selection. Here, we studied a captive population of zebra finches (Taeniopygia guttata) in which selection lines for male courtship rate have been established. We measure BMR in these lines to see whether selection on male sexual activity would change BMR as a potentially correlated trait. We find that the genetic correlation between courtship rate and BMR is practically zero, indicating that the two traits can evolve independently of each other. Interestingly, we find that the heritability of BMR in our population (h²=0.45) is markedly higher than was previously reported for a captive zebra finch population from Norway. A comparison of the two studies shows that additive genetic variance in BMR has been largely depleted in the Norwegian population, especially the genetic variance in BMR that is independent of body mass. In our population, the slope of BMR increase with body mass differs not only between the sexes but also between the six selection lines, which we tentatively attribute to genetic drift and/or founder effects being strong in small populations. Our study therefore highlights two things. First, the evolvability of BMR may be less constrained by genetic correlations and lack of independent genetic variation than previously described. Second, genetic drift in small populations can rapidly lead to different evolvabilities across populations.     

Within seasons and among years: when are corticosterone levels repeatable?

Hormones play a central role in integrating internal and external cues to help mediate life-history decisions as well as changes in behavior and physiology of individuals. Describing the consistency of endocrine traits within and among individuals is an important step for understanding whether hormonal traits are dependable predictors of phenotypes that selection could act upon. However, few long-term field studies have investigated the individual consistency of hormonal traits. Glucocorticoid hormones mediate homeostatic responses to environmental variation as well as stress responses to acute, unpredictable disturbances. We characterized the repeatability of plasma corticosterone concentrations in two species of free-living passerines across multiple years. We found repeatability in baseline corticosterone concentrations in both sexes of great tits (Parus major) and in female tree swallows (Tachycineta bicolor) within the breeding season but no repeatability of this trait among seasons or across years. Stress-induced levels of corticosterone were only assessed in great tits and were not repeatable in either sex. Our data suggest that in line with their function in mediating responses of individuals to longer-term and acute demands, both baseline and stress-induced plasma corticosterone concentrations are rather plastic traits. However, individuals may differ in their degree of trait plasticity and hence in behavioral and physiological responses to a variety of organismal challenges.     

Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher

We examined proximate determination of sexually selected forehead patch size in a Central‐European population of Ficedula albicollis, the collared flycatcher, using a 9‐year database, and compared our results with those obtained in other populations of the same and the sister species. Between‐individual variation of forehead patch size was large, its repeatability larger than, and heritability similar to the Swedish population. Unlike in the other populations, the trait proved unaffected by body condition, and only very slightly influenced by age. There was no relationship between forehead patch size and breeding lifespan, and a marginal negative association with survivorship in adult males. Our results suggest that additive genetic variance of the trait in this population is large, but genes act independently of body condition, and there is no viability indicator value of the trait. This is the first report of a qualitative intraspecific difference in proximate determination of a sexually selected trait.     

Is BMR repeatable in deer mice? Organ mass correlates and the effects of cold acclimation and natal altitude

Basal metabolic rate (BMR) is probably the most studied aspect of energy metabolism in vertebrate endotherms. Numerous papers have explored its mass allometry, phylogenetic and ecological relationships, and ontogeny. Implicit in many of these studies (and explicit in some) is the view that BMR responds to selection, which requires repeatability and heritability. However, BMR is highly plastic in response to numerous behavioral and environmental factors and there are surprisingly few data on its repeatability. Moreover, the mechanistic underpinnings of variation in BMR are unclear, despite considerable research. We studied BMR repeatability in deer mice (Peromyscus maniculatus) across intervals of 30–60 days, and also examined the influence of birth altitude (3,800 m versus 340 m) and temperature acclimation (to ∼5 or ∼20°C) on BMR, and the relationship between BMR and organ size. Neither acclimation temperature nor natal altitude alone influenced BMR, but the combination of birth at high altitude and cold acclimation significantly increased BMR. Few visceral organ masses were correlated to BMR and most were inconsistent across natal altitudes and acclimation temperatures, indicating that no single organ ‘controls’ variation in BMR. In several treatment groups, the mass of the ‘running motor’ (combined musculoskeletal mass) was negatively correlated to BMR and the summed mass of visceral organs was positively correlated to BMR. We found no repeatability of BMR in any treatment group. That finding—in sharp contrast to high repeatability of BMR in several other small endotherms—suggests little potential for direct selection to drive BMR evolution in deer mice.     

Seasonal effects on metabolism and thermoregulation abilities of the Red-winged Starling (Onychognathus morio)

Basal metabolic rate (BMR) of birds is beginning to be viewed as a highly flexible physiological trait influenced by environmental fluctuations, and in particular changes in ambient temperatures (T_a). Southern Africa is characterized by an unpredictable environment with daily and seasonal variation. This study sought to evaluate the effects of seasonal changes in T_a on mass-specific resting metabolic rate (RMR), BMR and body temperature (T_b) of Red-winged Starlings (Onychognathus morio). They have a broad distribution, from Ethiopia to the Cape in South Africa and are medium-sized frugivorous birds. Metabolic rate (VO₂) and T_b were measured in wild caught Red-winged Starlings after a period of summer and winter acclimatization in outdoor aviaries. RMR and BMR were significantly higher in winter than summer. Body mass of Starlings was significantly higher in winter compared with summer. The increased RMR and BMR in winter indicate improved ability to cope with cold and maintenance of a high T_b. These results show that the metabolism of Red-winged Starlings are not constant, but exhibit a pronounced seasonal phenotypic flexibility with maintenance of a high T_b.     

Water and energy economy of an omnivorous bird: population differences in the Rufous-collared Sparrow (Zonotrichia capensis)

We investigated the intraspecific variation in basal metabolic rate (BMR) and total evaporative water loss (TEWL) in the omnivorous passerine Zonotrichia capensis from two populations inhabiting regions with different precipitation regimes and aridity indices. Values of TEWL in birds from the semi-arid region were significantly lower than those found in sparrows from the mesic region. TEWL in birds from the semi-arid site was 74% of the expectation based on body mass for passerines from mesic areas and similar to the allometric expectation for passerines from arid environments. In sparrows from the mesic area, TEWL was higher than predicted by their body mass for passerines from arid environments (133%), but very close (97%) to the expectation for passerines from mesic areas. BMR values were 25% lower in sparrows from the semi-arid region. The lower TEWL and BMR of birds from the semi-arid region may be a physiological adjustment that allows them to cope with fewer resources and/or water. We propose that the lower endogenous heat production in birds from the semi-arid environment may decrease their water requirements.     

Repeatability of energy metabolism and resistance to dehydration in the invasive slug Limax maximus

Standard metabolic rate (SMR) and resistance to body dehydration (BD) are important physiological traits that have an effect on water balance and the amount of energy available for activity and production, and thus could contribute to variation in life history traits expressed across a range of environments. Few studies have tested whether SMR and BD show consistent between‐individual variation in molluscs. Significant repeatability of SMR and BD indicates that the traits might be heritable and therefore a possible target for natural selection, so describing the repeatability of SMR and BD is important in studies of phenotypic variability. Here, we studied energy metabolism (body mass‐corrected SMR) and the change in the scaling relationship of SMR and body mass in response to time between measurements in the giant garden slug Limax maximus. Limax maximus is one of the most invasive terrestrial molluscs, with a wide geographical distribution, and is considered an important pest of horticultural and agricultural crops. Our results show that L. maximus follows the expected relationship of increasing SMR with increasing mass, but the scaling exponent varies through time and is different from that described for other gastropods. We also found significant inter‐individual variation in VCO_{2 Mean}, VCO_{2 Min}, VCO_{2 Max}, and BD (τ=0.25, 0.29, 0.24, 0.22, p<0.05, respectively), and significant repeatability of body mass (τ=0.90). To our knowledge, this is the first comprehensive analysis of the repeatability of body mass‐corrected SMR and BD in terrestrial slugs. Our results suggest that energy metabolism and water balance could potentially respond to selection.     

Repeatable inter‐individual variation in the thermal sensitivity of metabolic rate

Assessing whether trait variations among individuals are consistent over time and among environmental conditions is crucial to understand evolutionary responses to new selective pressures such as climate change. According to the universal thermal dependence hypothesis, thermal sensitivity of metabolic rate should not vary strongly and consistently among organisms, implying limited evolutionary response for metabolic traits under climate change. However, this hypothesis has been rarely tested at an individual level, leaving a gap in our understanding of climate change impacts on metabolic responses and their potential evolution. Using the amphipod Gammarus fossarum, we investigated the variability and repeatability of individual metabolic thermal reaction norms over time. We found large variations in both the thermal sensitivity (i.e. slope) and expression level (i.e. intercept) of individual metabolic reaction norms. Moreover, differences among individuals were consistent over time, and therefore repeatable. Inter‐individual variations in body mass resulted in a high repeatability of metabolic expression level but had no significant effect on the repeatability of thermal sensitivity. Overall, our results highlight that inter‐individual variability and repeatability of thermal reaction norms can be substantial. We conclude that these consistent differences among individuals should not be overlooked when apprehending the ecological and evolutionary effects of climate change.     

福寿螺表型性状的空间尺度变异

格局和尺度是生态学的核心概念。尺度的变化可能导致生态学格局的改变。入侵物种性状的变异会对种群的建立和扩散产生重要的影响。为了研究入侵物种福寿螺(Pomacea canaliculata)表型性状的尺度变异并推测可能的作用机制,在广东省开展了福寿螺的体质量、体高、体宽、壳口宽4个表型性状在城市、乡镇、生境、样方、个体5个空间尺度上变异的研究。通过拟合混合模型,进行方差分解,结果发现个体和样方差异解释了近80%的性状变异,生境的差异解释了除体重外其他性状的剩余变异;除体重外乡镇和城市尺度上性状的变异并不明显。结果进一步表明,区域尺度的过程如气候特征等对福寿螺表型性状变异不起主要作用;福寿螺种群特征的研究及防控的重点应考虑其遗传结构特征及局部尺度环境因素。通过不同尺度下性状的变异系数和频度分布曲线的分析,进一步验证了以上结果。     

Divergent patterns of telomere shortening in tropical compared to temperate stonechats

Telomeres have emerged as important biomarkers of health and senescence as they predict chances of survival in various species. Tropical birds live in more benign environments with lower extrinsic mortality and higher juvenile and adult survival than temperate birds. Therefore, telomere biology may play a more important role in tropical compared to temperate birds. We measured mean telomere length of male stonechats (Saxicola spp.) at four age classes from tropical African and temperate European breeding regions. Tropical and temperate stonechats had similarly long telomeres as nestlings. However, while in tropical stonechats pre‐breeding first‐years had longer telomeres than nestlings, in temperate stonechats pre‐breeding first‐years had shorter telomeres than nestlings. During their first breeding season, telomere length was again similar between tropical and temperate stonechats. These patterns may indicate differential survival of high‐quality juveniles in tropical environments. Alternatively, more favorable environmental conditions, that is, extended parental care, may enable tropical juveniles to minimize telomere shortening. As suggested by previous studies, our results imply that variation in life history and life span may be reflected in different patterns of telomere shortening rather than telomere length. Our data provide first evidence that distinct selective pressures in tropical and temperate environments may be reflected in diverging patterns of telomere loss in birds.     

Within seasons and among years: When are corticosterone levels repeatable?

Hormones play a central role in integrating internal and external cues to help mediate life-history decisions as well as changes in behavior and physiology of individuals. Describing the consistency of endocrine traits within and among individuals is an important step for understanding whether hormonal traits are dependable predictors of phenotypes that selection could act upon. However, few long-term field studies have investigated the individual consistency of hormonal traits. Glucocorticoid hormones mediate homeostatic responses to environmental variation as well as stress responses to acute, unpredictable disturbances. We characterized the repeatability of plasma corticosterone concentrations in two species of free-living passerines across multiple years. We found repeatability in baseline corticosterone concentrations in both sexes of great tits (Parus major) and in female tree swallows (Tachycineta bicolor) within the breeding season but no repeatability of this trait among seasons or across years. Stress-induced levels of corticosterone were only assessed in great tits and were not repeatable in either sex. Our data suggest that in line with their function in mediating responses of individuals to longer-term and acute demands, both baseline and stress-induced plasma corticosterone concentrations are rather plastic traits. However, individuals may differ in their degree of trait plasticity and hence in behavioral and physiological responses to a variety of organismal challenges.