Phenotypic Flexibility Research Articles

Latitudinal patterns in phenotypic plasticity: the case of seasonal flexibility in lizards’ fat body size

Several studies published over the last years suggest that the ability of many species to cope with global change will be closely related to the current amount of plasticity for fitness-related traits. Thus, disentangling general patterns in phenotypic flexibility, which could be then included in models aimed to predict changes in species distribution, represent a central goal in the current ecological agenda. The climatic variability hypothesis (CVH) could be considered a timely and promising hypothesis since it provides an explicit link between climatic and geographic variables and phenotypic plasticity. Specifically, the CVH states that as the range of climatic fluctuation experienced by terrestrial animals increases with latitude, individuals at higher latitudes should present greater levels of phenotypic flexibility. Within this framework, here we evaluate the existence of latitudinal patterns in fat body size flexibility--estimated as the difference between maximum and minimum fat body size values observed throughout a year--for 59 lizard species, comprising the first evaluation of the CVH for a trait, other than thermic or metabolic characters, in ectothermic species. Conventional and phylogenetic analyses indicated a positive relationship between fat body size flexibility and latitude, and also between flexibility and temperature variability indexes. Together with previous findings our results suggest that: (1) latitudinal pattern for fitness-related traits, other than thermal characters, are beginning to emerge; (2) latitude is usually a better predictor of phenotypic plasticity than putative climatic variables; (3) hemispheric differences in climatic variability appears to be correlated with hemispheric differences in phenotypic plasticity.

Metabolic response to changes in temperature in northern wheatears from an arctic and a temperate populations

Until recently it had been widely accepted that birds are energetically adapted to the latitude they inhabit, having an increased basal metabolic rate (BMR) at higher latitudes. Latterly, this general view has been questioned and the influence of phenotypic flexibility, due to factors such as habitat, life‐history or acclimatization has received increased attention. In particular, focus has been directed towards comparing species from arid and mesic habitats, but less attention has been given to species which breed in cold climates. We chose to study northern wheatears Oenanthe oenanthe from two populations at different latitudes (southern Norway, Iceland), but with similar life‐histories and habitat requirements throughout the year, in a common‐garden experiment. In order to assess true latitudinal trends in metabolic rate, we estimated the nocturnal resting metabolic rate (RMR) of northern wheatears from southern Norway and Iceland at different temperatures from 0° to 30°C. We found that Norwegian birds had overall lower metabolic rates than Icelandic birds, which were also slightly larger. This difference was not observed at 0°C, which might indicate that Icelandic birds might rely on better feather insulation reducing metabolic costs at very low temperatures. At temperatures above 10°C birds of both populations had constant metabolic values, indicating that their thermoneutral range almost completely covered the temperatures experienced during the breeding period. This study shows that the northern wheatear, which is one of only a few insectivorous long‐distance migratory songbirds occurring at such high latitudes, has evolved metabolic adaptations to life at cold temperatures which are endogenously determined.

Phenotypic flexibility in body mass, basal metabolic rate and summit metabolism in southern red bishops (Euplectes orix): Responses to short term thermal acclimation

Avian basal metabolic rate (BMR) and summit metabolism (Msum) vary within individuals in response to seasonal acclimatization in free-ranging birds, and thermal acclimation under laboratory conditions. We examined relationships between acclimation air temperature (Tacc) and body mass (Mb), BMR and Msum in female southern red bishops (Euplectes orix) from a relatively mild coastal site and a seasonally colder, inland site. Following acclimation for 21days to Tacc=10, 22 or 35°C, Mb, BMR and Msum were all significantly and negatively related to Tacc. The significant relationship between BMR and Tacc did not remain after Mb was included as a covariate, whereas that between Msum and Tacc did. A subsequent reverse acclimation protocol, where bishops were acclimated to a second Tacc value and then re-acclimated to the first, revealed that short-term changes in Mb and BMR were completely reversible, but changes in Msum were only partially reversible. Following the reverse-acclimation protocol, metabolic expansibility (Msum/BMR) varied significantly with air temperature, being greatest at Tacc=35°C. Our data suggest that the intraspecific variation in seasonal metabolic variation previously reported for this species is at least partly driven by factors other than temperature.

Physiological and biochemical thermoregulatory responses of Chinese bulbuls Pycnonotus sinensis to warm temperature: Phenotypic flexibility in a small passerine

Temperature is an important environmental cue for the regulation of thermogenesis in small birds. We tested the hypothesis that a small passerine, the Chinese bulbul Pycnonotus sinensis can decrease thermogenesis in response to warmer temperatures by decreasing body mass, the organ mass and changing physiological and biochemical processes in the liver and muscle. Captive Chinese bulbuls decreased in body mass and basal metabolic rate (BMR) during 4 weeks of acclimation to 30±1°C. They also showed a decrease in liver, kidney and small intestine mass and reduced mitochondrial state-4 respiration and cytochrome C oxidase (COX) activity in the liver and muscle compared to 10±1°C. Furthermore, BMR was positively correlated with body mass, organ mass (liver, kidney, small intestine and entire digestive tract), and mitochondrial state-4 respiration and cytochrome C oxidase (COX) activity in the liver and muscle. These results indicate that changes in body mass, organ mass and respiratory enzyme activity are mechanisms by which Chinese bulbuls adapt to warmer temperatures. The data support the hypothesis that such physiological flexibility is ubiquitous in birds.

Phenotypic flexibility in migrating bats: seasonal variation in body composition, organ sizes and fatty acid profiles

Many species of bats migrate long distances, but the physiological challenges of migration are poorly understood. We tested the hypothesis that migration is physiologically demanding for bats by examining migration-related phenotypic flexibility. Both bats and birds are endothermic, flying vertebrates; therefore, we predicted that migration would result in similar physiological trade-offs. We compared hoary bats (Lasiurus cinereus) during spring migration and summer non-migratory periods, comparing our results with previous observations of birds. Migrating bats had reduced digestive organs, enlarged exercise organs, and fat stores had higher proportions of polyunsaturated fatty acids (PUFAs). These results are consistent with previous studies of migrating birds; however, we also found sex differences not typically associated with bird migration. Migrating female hoary bats increased the relative size of fat stores by reducing lean body components, while males maintained the same relative amount of fat in both seasons. The ratio of n-6 to n-3 PUFA in flight muscle membrane increased in migrating males and decreased in migrating females, consistent with males using torpor more frequently than females during spring migration. Enlarged exercise organs, reduced digestive organs and changes in adipose tissue composition reflect the elevated energetic demands of migration. Sex-specific patterns of fat storage and muscle membrane composition likely reflect challenges faced by females that migrate while pregnant. Our results provide some of the first insights into the physiological demands of bat migration and highlight key differences between bats and birds.

Extinction or Survival? Behavioral Flexibility in Response to Environmental Change in the African Striped Mouse Rhabdomys

The rapid rate of anthropogenic-related climate change is expected to severely impact ecosystems and their constituent organisms, leading to mass extinction. A rapid adaptive response of animals to such change could be due to reversible phenotypic flexibility, including behavioral flexibility. Our model, the African striped mouse Rhabdomys, is a small rodent widely distributed in southern Africa. The desert-living species R. pumilio displays social flexibility, whereby individuals switch their social organization in response to prevailing conditions, potentially allowing for persistence in rapidly changing environments. Individuals of the species from the moist grasslands (R. dilectus) show some flexible traits, but opportunities to utilize this potential are apparently not realized. The climate in southern Africa is predicted to become drier, making both desert and grassland species vulnerable to environmental change. Based on realized or potential social flexibility in striped mice, we provide three (not mutually exclusive) scenarios that consider: (i) extinction of the desert species as its habitat changes; (ii) range expansion and utilization of pre-existing adaptations of the desert species to displace the current grassland species; and (iii) grassland species exploiting their potential flexibility (behavioral adaptation) and surviving in their current habitat. Behavioral flexibility is costly but could allow species to persist in rapidly changing environments.

Aquatic tail size carries over to the terrestrial phase without impairing locomotion in adult Eastern Red-spotted Newts (Notophthalmus viridescens viridescens)

Many species have evolved phenotypic flexibility to adjust to seasonal changes in their environment, including seasonal breeding phenotypes that increase reproductive success. If there are limits to this flexibility, such that traits carry over across seasons, there may be costs incurred as a result of trade-offs in optimal performance. Male and female Eastern Red-spotted Newts (Notophthalmus viridescens viridescens (Rafinesque, 1820)) increase tail size for the aquatic breeding season, and reduce their tail size as they return to the terrestrial environment after reproducing. We tested whether large aquatic tails (which should increase swim performance) carry over to become larger tails in the terrestrial phase (relative to body size), and whether this incurs a cost of decreased walking speed on land. We found a strong correlation between tail size in both phases, suggesting that this trait does carry-over between seasons and environments. Tail size was positively related to locomotor speed in the aquatic phase, but we found no evidence of a locomotor trade-off associated with tail size in the terrestrial phase. Further research that tests for alternative costs of developing large aquatic tails that are then carried over to the terrestrial environment would help to clarify the evolution of this life-cycle staging trait.

Inter‐ and intra‐specific variability in isoprene production and photosynthesis of Central European oak species

European deciduous oaks are closely related and are known for their strong emission of volatile isoprenoids. They are chemo-taxonomically diverse, but hybridise frequently. Four-year-old oak seedlings growing together in a model ecosystem facility under near-natural conditions were studied. The leaves were morphologically classified in the three oak species Quercus robur, Q.pubescens and Q.petraea (with four provenances each) and further investigated by a molecular-genetic approach. Q.robur was morphologically and genetically clearly different from Q.pubescens and Q.petraea, whereas Q.pubescens and Q.petraea individuals used in this study were morphologically and genetically more similar. There was a minor impact of among and within species variability on isoprene synthesis, isoprene emission and photosynthesis. Isoprene emission rates normalised to 25°C leaf temperature ranged from 5.78 to 10.66nmolm(-2) s(-1) , whereas photosynthesis ranged from 12.8 to 17.6μmolm(-2) s(-1) . On cloudy days, among the provenances of each species, only net photosynthesis of the Q.robur provenance Hünenberg was reduced and isoprene synthase activity of the Q.pubescens provenance Promotogno increased. On sunny days, photosynthesis did not differ among the provenances. Over all provenances, gas exchange on cloudy days did not differ significantly from sunny days. In the combined data of cloudy and sunny days, no differences between the studied provenances and oak species were detected in isoprene emission and photosynthesis. Thus, isoprene emission and photosynthesis rates were remarkably stable among oak species and provenances. The results indicate that taxonomic differences in the studied oak species are not reflected in isoprene emission and photosynthesis, probably because of the high plasticity of gene expression resulting in high phenotypic flexibility.

Magnetic Resonance Imaging Volumetry for Noninvasive Measures of Phenotypic Flexibility during Digestion in Burmese Pythons

Pythons are renowned for the profound phenotypical flexibility of their visceral organs in response to ingestion of large meals following prolonged fasting. Traditionally, the phenotypic changes are studied by determining organ mass of snakes killed at different times during digestion. Here we evaluate the use of magnetic resonance imaging (MRI) for in vivo measurements of the visceral organs in fasting and digesting snakes. Twelve snakes were MRI scanned immediately before the organs were removed and weighed to provide direct comparison of the two methods. Both methods provided similar estimates for the mass of liver, gallbladder, and pancreas, whereas MRI overestimated the size of the heart and small intestine, probably because blood and digesta contributed to the volume determined by MRI. The correlations were used to derive wet organ mass from MRI-based volumes to evaluate the mass development through repeated MRI scans of five digesting snakes. MRI was performed at fasting and 24, 48, 72, 132, and 500 h after eating a meal corresponding to 25% of body mass. This observation period revealed a reversible volume upregulation of the visceral organs, supporting the view that successive MRI facilitates in vivo investigations of structural changes accompanied by digestion.

Seasonal plasticity of gut morphology and small intestinal enzymes in free-living Mongolian gerbils

The phenotypic plasticity of the digestive system may determine the diversity of animal diets and, thus, their niche width. This study examines the effects of seasonal fluctuations in food quality and temperature on the gut morphology and the activity of sucrase, maltase, and aminopeptidase-N in the small intestinal brush-border membrane of male Mongolian gerbils (Meriones unguiculatus). Based on the adaptive modulation hypothesis and the principle of optimal gut function design, we hypothesize that the gut size, tissue-specific activity, and total hydrolytic capacity of intestinal digestive enzyme are upregulated in winter and downregulated in summer in response to diet shifts and energy demand in free-living Mongolian gerbils. Various seasonal modulation patterns in digestive enzyme activity in different regions of the small intestines were observed. The results show that male gerbils have the longest and heaviest small intestines in winter. This mechanism may be adapted to increase their food intake during winter. Male gerbils also exhibit the highest tissue-specific and total sucrase, maltase, and aminopeptidase-N activity in winter and in spring. Seasonal modulations are more distinct in the jejunum than in the duodenum and the ileum of the small intestines. The digestive phenotypic flexibility of male gerbils effectively corresponded with seasonal diet shifts and temperature fluctuations.

The Capital Economy in Hominin Evolution

The global distribution of our species indicates a biology capable of adapting to an extraordinary range of ecosystems, generating interest in how such a biology evolved. Whereas much attention has been directed to genetic adaptation and developmental plasticity as adaptive strategies, ecological stochasticity within the life course may be addressed by additional strategies such as bet hedging and phenotypic flexibility. Both social relationships and adipose tissue may be considered as “energy capital” conferring reversible phenotypic flexibility across the life course. Evidence from primates and contemporary humans demonstrates the value of such energy capital in accommodating ecological uncertainty. The fact that Homo sapiens is characterized by high levels of both cooperative sociality and adiposity compared with extant apes suggests that ecological stochasticity may have been a key ecological stress in the evolution of our genus. The benefits of phenotypic flexibility for ecological risk management may have preceded and enabled the emergence of traits such as carnivory, encephalization, colonizing, and the maintenance of a single breeding species across diverse environments.

Seasonal Metabolic Variation in Two Populations of an Afrotropical Euplectid Bird

Many birds exhibit seasonal phenotypic flexibility in basal metabolic rate (BMR) and summit metabolism (M(sum)), but very little information is available for species from subtropical latitudes or for conspecific populations from sites that vary in climate. We measured body mass (M(b)), BMR, and M(sum) in summer and winter in two populations of the southern red bishop Euplectes orix, a passerine that is widespread in southern Africa. One population occurs at a comparatively warmer coastal site (mean daily minimum air temperature [T(a)] in midwinter, 8.3°C) and the other at a colder inland site (mean daily minimum T(a) in midwinter, -2.8°C). Bishops from both populations significantly increased M(b) in winter. However, seasonal metabolic adjustments differed considerably between the populations. The inland population significantly increased BMR by approximately 58%, mass-specific BMR by approximately 31%, and M(sum) by approximately 15% in winter, although mass-specific M(sum) did not change significantly. In contrast, the coastal population showed no significant seasonal change in BMR and significant winter reductions in mass-specific BMR (~15%), M(sum) (~8%), and mass-specific M(sum) (~15%). The interpopulation differences in the magnitude and direction of seasonal mass-specific BMR changes are qualitatively consistent with global patterns, although the increase shown by the inland population is larger than expected. Our data reveal that avian seasonal metabolic adjustments can vary greatly within subtropical species depending on the climatic conditions experienced by the birds, and our findings reiterate the need to better understand metabolic flexibility in species that inhabit lower latitudes.

Inducing ossification in an engineered 3D scaffold-free living cartilage template

Large and complex bone defects or voids cannot rely on natural bone healing process for recovery. They require natural or engineered grafts to facilitate osteo-progenitor cell recruitment and development. In this study, we have employed an in vitro macro-sized 3D cell-based platform for investigation and application of osteogenesis. The model is based on a porous construct made of engineered living cartilaginous tissue named living hyaline cartilaginous graft (LhCG). It is scaffold-free and is solely made up of living chondrocytes and their extra cellular matrix (ECM). To evaluate the efficiency of LhCG as a viable platform for bone formation, osteoblast and human mesenchymal stem cell (hMSC) were seeded respectively into LhCG constructs, establishing a co-culture system consisting of osteo-progenitors and chondrocytes. The results showed that LhCG could support both osteoblast and hMSC maturation and differentiation to the osteogenic lineage respectively. Successful osteogenesis is also observed after subcutaneous implantation in nude mice model suggesting that bone formation could be achieved both in vitro and in vivo. Additionally, with exposure to osteogenic medium, LhCG construct without any further cell seeding expressed similar levels of osteogenic phenotype markers as the ones with hMSC seeded on. It suggests the existence of an osteoprogenitor sub-population residing within LhCG chondrocytes. Hence, it is demonstrated that LhCG, as a cartilage template, could serve as a dynamic platform to support osteogenesis and its intrinsic phenotypic flexibility may also permit a wide range of applications for stem cell research and processing.

The evolution of human adiposity and obesity: where did it all go wrong?

Because obesity is associated with diverse chronic diseases, little attention has been directed to the multiple beneficial functions of adipose tissue. Adipose tissue not only provides energy for growth, reproduction and immune function, but also secretes and receives diverse signaling molecules that coordinate energy allocation between these functions in response to ecological conditions. Importantly, many relevant ecological cues act on growth and physique, with adiposity responding as a counterbalancing risk management strategy. The large number of individual alleles associated with adipose tissue illustrates its integration with diverse metabolic pathways. However, phenotypic variation in age, sex, ethnicity and social status is further associated with different strategies for storing and using energy. Adiposity therefore represents a key means of phenotypic flexibility within and across generations, enabling a coherent life-history strategy in the face of ecological stochasticity. The sensitivity of numerous metabolic pathways to ecological cues makes our species vulnerable to manipulative globalized economic forces. The aim of this article is to understand how human adipose tissue biology interacts with modern environmental pressures to generate excess weight gain and obesity. The disease component of obesity might lie not in adipose tissue itself, but in its perturbation by our modern industrialized niche. Efforts to combat obesity could be more effective if they prioritized ‘external’ environmental change rather than attempting to manipulate ‘internal’ biology through pharmaceutical or behavioral means.

Seasonal phenotypic flexibility of flight muscle size in small birds: a comparison of ultrasonography and tissue mass measurements

Changes in flight muscle size are important mediators of phenotypic flexibility in birds, so the ability to track such changes over time in individual birds is a valuable tool for investigating phenotypic flexibility. Ultrasonography has been used to track changes in flight muscle size in shorebirds, but has not been previously used to track such changes in small birds, despite variation in flight muscle size being an important contributor to phenotypic flexibility in these birds. One prominent avian example of phenotypic flexibility is the seasonal phenotypes of small birds in response to climatic variation. The winter phenotype in these birds is characterized by increases in organismal metabolic rates and pectoralis muscle mass. We measured seasonal flight muscle size in House Sparrows (Passer domesticus, 25–30 g) using both ultrasonography and wet muscle mass and tested the correlation between ultrasonographic measures of breast muscle thickness and muscle mass. We further tested whether ultrasonographic measures of muscle thickness were sufficiently precise to detect seasonal variation in flight muscle mass. Muscle mass was significantly and positively associated with ultrasonographic measurements of breast muscle thickness for short-axis (SA), long-axis (LA), and combined SA and LA measurements. Breast muscle mass was significantly greater in winter than in summer (17.5 %) and muscle thickness also increased significantly in winter for both SA (9.1 %) and LA (7.5 %) measures. Thus, these data confirm that winter elevations of flight muscle mass consistently contribute to the winter phenotype in House Sparrows and that ultrasonography is effective in detecting seasonal changes in muscle mass in small birds.

A model of clearance rate regulation in mussels

Clearance rate regulation has been modelled as an instantaneous response to food availability, independent of the internal state of the animals. This view is incompatible with latent effects during ontogeny and phenotypic flexibility in clearance rate. Internal-state regulation of clearance rate is required to account for these patterns. Here I develop a model of internal-state based regulation of clearance rate. External factors such as suspended sediments are included in the model. To assess the relative merits of instantaneous regulation and internal-state regulation, I modelled blue mussel clearance rate and growth using a DEB model. In the usual standard feeding module, feeding is governed by a Holling's Type II response to food concentration. In the internal-state feeding module, gill ciliary activity and thus clearance rate are driven by internal reserve level. Factors such as suspended sediments were not included in the simulations. The two feeding modules were compared on the basis of their ability to capture the impact of latent effects, of environmental heterogeneity in food abundance and of physiological flexibility on clearance rate and individual growth. The Holling feeding module was unable to capture the effect of any of these sources of variability. In contrast, the internal-state feeding module did so without any modification or ad hoc calibration. Latent effects, however, appeared transient. With simple annual variability in temperature and food concentration, the relationship between clearance rate and food availability predicted by the internal-state feeding module was quite similar to that observed in Norwegian fjords. I conclude that in contrast with the usual Holling feeding module, internal-state regulation of clearance rate is consistent with well-documented growth and clearance rate patterns.

Independence among physiological traits suggests flexibility in the face of ecological demands on phenotypes

Phenotypic flexibility allows animals to adjust their physiology to diverse environmental conditions encountered over the year. Examining how these varying traits covary gives insights into potential constraints or freedoms that may shape evolutionary trajectories. In this study, we examined relationships among haematocrit, baseline corticosterone concentration, constitutive immune function and basal metabolic rate in red knot Calidris canutus islandica individuals subjected to experimentally manipulated temperature treatments over an entire annual cycle. If covariation among traits is constrained, we predict consistent covariation within and among individuals. We further predict consistent correlations between physiological and metabolic traits if constraints underlie species-level patterns found along the slow-fast pace-of-life continuum. We found no consistent correlations among haematocrit, baseline corticosterone concentration, immune function and basal metabolic rate either within or among individuals. This provides no evidence for constraints limiting relationships among these measures of the cardiovascular, endocrine, immune and metabolic systems in individual red knots. Rather, our data suggest that knots are free to adjust individual parts of their physiology independently. This makes good sense if one places the animal within its ecological context where different aspects of the environment might put different pressures on different aspects of physiology.

Latitudinal Patterns in Rodent Metabolic Flexibility

Macrophysiology is defined as the study of variation in physiological traits-including physiological trait flexibility-over large geographical and temporal scales, and the ecological implications of this variation. A classic example of a macrophysiological trend is the one emerging from the climatic variability hypothesis, which states that as the range of climatic fluctuation experienced by terrestrial animals increases with latitude, individuals at higher latitudes should be more plastic than individuals inhabiting lower latitudes. In this context, we evaluate the correlation between absolute metabolic scope during cold exposure (an instantaneous measure of metabolic flexibility) and different geographic and climatic variables for 48 rodent species. Conventional and phylogenetic informed analyses indicated a positive correlation between metabolic scope and geographic latitude. These findings, together with previous reports on latitudinal pattern in phenotypic flexibility, suggest that an increase in physiological flexibility with latitude may hold for many phenotypic traits.

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.

Phenotypic Plasticity and Adaptation in a Holometabolous Insect: The Chironomid Midge

Attention is currently shifting from a gene-centred view of evolution to a more phenotype-focussed one. Here, I attempt to test this new paradigm against a diverse and ecologically prominent taxon, the chironomid midge. I conclude that putting phenotypic and developmental flexibility at the forefront helps resolve some persistent difficulties in understanding the process of adaptation.