Stephen M. Secor

Specific dynamic action: a review of the postprandial metabolic response

For more than 200 years, the metabolic response that accompanies meal digestion has been characterized, theorized, and experimentally studied. Historically labeled “specific dynamic action” or “SDA”, this physiological phenomenon represents the energy expended on all activities of the body incidental to the ingestion, digestion, absorption, and assimilation of a meal. Specific dynamic action or a component of postprandial metabolism has been quantified for more than 250 invertebrate and vertebrate species. Characteristic among all of these species is a rapid postprandial increase in metabolic rate that upon peaking returns more slowly to prefeeding levels. The average maximum increase in metabolic rate stemming from digestion ranges from a modest 25% for humans to 136% for fishes, and to an impressive 687% for snakes. The type, size, composition, and temperature of the meal, as well as body size, body composition, and several environmental factors (e.g., ambient temperature and gas concentration) can each significantly impact the magnitude and duration of the SDA response. Meals that are large, intact or possess a tough exoskeleton require more digestive effort and thus generate a larger SDA than small, fragmented, or soft-bodied meals. Differences in the individual effort of preabsorptive (e.g., swallowing, gastric breakdown, and intestinal transport) and postabsorptive (e.g., catabolism and synthesis) events underlie much of the variation in SDA. Specific dynamic action is an integral part of an organism’s energy budget, exemplified by accounting for 19–43% of the daily energy expenditure of free-ranging snakes. There are innumerable opportunities for research in SDA including coverage of unexplored taxa, investigating the underlying sources, determinants, and the central control of postprandial metabolism, and examining the integration of SDA across other physiological systems.

A vertebrate model of extreme physiological regulation.

Investigation of vertebrate regulatory biology is restricted by the modest response amplitudes in mammalian model species that derive from a lifestyle of frequent small meals. By contrast, ambush-hunting snakes eat huge meals after long intervals. In juvenile pythons during feeding, there are large and rapid increases in metabolism and secretion, in the activation of enzymes and transporter proteins, and in tissue growth. These responses enable an economic hypothesis concerning the evolution of regulation to be tested. Combined with other experimental advantages, these features recommend juvenile pythons as the equivalent of a squid axon in vertebrate regulatory biology.

Evolution of regulatory responses to feeding in snakes.

Do animal species that normally consume large meals at long intervals evolve to down‐regulate their metabolic physiology while fasting and to up‐regulate it steeply on feeding? To test this hypothesis, we compared postfeeding regulatory responses in eight snake species: four frequent feeders on small meals and four infrequent feeders on large meals. For each species, we measured factorial changes in metabolic rate, in activities and capacities of five small intestinal brush border nutrient transporters, and in masses of eight organs that function in nutrient processing after consumption of a rodent meal equivalent to 25% of the snakes body mass. It turned out that, compared with frequent feeders, infrequent feeders digest that meal more slowly; have lower metabolic rates, organ masses, and nutrient uptake rates and capacities while fasting; have higher energy expenditure during digestion; and have higher postfeeding factorial increases in metabolic rate, organ masses, and nutrient uptake rates and capacities. These conclusions, which conform to the hypothesis mentioned above, remain after phylogeny has been taken into account. The small organ masses and low nutrient transporter activities during fasting contribute to the low fasting metabolism of infrequent feeders. Quantitative calculations of partial energy budgets suggest that energy savings drive the evolution of low mass and activities of organs during fasting and of large postfeeding regulatory responses in infrequent feeders. We propose further tests of this hypothesis among other snake species and among other ectotherms.

The Burmese python genome reveals the molecular basis for extreme adaptation in snakes

Significance The molecular basis of morphological and physiological adaptations in snakes is largely unknown. Here, we study these phenotypes using the genome of the Burmese python (Python molurus bivittatus), a model for extreme phenotypic plasticity and metabolic adaptation. We discovered massive rapid changes in gene expression that coordinate major changes in organ size and function after feeding. Many significantly responsive genes are associated with metabolism, development, and mammalian diseases. A striking number of genes experienced positive selection in ancestral snakes. Such genes were related to metabolism, development, lungs, eyes, heart, kidney, and skeletal structure—all highly modified features in snakes. Snake phenotypic novelty seems to be driven by the system-wide coordination of protein adaptation, gene expression, and changes in genome structure. Snakes possess many extreme morphological and physiological adaptations. Identification of the molecular basis of these traits can provide novel understanding for vertebrate biology and medicine. Here, we study snake biology using the genome sequence of the Burmese python (Python molurus bivittatus), a model of extreme physiological and metabolic adaptation. We compare the python and king cobra genomes along with genomic samples from other snakes and perform transcriptome analysis to gain insights into the extreme phenotypes of the python. We discovered rapid and massive transcriptional responses in multiple organ systems that occur on feeding and coordinate major changes in organ size and function. Intriguingly, the homologs of these genes in humans are associated with metabolism, development, and pathology. We also found that many snake metabolic genes have undergone positive selection, which together with the rapid evolution of mitochondrial proteins, provides evidence for extensive adaptive redesign of snake metabolic pathways. Additional evidence for molecular adaptation and gene family expansions and contractions is associated with major physiological and phenotypic adaptations in snakes; genes involved are related to cell cycle, development, lungs, eyes, heart, intestine, and skeletal structure, including GRB2-associated binding protein 1, SSH, WNT16, and bone morphogenetic protein 7. Finally, changes in repetitive DNA content, guanine-cytosine isochore structure, and nucleotide substitution rates indicate major shifts in the structure and evolution of snake genomes compared with other amniotes. Phenotypic and physiological novelty in snakes seems to be driven by system-wide coordination of protein adaptation, gene expression, and changes in the structure of the genome.

Determinants of the Postfeeding Metabolic Response of Burmese Pythons, Python molurus

The relatively large meal sizes consumed by sit-and-wait-foraging snake species make them favorable for investigating specific dynamic action, the rise in metabolic rate associated with digestion. Hence, we measured O₂ consumption rates (V̇o2) before and up to 20 d after Burmese pythons (Python molurus) either had only constricted and killed rodent meals or had also been allowed to consume meals ranging in size from 5% to 111% of their body mass. Postprandial V̇o2 peaked within 2 d at a value that increased with meal size, up to 44 times standard metabolic rate for the largest meals. In addition to being the largest known magnitude of postprandial metabolic response, this also exceeds the factorial increase in V̇o2 during peak physical activity for all studied animals except perhaps racehorses. Specific dynamic action, calculated from the extra V̇o2 above standard metabolic rate over the duration of digestion, increased with meal size and equaled 32% of ingested meal energy. The allometric exponent for body mass was 0.68 for standard metabolic rate, 0.90 for peak postprandial V̇o2, and 1.01 for specific dynamic action. Specific dynamic action is higher, and standard metabolic rate is lower, in sit-and-waitforaging snake species than in actively foraging snake species. This suggests that sit-and-wait-foraging snakes, which consume large meals at long and unpredictable intervals, reduce standard metabolic rate by allowing the energetically expensive small intestine and other associated organs to atrophy between meals but thereby incur a large specific dynamic action while rebuilding those organs upon feeding.

Regulation of digestive performance: a proposed adaptive response

Among snakes a correlation exists between feeding habits (frequent or infrequent) and the magnitude by which digestive performance is regulated (modest or large). This paper investigates whether the observed regulation of digestive performance is an adaptation to feeding habits and therefore, a product of natural selection. Using data on metabolic and intestinal responses to feeding for amphibians and reptiles, it is attempted to show the selective advantage and independent origin of either modestly or widely regulating gut performance. In an energetic model, snakes that naturally feed frequently on small meals benefit (from lower energy output) from modestly regulating gut performance as opposed to widely regulating gut performance. Likewise, the model suggests an energetic benefit for infrequently-feeding snakes secondary to the wide regulation of gut performance. This benefit is a function of long spans of fasting with a down-regulated gut (thereby incurring a lower standard metabolic rate) and the occasionally incursion of a costly up-regulation of the gut. In a comparison across several distantly-related lineages of amphibians and reptiles, frequently-feeding species all exhibit small postprandial responses in metabolism and intestinal nutrient transport capacities. In contrast, frogs and snakes that routinely fast for long periods independently experience five- to 30-fold increases in metabolism and intestinal performance with feeding. Among amphibians and reptiles the evidence presented supports the hypothesis that the extent by which the gut is regulated is an adaptive trait that evolved with divergence in feeding habits and energy budgets. In finishing, the foundations, caveats, and suggested future tests of this adaptive hypothesis are presented.

Fatty Acids Identified in the Burmese Python Promote Beneficial Cardiac Growth

A specific set of circulating fatty acids triggers cardiac hypertrophy in snakes and mammals. Burmese pythons display a marked increase in heart mass after a large meal. We investigated the molecular mechanisms of this physiological heart growth with the goal of applying this knowledge to the mammalian heart. We found that heart growth in pythons is characterized by myocyte hypertrophy in the absence of cell proliferation and by activation of physiological signal transduction pathways. Despite high levels of circulating lipids, the postprandial python heart does not accumulate triglycerides or fatty acids. Instead, there is robust activation of pathways of fatty acid transport and oxidation combined with increased expression and activity of superoxide dismutase, a cardioprotective enzyme. We also identified a combination of fatty acids in python plasma that promotes physiological heart growth when injected into either pythons or mice.

Ecological Significance of Movements and Activity Range for the Sidewinder, Crotalus cerastes

winders traveled on average 60% of the days monitored during their activity season (April-Oct.), with a resultant mean daily distance traveled of 117.8 ? 11.2 m/day. Although direction of travel was generally random, sidewinders exhibited significant directionality during the fall as they moved eastwardly to the sand-alluvial interface of the study site to overwinter. I speculate that overwintering in rodent burrows at the sand-alluvial interface increases overwintering survival because of decreased likelihood of exposure to freezing subsurface temperatures, greater structural stability of burrows, and lower risk of predation. Activity ranges of C. cerastes, calculated by minimum convex polygon (F = 23.2 + 2.8 ha) and harmonic mean (9 = 20.9 ? 2.6 ha) methods, are among the largest documented for snakes. For this population of sidewinders, there were no significant differences in activity range size between sexes or age classes (subadult vs adult). Core areas of activity (harmonic mean 50% isopleths) averaged 9.2 + 0.9% of total activity range size (harmonic mean 95% isopleths) and also did not differ in size between sexes and age classes. Activity range size did not correlate with body size (SVL and mass), although it did correlate with the number of locality coordinates used in its calculation. Activity ranges of individual sidewinders overlapped extensively on the study site, and snakes commonly shifted their centers of activity seasonally. Sidewinders moved their activity centers during the fall to the sites sand-alluvial edge and returned to the sites sandy region following emergence from hibernation.

Effects of Meal Size, Meal Type, Body Temperature, and Body Size on the Specific Dynamic Action of the Marine Toad, Bufo marinus

Specific dynamic action (SDA), the accumulated energy expended on all physiological processes associated with meal digestion, is strongly influenced by features of both the meal and the organism. We assessed the effects of meal size, meal type, body temperature, and body size on the postprandial metabolic response and calculated SDA of the marine toad, Bufo marinus. Peak postprandial rates of O2 consumption ( \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape