Lecture 2: Accomplishments of Physiological Ecology; Evolution and the Phenotypic Hierarchy

1. Lecture 2: • Accomplishments of Physiological Ecology; • Evolution and thePhenotypic Hierarchy

2. Accomplishments of Physiological Ecology Reading: Bennett, A. F. 1987. The accomplishments of physiological ecology. Pages 1-10 in M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey, eds. New directions in ecological physiology. Cambridge Univ. Press., Cambridge, U.K. & New York.

3. The Accomplishments of Physiological Ecology 1. Energy availability and utilization are important constraints on animal function. Energy availability can impose constraints on what organisms can do. For poikilotherms, these constraints can be temperature dependent.

4. Measurement of energy exchange leads easily to links with behavior and ecology: 1. optimal foraging theory - costs and benefits usually phrased in energy 2. population- and community-level usage of energy affect ecosystem dynamics

5. Measurement of energy exchange leads easily to links with behavior and ecology: 1. optimal foraging theory - costs and benefits usually phrased in energy 2. population- and community-level usage of energy affect ecosystem dynamics Evolutionary linkage is often via life history theory, which deals with things like optimal size and number of offspring, given a limited amount of energy available for reproduction: trade-offs can be important … if energy is truly limiting.

6. Development of a quick-reading mercury thermometer was a technological advance that allowed study of body temperatures of lizards. 2. Body temperature regulation is expensive in time and energy. Its alternative, temperature conformity, entails variability in all physiological processes. Thermoregulation has long been a favorite subject of study.

7. Early papers showed that desert lizards often maintained high (35-40oC) and relatively stable body temperatures when active. Dipsosaurus dorsalis,the desert iguana Cnemidophorus tigris,the whiptail Uma scoparia,the fringe-toed lizard

8. Cowles, R. B., and C. M. Bogert. 1944. A preliminary study of the thermal requirements of desert reptiles. Bull. Amer. Mus. Nat. Hist. 83:265-296. Bogert, C. M. 1949. Thermoregulation in reptiles, a factor in evolution. Evolution 3:195-211. This was different from what most people thought, who had typically observed lizards in captive situations where they could not thermoregulate normally (e.g., no heat lamp). Grab 'em and jab 'em! Noose 'em and goose 'em! (Find 'em and grind 'em!)

9. http://www.wildherps.com/species/S.occidentalis.html Data from Prof. Stephen C. Adolph, Department of Biology, Harvey Mudd College, Claremont, California

10. And later telemetry was used …

11. Huey, R. B., and M. Slatkin. 1976. Cost and benefits of lizard thermoregulation. Quart. Rev. Biol. 51:363-384.

12. Empirical studies were followed by development of biophysical models of heat and water exchange, e.g., Porter, Bakken, Gates: 1. pure theory "consider a spherical cow"http://en.wikipedia.org/wiki/Spherical_cow 2. copper models (painted) Dzialowski, E. M. 2005. Use of operative temperature and standard operative temperature models in thermal biology. Journal of Thermal Biology 30:317-334.

13. Empirical studies were followed by development of biophysical models of heat and water exchange, e.g., Porter, Bakken, Gates: 1. pure theory "consider a spherical cow"http://en.wikipedia.org/wiki/Spherical_cow 2. copper models (painted) Dzialowski, E. M. 2005. Use of operative temperature and standard operative temperature models in thermal biology. Journal of Thermal Biology 30:317-334. Sometimes these models can do a good job of predicting temperatures of animals (or plants) without having to measured them directly. If so, this allows application to broad-scale studies in both space and time, including predicitons of effects of climate change.

14. Thermoregulation was generally viewed asonly a good thing, because our frame of reference was Homo sapiens. What might be the problems associated with temperature variability?

15. Later, it was recognized that thermoregulation also has costs. What might be the costs of thermoregulation?

16. Later, it was recognized that thermoregulation also has costs. What might be the costs of thermoregulation? a. exposure to predators b. increased metabolic rate and hence energy costs c. lost opportunity to do other things So, focus changed to the relative costs and benefits of thermoregulation. Sometimes better to allow Tb to vary, and many organisms do just that.

17. For example, some lizards do not bask in the sun, but rather are thermoconformers.

18. The same species in two different habitats: Huey, R. B., and M. Slatkin. 1976. Cost and benefits of lizard thermoregulation. Quart. Rev. Biol. 51:363-384.

19. An Extreme Thermoconformer Australian Gecko Nephrurus laevissimus Eric Pianka, U. Texas Biology 213, 9th.Lecture.ppt

20. Thus, multiple solutions are possible, and one is not necessarily "better" than another.

21. 3. Body size affects nearly every biological variable. (we will return to this in a later lecture … have already mentioned brain size example)

22. 4. Behavior is an important component of functional adjustment to the environment. Laboratory physiologists go to extreme lengths to standardize measurement conditions and to control extraneous variables. This is necessary to obtain values that can be compared across studies, across labs, and across species.

23. But it can make the measurements of low relevance to what goes on in nature. • A trade-off exists between getting precisely controlled physiological measurements and making those measurements ecologically relevant. • Behavioral adjustments are often not seen in lab settings, either because they are just impossible, or because the animal is "stressed out" and isn't acting normally. • Examples: wild rodents often huddle; • forced diving in seals leads to abnormal physiological responses.

24. Only way to overcome this is with field observations of free-living animals and a thorough understanding of their natural history and behavior. Many animals simply avoid the most stressful of conditions that occur in their environment. Examples: most desert rodents are nocturnal; many arctic or high-altitude animals hibernate. Recent technological advances, e.g., miniaturized radio transmitters coupled with thermometers, motion detectors, or force transducers, are allowing measurements of free-living animals. May also be coupled with GPS to get movement data.

25. 5. Animals ARE adapted to their environment. Trivially, one can show that organisms can indeed live where they do! But it is not always obvious how they will be doing it. Will they have adapted physiologically, morphologically, or perhaps "only" behaviorally, e.g., nocturnal animals avoid daytime heat extremes? Example: Lake Titicaca frog does multiple things, but not all things.

26. Lake Titicaca: at high-altitude(3,800 meters or 12,500 feet) in South America

27. world's highestnavigable lake

29. Hutchison, V. H., H. B. Haines, and G. Engbretson. 1976. Aquatic life at high altitude: respiratory adaptations in the Lake Titicaca frog, Telmatobiusculeus. Respiration Physiology 27:115-129. • "Telmatobiusculeus has a combination of behavioral, morphological and physiological adaptations which allows an aquatic life in cool (10 oC) O2-saturated (at 100 mm Hg) waters at high altitude (3,812 m).” • Rarely surfaces to breathe. • Greatly reduced lungs. • Pronounced folds on skin, with cutaneous capillaries penetrating to outer layers.

30. If prevented from surfacing in hypoxic waters, use "bobbing" behavior to ventilate skin. • "The oxygen transport properties of the blood show several distinct adaptations for an aquatic life at high altitude.” • erythrocyte counts ... greater than that reported for any frog • erythrocyte volume is the smallest ... known among amphibians • hematocrit (%) of 27.9 is within the range of most amphibians • oxygen capacity (ml/100 ml) of 11.7 is fairly high among amphibians

31. hemoglobin content (g/100 ml) falls within the upper range of amphibians • mean cell hemoglobin concentration (pg/um3) of 0.281 is in the upper range of those previously observed in amphibians • lowest P50 of any frog at comparable temperature (10 oC)"

32. Summary: Smallest red blood cells of any amphibian. Most red blood cells per volume blood. Lowest P50. Relatively high hematocrit, hemoglobin concentration, and O2 capacity of blood. Low resting metabolic rate. Note that the authors assumed that everything they saw was an adaptation!!! Did not specifically ask: what does the closest relative that does not at high altitude look like? Not what modern evolutionary physiology would do.

33. A similar example: African ranid frog Trichobatrachus robustus. During the breeding season, males have long, hair-like projections of vascularized epidermis. They are known to sit on clutches of eggs in streams, and presumably the "hairs" function to increase cutaneous respiration, thereby allowing males to remain under water for longer periods of time (Duellman and Trueb, 1986). Multiple solutions …

34. 6. The organism is a compromise. The result of natural selection is adequacy and not perfection. Although animals are indeed adapted to their environments, they are far from perfectly so. All sorts of constraints prevent organisms from being the best that might be theoretically possible. It has often been said that organisms "make the best of a bad situation," but it is not clear that they even do that! (we will have a whole lecture on this later …)

35. 7. Physiology-environment correlations can be seen at molecular and cellular levels as well as at higher levels. But still better to start with behavior, whole-organism performance, and work your way down. More "accomplishments" from: Feder, M. E. 1987. The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology. Pp. 38-75 in M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey, eds. New directions in ecological physiology. Cambridge University Press, Cambridge, U.K.

36. 8. "Behavior" and "morphology" should be considered coequal with "physiology" in our analyses. More "accomplishments" from: Feder, M. E. 1987. The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology. Pp. 38-75 in M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey, eds. New directions in ecological physiology. Cambridge University Press, Cambridge, U.K.

37. 9. Microclimate may be more meaningful than gross climate in characterizing physiology-environment correlations. For example, small organisms can find many places out of the sun or wind. They do not face the world on our scale. More "accomplishments" from: Feder, M. E. 1987. The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology. Pp. 38-75 in M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey, eds. New directions in ecological physiology. Cambridge University Press, Cambridge, U.K.

38. 10. Organisms from extreme environments may exhibit very obvious physiology-environment correlations. More "accomplishments" from: Feder, M. E. 1987. The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology. Pp. 38-75 in M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey, eds. New directions in ecological physiology. Cambridge University Press, Cambridge, U.K.

39. 11. Function of a part in the context of a whole organism may yield different insights than function of a part in isolation in an experimental preparation. For example, the thermal dependence of an isolated enzyme or organ may not match the thermal dependende of whole-organism performance. More "accomplishments" from: Feder, M. E. 1987. The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology. Pp. 38-75 in M. E. Feder, A. F. Bennett, W. W. Burggren, and R. B. Huey, eds. New directions in ecological physiology. Cambridge University Press, Cambridge, U.K.

40. Evolution and thePhenotypic Hierarchy Reading: Garland, T., Jr., and P. A. Carter. 1994. Evolutionaryphysiology. Annual Review of Physiology 56:579-621.

41. A General Question: • How do traits atdifferent levels of biological organization evolve in a coherent fashion?

42. Behavior OrganismalPerformance OrganSystems Organs Tissues Cells Organelles Proteins, etc. DNA Darwinian Fitness:age at 1st reprod., fecundity, lifespan Organisms are complex and hierarchical entities.

43. Although scientists tend to specialize on particular levels of biological organization, organisms evolve as coordinated wholes. Therefore, cross-disciplinary studies are required to understand how organisms work and evolve. The inseparability of physiology from behavior and from the environmental context has long been a central tenant of physiological ecology. For example: when challenged by cold, endotherms can change their posture (body shape) to reduce heat loss, move to a warmer area, or huddle with other individuals.

44. But only in the last 20 years or so have attempts been made to formalize such relationships conceptually and in operational terms. Nonetheless, the general problem has long been appreciated ....

45. "The whole organism is so tied together that when slight variations in one part occur, and are accumulated through natural selection, other parts become modified. (Darwin, 1859, The Origin of Species) This is avery important subject, mostimperfectly understood."

46. Darwinian Fitness:age at 1st reprod., fecundity, lifespan Behavior Selection = a correlation between fitness and one or more traits at lower levels of organization. OrganismalPerformance OrganSystems Organs Tissues Cells Organelles Proteins, etc. DNA

47. Darwinian Fitness:age at 1st reprod., fecundity, lifespan Behavior OrganismalPerformance OrganSystems In nature, selection may often act most directly on behavior. Organs Tissues Cells Organelles Proteins, etc. DNA

48. "Many if not most acquisitions of new structures in the course of evolution can be ascribed to selection forces exerted by newly acquired behaviors ... (Mayr, 1982, p. 612) Behavior, thus, plays an important role as the pacemaker of evolutionary change. Most adaptive radiations were apparently caused by behavioral shifts."

49. Darwinian Fitness:age at 1st reprod., fecundity, lifespan Behavior Wherever it acts, selectionmay cause changes in other traits at that level, and at other levels, but perhaps with some lag. OrganismalPerformance OrganSystems Organs Tissues Cells Organelles Proteins, etc. DNA

50. Behavior A Simple Model of Correlated Responses to Selection on Behavior: The "Behavior Evolves First" Hypothesis OrganismalPerformance OrganSystems Organs Tissues Cells Organelles Proteins, etc.