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

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

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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.

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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.

The Accomplishments of Physiological Ecology

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Measurement of energy exchange leads easily to links with behavior and ecology:

1. optimal foraging theory - costs andbenefits usually phrased in energy

2. population- and community-level usageof energy affect ecosystem dynamics

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Measurement of energy exchange leads easily to links with behavior and ecology:

1. optimal foraging theory - costs andbenefits usually phrased in energy

2. population- and community-level usageof 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.

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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.Development of a quick-reading mercury thermometer was a technological advance that allowed study of body temperatures of lizards.

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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

8Cowles, 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!)

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Western Fence Lizard (Sceloporus occidentalis)Table Mtn. (elev. 7200', near Wrightwood)

y = 33.2 + 0.0627x R2= 0.00339

Bod

y Te

mpe

ratu

re (°

C)

Air Temperature (°C)

Data from Prof. Stephen C. Adolph, Department of Biology, Harvey Mudd College,Claremont, California

http://www.wildherps.com/species/S.occidentalis.html

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And later telemetry was used …

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

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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.

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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.

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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?

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

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

a. exposure to predatorsb. increased metabolic rate and hence

energy costsc. 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.

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

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

The same species in two different habitats:

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An Extreme Thermoconformer

Australian Gecko

Nephrurus laevissimus

Eric Pianka, U. Texas Biology 213, 9th.Lecture.ppt

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

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

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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.

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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.

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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.

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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.

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

27world's highestnavigable lake

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Hutchison, V. H., H. B. Haines, and G. Engbretson. 1976. Aquatic life at high altitude: respiratory adaptations in the Lake Titicaca frog, Telmatobius culeus. Respiration Physiology 27:115-129."Telmatobius culeus 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.

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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 frogerythrocyte volume is the smallest ... known among amphibianshematocrit (%) of 27.9 is within the range of most amphibiansoxygen capacity (ml/100 ml) of 11.7 is fairly high among amphibians

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

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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.

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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 …

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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 …)

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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.

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8. "Behavior" and "morphology" should be considered coequal with "physiology" in our analyses.


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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.


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10. Organisms from extreme environments may exhibit very obvious physiology-environment correlations.


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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.


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Evolution and thePhenotypic Hierarchy

Reading:

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

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A General Question:How do traits atdif ferent levels of biological organization evolve in a coherent fashion?

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DNAProteins, etc.

OrganellesCells

TissuesOrgans

OrganSystems

OrganismalPer formance

Behavior

DarDar winian Fiwinian Fi tt ness:ness:age at 1st reprod., fecundity, lifespanage at 1st reprod., fecundity, lifespan

Organisms are complex and complex and hierarchicalhierarchical entities.

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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.

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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 ....

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"The whole organism is so tied together that when slight variations in one par t occur, and are accumulated through natural selection, other parts become modified.

(Darwin, 1859, The Origin of Species)

This is aver y impor tant subject, mostimper fectly understood."

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DNAProteins, etc.

OrganellesCells

TissuesOrgans

OrganSystems


Behavior


Selection =a correlation between fitness and one or more traits at lower levels of organization.

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DNAProteins, etc.

OrganellesCells

TissuesOrgans

OrganSystems


Behavior

In nature, selection may of ten act most directly on behaviorbehavior.


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"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."

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DNAProteins, etc.

OrganellesCells

TissuesOrgans

OrganSystems


Behavior Wherever it acts, selectionmay cause changes in other traits at that level, and and at other levelsat other levels, but perhaps with some laglag.


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Proteins, etc.

Organelles

Cells

Tissues

Organs

OrganSystems


Behavior A Simple Model of Correlated Responses

to Selection on Behavior: The The

"Behavior Evolves "Behavior Evolves First" HypothesisFirst" Hypothesis

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Proteins, etc.

Organelles

Cells

Tissues

Organs

OrganSystems


Behavior

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Proteins, etc.

Organelles

Cells

Tissues

Organs

OrganSystems


Behavior

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Proteins, etc.

Organelles

Cells

Tissues

Organs

OrganSystems


Behavior

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Proteins, etc.

Organelles

Cells

Tissues

Organs

OrganSystems


Behavior

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Proteins, etc.

Organelles

Cells

Tissues

Organs

OrganSystems


Behavior

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Proteins, etc.

Organelles

Cells

Tissues

Organs

OrganSystems


Behavior

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Proteins, etc.

Organelles

Cells

Tissues

Organs

OrganSystems


Behavior

An apparent example is on the next slide …

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Figure 3 (page 257) from D. J. Futuyma. 1986. Evolutionary biology. 2nd. Ed. Sinauer Associates, Sunderland, Massachusetts.

The DipperThe Dipperdives to dives to forage.forage.Presumably, Presumably, selection selection favored diving favored diving to exploit an to exploit an underutilized underutilized food resource.food resource.

Cinclus mexicanus

Homework: Check YouTube for movies

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Figure 3 (page 257) from D. J. Futuyma. 1986. Evolutionary biology. 2nd. Ed. Sinauer Associates, Sunderland, Massachusetts.

But dippers show rr elativelyelatively few morpho-few morpho-logical or logical or physiological physiological specializationsspecializations that might enhance the ability to dive.

Cinclus mexicanus

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Natural& Sexual Selection

BehaviorAct On

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BehaviorAct On

Organismal Performance

Abilities

Constrain

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BehaviorAct On


Abilities

Constrain

Morphology,Physiology,Biochemistry

Deter- mine

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BehaviorAct On


Abilities

Constrain


Deter- mine

This model presumes that animals can be maximally motivated to perform ...

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BehaviorAct On


Abilities

Constrain


Deter- mine

Hormones

The model is also too simple because it leaves out such things as direct effects of hormones on behavior.

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Traditionally, many studies in morphology and physiology would just study traits at the lowest level (morphology, physiology, biochemistry), and then try to correlate variation here with variation in behavior or ecology.Organismal performance was not measured.

Examples:

661. correlating leg length with habitat usage of lizards, without ever showing empirically that leg length affects some measure of per formance, such as sprinting or climbing abilities.

Performance was not measured. Instead, it was inferred from morphology.

672. correlating bill dimensions of birds with diet, without showing that bill proportions actually affect feeding abilities on different types of food.


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3. correlating wing dimensions of birds or bats with lifestyle, generally in the absence of studies measuring effects of wing dimensions on flying abilities.


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4. relating the thermal dependence of an enzyme activity or of the contractile properties of isolated muscles to the temperature at which animals normally live.

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Time required for exposure to 37oC to inactivate myofibrillar ATPase is positively correlated with thermal environment across species of fish(Fig. 3.2c of Feder 1987. From Johnston, I. A., and N. J. Walesby. 1977. Molecular mechanisms of temperature adaptation in fish myofibrillar adenosine triphosphatases. Journal of Comparative Physiology 119:195-206.)

(min

utes

)

Performance of the whole organism was not measured. Instead, it was implicitly inferred from biochemistry.

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Maximum isometric twitch tension of lizard muscles is positively correlated with PBT across species(Licht, Dawson, and Shoemaker, 1969).

Performance of the whole organism was not measured. Instead, it was implicitly inferred from the isolated muscle.

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A major conceptual advance in the last 25 years has been adopting the perspective that you really need to make some measures of organismalper formance to allow a clear link between lower-level traits and behavior/ecology.

It is somewhat surprising that performance was not measured, because in many cases it is not that difficult. For example, to measure frog jumping performance, about all you need is a tape measure and a thermometer. However, you do need to have live, healthy animals.

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Extra Slides Follow ...

Stopped here 14 Jan. 2014

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DNAProteins, etc.

OrganellesCells

TissuesOrgans

OrganSystems


Behavior


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Phylogeny - "tree of life" indicating relatively how recently different species (or lineages) diverged from each other. Can be estimated in various ways, such as comparisons of morphology or DNA sequences.

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Why do birds migrate?Why do birds sing?See Mayr (1961) for discussion of "proximate" versus "ultimate" types of explanations for biological phenomena.

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Chapin, F.S. III, K. Autumn, and F. Pugnaire. 1993. Evolution of suites of traits in response to environmental stress. Am. Nat. 142:S78-S92.

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