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Lecture 2:
Accomplishments of
Physiological Ecology;
Evolution and the
Phenotypic 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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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.
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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
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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.
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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
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!)
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Body Temperature (°C)
W estern Fence Lizard (S celoporus occidentalis)
Table Mtn. (elev. 7200', near W rightwood)
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y = 33.2 + 0.0627x R2= 0.00339
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Air Temperature (°C)
http://www.wildherps.com/species/S.occidentalis.html
Data from Prof. Stephen C. Adolph, Department of Biology, Harvey Mudd College,
Claremont, California
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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 as
only 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 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.
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For example, some lizards do not bask in the sun,
but rather are thermoconformers.
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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.
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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
world's highest
navigable 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 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
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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)"
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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, wholeorganism 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.
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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9. Microclimate may be more meaningful than
gross climate in characterizing physiologyenvironment 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.
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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.
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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.
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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Evolution and the
Phenotypic Hierarchy
Reading:
Garland, T., Jr., and P. A. Carter. 1994. Evolutionary
physiology. Annual Review of Physiology 56:579-621.
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A General Question:
How do traits at
different levels of
biological organization
evolve in a coherent
fashion?
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Darwinian Fitness:
age at 1st reprod., fecundity, lifespan
Behavior
Organismal
Organ Performance
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
DNA
Organisms are
complex and
hierarchical
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 part occur, and
are accumulated through
natural selection, other parts
become modified. This is a
very important subject, most
imperfectly understood."
(Darwin, 1859, The Origin of Species)
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Darwinian Fitness:
age at 1st reprod., fecundity, lifespan
Behavior
Organismal
Organ Performance
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
DNA
Selection =
a correlation
between
fitness and
one or more
traits at lower
levels of
organization.
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Darwinian Fitness:
age at 1st reprod., fecundity, lifespan
Behavior
Organismal
Organ Performance
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
DNA
In nature,
selection may
often act most
directly on
behavior.
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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 ...
Behavior, thus, plays an important
role as the pacemaker of
evolutionary change. Most adaptive
radiations were apparently caused
by behavioral shifts."
(Mayr, 1982, p. 612)
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Darwinian Fitness:
age at 1st reprod., fecundity, lifespan
Behavior
Organismal
Organ Performance
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
DNA
Wherever it
acts, selection
may cause
changes in
other traits at
that level, and
at other levels,
but perhaps
with some lag.
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Behavior
Organismal
Performance
Organ
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
A Simple Model of
Correlated Responses
to Selection on
Behavior: The
"Behavior Evolves
First" Hypothesis
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Behavior
Organismal
Performance
Organ
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
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Behavior
Organismal
Performance
Organ
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
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Behavior
Organismal
Performance
Organ
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
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Behavior
Organismal
Performance
Organ
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
55
Behavior
Organismal
Performance
Organ
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
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Behavior
Organismal
Performance
Organ
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
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Behavior
Organismal
Performance
Organ
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
An apparent
example is
on the next
slide …
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Cinclus mexicanus
Figure 3 (page 257) from D. J. Futuyma.
1986. Evolutionary biology. 2nd. Ed. Sinauer
Associates, Sunderland, Massachusetts.
The Dipper
dives to
forage.
Presumably,
selection
favored diving
to exploit an
underutilized
food resource.
Homework: Check
YouTube for movies
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Cinclus mexicanus
Figure 3 (page 257) from D. J. Futuyma.
1986. Evolutionary biology. 2nd. Ed. Sinauer
Associates, Sunderland, Massachusetts.
But dippers
show relatively
few morphological or
physiological
specializations
that might
enhance the
ability to dive.
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Natural
& Sexual
Selection
Act
On
Behavior
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Natural
& Sexual
Selection
Act
On
Behavior
Organismal
Performance
Abilities
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Natural
& Sexual
Selection
Act
On
Morphology, DeterPhysiology,
Biochemistry mine
Behavior
Organismal
Performance
Abilities
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Natural
& Sexual
Selection
Act
On
Behavior
This model presumes
that animals can be
maximally motivated to
perform ...
Morphology, DeterPhysiology,
Biochemistry mine
Organismal
Performance
Abilities
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Natural
& Sexual
Selection
Act
On
Behavior
The model is also
too simple because
it leaves out such
things as direct
effects of hormones
on behavior.
Morphology, DeterPhysiology,
Biochemistry mine
Organismal
Performance
Abilities
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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:
1. correlating leg length with habitat usage of
lizards, without ever showing empirically that leg
length affects some measure of performance,
such as sprinting or climbing abilities.
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Performance was
not measured.
Instead, it was
inferred from
morphology.
2. correlating bill dimensions of birds with diet,
without showing that bill proportions actually
affect feeding abilities on different types of food.
Performance was
not measured.
Instead, it was
inferred from
morphology.
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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.
Performance was
not measured.
Instead, it was
inferred from
morphology.
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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.
(minutes)
Performance of the whole organism was not measured.
Instead, it was implicitly inferred from biochemistry.
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.)
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Performance of the whole organism was not measured.
Instead, it was implicitly inferred from the isolated muscle.
Maximum
isometric twitch
tension of lizard
muscles is
positively
correlated with
PBT across
species
(Licht, Dawson,
and Shoemaker,
1969).
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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 organismal
performance to allow a clear link between lowerlevel 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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Stopped here 14 Jan. 2014
Extra Slides
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Darwinian Fitness:
age at 1st reprod., fecundity, lifespan
Behavior
Organismal
Organ Performance
Systems
Organs
Tissues
Cells
Organelles
Proteins, etc.
DNA
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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.