Transcript 174-16-Winter_7_26_J..

Lecture 9 & 10:
Evolution of
Endothermy
1
Endothermy has evolved multiple times in
both animals and plants:
birds and mammals, or their ancestors
2
Endothermy has evolved multiple times in
both animals and plants:
some reptiles (brooding pythons, large sea
turtles, maybe dinosaurs,
pterosaurs)
3
Endothermy has evolved multiple times in
both animals and plants:
scombrid fishes (e.g., tunas and billfishes)
lamnid sharks
4
Endothermy has evolved multiple times in
both animals and plants:
insects (e.g., moths, bees
some
beetles)
5
Endothermy has evolved multiple times in
both animals and plants:
at least eight genera of plants within the
family Araceae
6
Endothermy is often considered to
represent a "key innovation,"
i.e., a characteristic that allows a
fundamentally new way of life and may lead
to an adaptive radiation.
If so, then we should be able to recognize
clear benefits (advantatges) of endothermy,
while also identifying costs (disadvantages).
7
Costs/Benefits of Ectothermy/Endothermy
Early comparative physiologists assumed that
ectothermy was "primitive" and, in general,
inferior to endothermy, e.g.,
"lower" vs. "higher" vertebrates.
Now, it is recognized that many characteristics
of "lower" vertebrates are actually
specializations that promote a low-energy
lifestyle.
A general separation in average body sizes
also exists.
Low energy requirements go along with small
body size:
8
Body Mass Distributions
K. S. Kilburn,
Old Dominion University
… and small endotherms have severe
problems with heat loss because of
unfavorable surface/volume ratios.
9
Costs/Benefits of Ectothermy/Endothermy
Ectotherm Benefits:
Do not spend direct metabolic energy on
thermoregulation
Can spend more on growth and reproduction
Require less food overall than do endotherms
10
Allometry of field
metabolic rate based
on doubly labeled water
studies (excluding animals
that were seasonally inactive
[hibernating mammals,
overwintering reptiles]).
Note that the lowest
mammal and the
highest reptiles
overlap!
Lines are least-squares
linear regressions plus
95% prediction intervals.
Nagy, K. A., I. A. Girard, and T. K. Brown. 1999. Energetics of free-ranging mammals, reptiles, and birds. Annual Review of Nutrition 19:247-277.
11
For all data:
Note that birds
tend to be higher
than mammals.
Nagy, K. A. 2005. Field metabolic rate and body size. Journal of Experimental Biology 208:1621-1625.
12
Legend for previous slide:
Nagy, K. A. 2005. Field metabolic rate and body size. Journal of Experimental Biology 208:1621-1625.
13
Nagy, K. A. 2005. Field metabolic rate and body size. Journal of Experimental Biology 208:1621-1625.
14
Costs/Benefits of Ectothermy/Endothermy
Ectotherm Benefits:
Do not spend direct metabolic energy on
thermoregulation
Can spend more on growth and reproduction
Require less food overall than do endotherms
Can spend less time in risky foraging activities
Lose less water by evaporation because their
metabolic rate is lower and because their Tb is
generally lower
Generally "preadapted" for life
in hot deserts
15
Costs/Benefits of Ectothermy/Endothermy
Ectotherm Costs:
Activity times more constrained on a daily and
seasonal basis
Cannot sustain high work rates aerobically
(lower maximal aerobic speed)
16
Costs/Benefits of Ectothermy/Endothermy
Endotherm Benefits:
Are more independent of ambient temperature
on a daily and seasonal basis, as well as
latitudinally and altitudinally
Can grow more rapidly
17
GRAMS
Mammals similar to precocial
birds; altricial birds are higher
Slope for
mammals
= 0.72
Case, T. J. 1978. On the evolution and adaptive
significance of postnatal growth rates in the
terrestrial vertebrates. Q. Rev. Biol. 53:243-282.
18
GRAMS
Reptiles and fishes are
lower than birds &
mammals
Case, T. J. 1978. On the evolution and adaptive
significance of postnatal growth rates in the
terrestrial vertebrates. Q. Rev. Biol. 53:243-282.
19
Costs/Benefits of Ectothermy/Endothermy
Endotherm Benefits:
Are more independent of ambient temperature
on a daily and seasonal basis, as well as
latitudinally and altitudinally
Can grow more rapidly
Can sustain high rates of work aerobically
(higher maximal aerobic speed)
Long-distance migrations
Powered flight in relatively larger animals
Intense feeding of offspring
McClellan, C. M., and A. J. Read. 2007. Complexity and variation in
loggerhead sea turtle life history. Biology Letters 3:592-594. [long-distance movements, tied to endothermy?]
Enzymes can function more efficiently over a
narrower temperature range
20
Costs/Benefits of Ectothermy/Endothermy
Endotherm Costs:
Need a lot more food
Need larger home ranges and spend more
time foraging, conspicuously, and may be
more apparent to predators
Note that many ectotherms (e.g., lizards) combine
activities (multitask), alternating between basking,
foraging, signaling, defending their territories,
looking for mates, watching for predators
Stopped here 4 Feb. 2014
21
Where did endothermy evolve in the lineage
leading to modern mammals?
What characterizes a modern mammal?
Endothermy
High Metabolic Rate
Homeothermy
Response to Lowered Ambient Temperature
(shivering + non-shivering thermogenesis)
Fur or Hair
Most of these features are
Live Birth
absent or unclear in the
Parental Care
fossil record.
Lactation
Large Brain
4-chambered Heart
22
In the fossil record, mammals are defined mainly
by the presence of a single bone (dentary) in the
lower jaw.
Other fossil-visible features include:
Multi-cuspid Teeth,
Differentiated Along the Jaw
Secondary Palate
Upright Posture
Large Brains
These changes occur gradually in the fossil
record. If or how they are associated with
endothermy is often unclear.
Stopped here 3 Feb. 2015
23
The endothermy of birds and mammals is
distinctive, because at rest it results primarily
from metabolic heat production by visceral organs
(and the brain) rather than by muscles.
The endothermy of pythons, scombrid fishes,
sharks, and sea turtles results primarily, but
perhaps not exclusively, from myogenic heat
production coupled with relatively large body size
The endothermy of insects is also myogenically
based, but given their small size, endothermy in
insects also requires a highly effective insulation.
24
Only birds and mammals have metabolic rates
high enough and insulation effective enough (or
body size large enough) that they can maintain
body temperatures elevated above ambient while
at rest and in the absence of contractions by
skeletal muscles.
(If the slow swimming needed to ventilate the gills
of obligate ram ventilators is equated with the
effort needed to ventilate the lung of a bird or
mammal, then it can be argued that some fishes
also maintain elevated body temperatures while at
rest, i.e., during slow swimming.)
25
Increased resting metabolic rate has been
hypothesized to be associated with selection for:
1) thermal niche expansion (Bakken and Gates 1975;
Crompton et al. 1978; Block et al. 1993)
2) homeothermy (stable body temperature) and
increased metabolic efficiency
(Heinrich 1977; Avery 1979)
3) commitment to inertial homeothermy followed
by decreasing body size (McNab 1978)
4) postural changes that enhance exercise
performance (Heath 1968, cf. Carrier 1987)
5) increased brain size (cf. Hulbert 1980)
26
6) increased aerobic capacity during exercise
(Regal 1978; Bennett and Ruben 1979)
7) parental care
(Case 1978; Farmer 1998, 2000; Koteja 2000)
Case, T. J. 1978. Endothermy and parental care in the terrestrial vertebrates. American Naturalist 112:861-874.
Farmer, C. G. 1998. Hot blood and warm eggs. Journal of Vertebrate Paleontology 18, suppl. 3
(Abstracts. Fifty-eighth Annual Meeting of the Society of Vertebrate Paleontology), 40A.
Farmer, C. G. 2000. Parental care: the key to understanding endothermy and other convergent features in birds and mammals.
American Naturalist 155:326-334.
Koteja, P. 2000. Energy assimilation, parental care and evolution of endothermy. Proc. Royal. Soc. Lond. B 267:479-484.
Angilletta, M. J. and M. W. Sears. 2003. Parental care as a selective factor for the evolution of endothermy?
American Naturalist 162:821-825.
Farmer, C. G. 2003. Reproduction: The adaptive significance of endothermy. American Naturalist 162:826-840.
8) resting metabolic rate set to optimize
cardiovascular O2 transport
(Krosniunas and Gerstner 2003)
27
Recent attempts to elucidate the selective
regime(s) responsible for the evolution of avian
and mammalian endothermy (i.e., ultimate causes)
have focused principally on #6, which is now
termed the aerobic capacity model.
28
Bennett and Ruben (1979) argued that selection
for higher capacity for sustainable activity,
supported by aerobic metabolic rate, was
important during the evolution of endothermy.
They noted that the energy (food) cost of
increasing resting metabolic rate was high
compared to the thermoregulatory benefits,
especially for small increases in resting
metabolism, for which thermoregulatory
improvements would be insignificant.
In contrast, any increase in maximal aerobic
capacity will be reflected in higher capacity for
sustainable activity.
29
The aerobic capacity model has two major parts.
1. directional selection related to activity capacity
resulted in the evolution of a higher maximal
aerobic metabolic rate.
Increase in VO2max would increase maximal
aerobic speed and thus enable animals to exercise
longer at higher levels.
This would be advantageous for many
reasons, e.g., better at capturing prey or
defending territories, able to traverse and hence
forage over greater areas.
However, higher aerobic capacity by itself would
not result in endothermy of resting animals.
30
2. maximal and resting metabolism are somehow
linked in a causal, mechanistic sense; thus,
evolutionary changes in the two traits cannot
occur independently.
This idea was based on the empirical
observation that in vertebrates maximal oxygen
consumption during exercise (VO2max) is typically
5-10 times resting oxygen consumption.
31
"Thus there appears to be a consistent linkage
between resting and maximal levels of oxygen
consumption in the vertebrates. When an animal
is in any given physiological state, oxygen
consumption may increase an average of only
five- to tenfold." (Bennett and Ruben 1979, p. 651)
They saw what they interpreted as a relatively
constant factorial aerobic scope, and viewed this
as indicative of a fundamental property of
vertebrate physiology.
But they concluded that the mechanisms
underlying such a relationship between activity
and resting metabolic rate were unclear.
32
One simple verbal model is the Volkswagen Ferrari analogy.
Does not use
much gas,
but cannot go
very fast.
Goes really
fast, but
uses a lot of
gas even
when idling.
33
Whatever the mechanism might be, the aerobic
capacity model assumes that selection for
increased maximum aerobic capacity will
necessarily result in increased resting metabolic
rate and, eventually, endothermy.
Note that this model is an interesting mix of
ultimate and proximate explanations for why and
how mammalian and avian endothermy evolved!
Some of the other ideas about the evolution of
endothermy (see slides 26-27) also mix these
levels, which is not a bad thing.
This would make a good exam question!
34
How can we test the aerobic capacity model?
In general, a model can be tested by testing its
predictions or by testing its assumptions.
Let's go through 5 possible tests that get at one or
the other.
35
1. If we intentionally selected for a higher
VO2max, then resting metabolic rate would be
predicted to increase more-or-less in parallel.
Hayes and colleagues bred 4 replicate lines of laboratory house mice for high
mass-independent VO2max during forced treadmill exercise (Wone et al. 2015
Heredity). The selection criterion included body mass as a covariate, so selection
was independent of effects of body mass on metabolic rate. 4 additional lines were
maintained as non-selected controls. Compared with controls, VO2max significantly
increased by 11.2% in lines bred for VO2max, while BMR did not change significantly
(+2.5%).
Koteja and colleagues bred 4 replicate lines of wild voles for swim-induced aerobic
capacity (Stawski et al. 2015 Comp. Biochem. Physiol. A 180:51-56) and got some
correlated response in BMR, but not maintaining the same factorial increase (i.e.,
BMR did not increase nearly as much as VO2max).
These studies offer, at most, weak support for the aerobic capacity model.
Of course, the relevance of small living rodents for (large?) therapsids is unclear.
36
2. If we estimated the additive genetic correlation
between VO2max and resting metabolic rate, it
would be positive and high.
Genetic correlations can be estimated much more
easily than doing a selection experiment (need fewer
generations), but the evidence they provide is not as
strong.
In laboratory house mice, Dohm et al. (2001) found weak evidence for a positive
additive genetic correlation.
In wild voles, the additive genetic correlation between BMR and the swim-induced
aerobic capacity was high and positive (Sadowska et al. 2005).
Some support for the aerobic capacity model.
37
3. What about the phenotypic correlation between
VO2max and resting metabolic rate?
Estimates of the phenotypic correlations
within species are much easier to obtain.
They were compiled in Hayes and Garland (1995),
and the following table gives their results with some
updates:
38
Species
Pear-
n
son's r
1-tailed Source
P
Amphibians
Bufo woodhousii
0.374
38
0.0104
Walton 1988
Callisaurus draconoides
0.224
20
0.1712
Garland, unpub. data
Chalcides ocellatus
0.089
28
0.3261
Pough and Andrews 1984
Cnemidophorus tigris
-0.010
24
0.5185
Garland, unpub. data
Ctenophorus nuchalis
0.219
56
0.0524
Garland and Else 1987
Ctenosaura similis
0.122
18
0.3148
Garland 1984
Dipsosaurus dorsalis
0.176
70
0.0725
John-Alder 1984
Sceloporus undulatus
0.318
47
0.0145
Pierce & John-Alder, pers. com.
0.11
250
0.0413
Walton, Bennett, Peterson, p.c.
Lizards
Snakes
Thamnophis sirtalis
39
Species
Pear-
n
son's r
1-tailed Source
P
Mammals
Peromyscus maniculatus - cold exp.
0.318
50
0.0122
Hayes 1989
Spermophilus beldingi
0.31
95
0.0011
M. A. Chappell, pers. comm.
Spermophilus beldingi - cold exp.
0.005
95
0.4804
M. A. Chappell, pers. comm.
Mus domesticus
0.05
337
n.s.
Dasypus novemcinctus - cold exp.
0.45
47
<0.005
Dohm et al. 2001
Boily 2002
Take-home message:
phenotypic correlations tend to be positive.
However, the picture for anuran amphibians is much less
consistently positive …
40
Gomes, F. R., J. G. Chauí-Berlinck, J. E. P. W. Bicudo, C. A. Navas. 2004.
Intraspecific relationships between resting and activity metabolism
in anuran amphibians: influence of ecology and behavior.
Physiological and Biochemical Zoology 77:197-208.
Studied 21 Neotropical species of anuran amphibians
(frogs and toads) from different geographical areas that
include remarkable diversity in behavior & thermal ecology.
"The three possible trends (positive, negative, and absent
correlations) were observed and appeared to be predictable from
ecological and behavioral variables that relate to evolutionary
physiological shifts in anurans. Positive correlations between
VO2rest and VO2act were more common in species with active
lifestyles (e.g., intense vocal activity) and in species that call at
low temperatures (e.g., winter or high-elevation specialists)."
41
Gomes, F. R., J. G. Chauí-Berlinck, J. E. P. W. Bicudo,
C. A. Navas. 2004. Intraspecific relationships between
resting and activity metabolism in anuran amphibians:
influence of ecology and behavior. Physiological and
Biochemical Zoology 77:197-208.
42
Also, even when the correlations are
positive, they are << 1.00, so it does not
seem that selection only to increase
VO2max would cause SMR or BMR to go
up in parallel (thus maintaining the
putative 5-10-fold ratio).
43
4. If we compared species, we would find a
positive correlation between VO2max and
resting metabolic rate.
Several studies have done this, with mostly
positive results (summary table follows).
For small birds and mammals, some have use
maximum cold-induced metabolic rate (MMR),
rather than VO2max.
Helium-oxygen may be used to increase heat
loss.
MMR sometimes > VO2max …
Not all analyzed phylogenetically (later lectures).
Here is most recent example for rodents ...
44
Rezende, E. L.,
F. Bozinovic, and
T. Garland, Jr. 2004.
Climatic adaptation and
the evolution of basal
and maximum rates of
metabolism in rodents.
Evolution 58:1361-1374.
57 species or
populations of
rodents
45
Rezende, E. L.,
F. Bozinovic, and
T. Garland, Jr. 2004.
Climatic adaptation and
the evolution of basal
and maximum rates of
metabolism in rodents.
Evolution 58:1361-1374.
Maximum metabolic
rate in cold with
helium-oxygen
46
r = 0.5
P < 0.001
Rezende, E. L., F. Bozinovic,
and T. Garland, Jr. 2004.
Climatic adaptation and the
evolution of basal and
maximum rates of
metabolism in rodents.
Evolution 58:1361-1374.
47
Summary of Studies on Interspecific Correlations
Tropical Birds P
VO2max
0.406
30
0.0130
Wiersma et al., 2007
Rezende, E. L., F. Bozinovic, and T. Garland, Jr. 2004. Climatic adaptation and the evolution
of basal and maximum rates of metabolism in rodents. Evolution 58:1361-1374.
Wiersma, P., M. A. Chappell, and J. B. Williams. 2007. Cold- and exercise-induced peak metabolic rates in tropical
birds. PNAS 104:20866-20871.
48
These positive interspecific correlations are
consistent with the aerobic capacity model, but a
similar pattern could arise if:
selection favored high resting metabolic rate
and maximal metabolic rate followed;
selection simultaneously favored both high
resting and maximal.
Therefore, we cannot rule out alternative
hypotheses based on this evidence.
49
5. If we studied basic physiology, we would find a
necessary relationship between maximal and
resting aerobic metabolic rates.
For example, if mitochondria have a
"minimum idling speed"
or perhaps if "leaky membranes" are
required for a high VO2max and also entail
a cost at rest.
Various suborganismal traits do differ consistently
between mammals and reptiles …
50
Various Suborganismal Traits Show Quantitative
Differences Between Mammals and Reptiles
"The difference in energy production capacity
was not due to any single parameter but was a
summation of several smaller differences. The
mammal had relatively larger internal organs
than the reptile, their organs had a greater
proportion of mitochondria, and their
mitochondria had a greater relative membrane
surface area. These differences, it is
suggested, may be due in part to different
thyroid function in reptiles and mammals."
Else, P. L., and A. J. Hulbert. 1981. Comparison of
the "mammal machine" and the "reptile machine":
energy production. Am. J. Physiol. 240 (Regulatory
Integrative Comp. Physiol. 9):R3-R9.
51
Various Suborganismal Traits Show Quantitative
Differences Between Mammals and Reptiles
"Rolfe and Brown (1997) concluded that
∼10% of the oxygen consumed during BMR
is consumed by nonmitochondrial processes,
∼20% is consumed by mitochondria to
counteract the mitochondrial proton leak, and
the remaining 70% is consumed for
mitochondrial ATP production.
At a whole-animal level, ATP production can
be divided into 20%–25% for Na+,K+-ATPase
activity, 20%–25% for protein synthesis,
∼5% for Ca2+-ATPase activity,
∼7% for gluconeogenesis,
∼2% for ureagenesis,
∼5% for actinomyosin-ATPase activity, and
∼6% for all other ATP-consuming processes.
Hulbert, A. J., and P. L. Else. 2004. Basal metabolic
rate: history, composition, regulation, and usefulness.
Physiological and Biochemical Zoology 77:869-876.
These estimates are averages over the entire
animal, and the relative contribution of the
different processes varies between tissues."
52
No single factor accounts for the higher resting
metabolic rates of mammals versus lizards.
A mechanism that would yield a necessary
relationship between maximal and resting metabolic
rates remains elusive ...
Also, how relevant are living vertebrates?
Except for fossils, therapsids are not available for
study, nor are the ancestors of modern birds.
Various indicators of metabolic rate in fossils have
been proposed, but do not seem definitive, and have
not been tested experimentally, e.g.,
bone histology
lung structure
nasal turbinates as an example …
53
Fig. 6.
Relationship of nasal passage crosssectional area to body mass (M) in
extant ectotherms (lizards &
crocodilians;
cross-sectional area = 0.11M 0.76 ) and
endotherms (mammals & birds;
cross-sectional area = 0.57M 0.68).
Also plotted are three genera of Late
Cretaceous dinosaurs - the
hadrosaurid Hypacrosaurus and the
theropods Tyrannosaurus
(Nanotyrannus) and Ornithomimus and five genera of Permo-Triassic
therapsids: (1) a gorgonopsian, (2, 3)
two primitive therocephalians, and the
cyndonts (4) Diademodon and (5)
Thrinaxodon. Values for dinosaurs
and therapsids were not used in
regression calculations. Modified from
Ruben et al. (1996, 1997).
Hillenius, W. J., and J. A. Ruben. 2004. The evolution
of endothermy in terrestrial vertebrates: Who? When?
Why? Physiol. Biochemical Zoology 77:1019-1042.
Therapsids
54
Parental care and the evolution of
mammalian/avian endothermy:
two models.
55
Farmer, C. G. 2000. Parental care: the key to
understanding endothermy and other
convergent features in birds and mammals.
American Naturalist 155:326-334.
1. Endothermy was driven by the development of
active incubation, which would lead to the
evolution of an increased metabolic heat
production and control of an elevated body
temperature.
2. The immediate advantages were an increased
growth rate of the offspring and improved
developmental stability.
56
3. Increased heat production was achieved by an
increased leakiness of plasma membranes,
particularly in the visceral organs.
4. High daily energy expenditure was partly a
consequence of the foregoing increase in BMR.
5. Provisioning offspring with warmth and
nutrition requires sustained vigorous exercise.
A mix of ultimate and proximate explanations.
57
Koteja, P. 2004. The evolution of concepts on the evolution of endothermy in birds and mammals.
Physiological and Biochemical Zoology 77:1043-1050.
58
Koteja, P. 2000. Energy assimilation, parental care
and evolution of endothermy. Proceedings of
the Royal Society of London B 267:479-484.
1. Selection favored increased feeding of
offspring by parents.
Guarding of offspring first.
Offspring ate scraps.
So, selection favored parents who caught more
than they ate, and returned to nest to eat it.
59
2. The increased total energy expenditure by
parents (increased DEE) came with increased
food requirements, and hence required an
increased performance from the visceral
organs, which resulted in an increased BMR,
etc. --> positive feedback mechanism.
(= "assimilation capacity model")
3. Selection also favored increased offspring
growth rate.
4. Social structure is facilitated.
Increase in brain size would cause some
increase in BMR.
60
5. Eventually, when parents forage at or near
maximal aerobic speed (MAS), selection favors
increased VO2max.
Would require increases in lots of suborganismal
traits, if symmorphosis applies (later lecture)!
6. BMR thus increases, which increases DEE.
7. Positive feedback mechanism ...
A mix of ultimate and proximate explanations.
But what about shivering, etc., in response to
lowered temperature? This is not addressed by
either Farmer or Koteja (or by the aerobic
capacity model).
61
Koteja, P. 2004. The evolution of concepts on the evolution of endothermy in birds and mammals.
Physiological and Biochemical Zoology 77:1043-1050.
62
Extra Slides
Follow ...
In 2014, this was only about 5 min short. Should add a bit.
In 2015, this was about 15 min short.
For next time, possibly cut some verbiage, eliminate redundancy,
reorganize a bit, show McNab graph, explain some of the other
models a bit more (e.g., quotes, figures).
Could add more fossil work.
Combine all endothermy stuff into one lecture, and expand the
previous locomotion lecture. Add fish examples???
Farmer et al. unidirectional flow in varanid lung.
63
Sixth International Congress of Comparative Physiology and Biochemistry Symposium Papers: Evolution and Advantages of
Endothermy
Frappell, P. B., and P. J. Butler. 2004. Minimal Metabolic Rate, What It Is, Its Usefulness, and Its Relationship to the Evolution of Endothermy:
A Brief Synopsis. Physiological and Biochemical Zoology 77:865-868.
Hulbert, A. J., and P. L. Else. 2004. Basal Metabolic Rate: History, Composition, Regulation, and Usefulness. Physiological and Biochemical
Zoology 77:869-876.
Cruz-Neto, A. P., and F. Bozinovic. 2004. The Relationship between Diet Quality and Basal Metabolic Rate in Endotherms: Insights from
Intraspecific Analysis. Physiological and Biochemical Zoology 77:877-889.
Ksiek, A., M. Konarzewski, and I. B. Lapo. 2004. Anatomic and Energetic Correlates of Divergent Selection for Basal Metabolic Rate in
Laboratory Mice Physiological and Biochemical Zoology 77:890-899.
Speakman, J. R., E. Król, and M. S. Johnson. 2004. The Functional Significance of Individual Variation in Basal Metabolic Rate. Physiological
and Biochemical Zoology 77:900-915.
Lovegrove, B. G. 2004. Locomotor Mode, Maximum Running Speed, and Basal Metabolic Rate in Placental Mammals. Physiological and
Biochemical Zoology 77:916-928.
White, C. R., and R. S. Seymour. 2004. Does Basal Metabolic Rate Contain a Useful Signal? Mammalian BMR Allometry and Correlations
with a Selection of Physiological, Ecological, and Life-History Variables. Physiological and Biochemical Zoology 77:929-941.
Schleucher, E. 2004. Torpor in Birds: Taxonomy, Energetics, and Ecology. Physiological and Biochemical Zoology 77:942-949.
Else, P. L., N. Turner, and A. J. Hulbert. 2004. The Evolution of Endothermy: Role for Membranes and Molecular Activity. Physiological and
Biochemical Zoology 77:950-958.
Pörtner, H. O. 2004. Climate Variability and the Energetic Pathways of Evolution: The Origin of Endothermy in Mammals and Birds.
Physiological and Biochemical Zoology 77:959-981.
Grigg, G. C., L. A. Beard, and M. L. Augee. 2004. The Evolution of Endothermy and Its Diversity in Mammals and Birds. Physiological and
Biochemical Zoology 77:982-997.
Dickson, K. A., and J. B. Graham. 2004. Evolution and Consequences of Endothermy in Fishes. Physiological and Biochemical Zoology
77:998-1018.
Hillenius, W. J., and J. A. Ruben. 2004. The Evolution of Endothermy in Terrestrial Vertebrates: Who? When? Why? Physiological and
Biochemical Zoology 77:1019-1042.
Koteja, P. 2004. The Evolution of Concepts on the Evolution of Endothermy in Birds and Mammals. Physiological and Biochemical Zoology
77:1043-1050.
Seymour, R. S., C. L. Bennett-Stamper, S. D. Johnston, D. R. Carrier, and G. C. Grigg. 2004. Evidence for Endothermic Ancestors of
Crocodiles at the Stem of Archosaur Evolution. Physiological and Biochemical Zoology 77:1051-1067.
Hillenius, W. J., and J. A. Ruben. 2004. Getting Warmer, Getting Colder: Reconstructing Crocodylomorph Physiology. Physiological and
Biochemical Zoology 77:1068-1072.
Seymour, R. S. 2004. Reply to Hillenius and Ruben. Physiological and Biochemical Zoology 77:1073-1075.
64
Descriptive Statistics
EXAM1
EXAM1PCT
Valid N (lis twis e)
N
Statis tic
41
41
41
Minimum
Statis tic
36.00
60.00
Maximum
Statis tic
58.50
97.50
Mean
Statis tic
Std. Error
49.2073
.9703
82.0122
1.6171
12
Std.
Deviation
Statis tic
6.21287
10.35478
Variance
Statis tic
38.600
107.221
Skewness
Statis tic
Std. Error
-.681
.369
-.681
.369
Kurtos is
Statis tic
Std. Error
-.637
.724
-.637
.724
10
10
8
8
6
6
4
4
Std. Dev = 6.21
2
2
Std. Dev = 10.35
Mean = 49.2
Mean = 82.0
N = 41.00
0
40.0
37.5
EXAM1
45.0
42.5
50.0
47.5
52.5
N = 41.00
0
55.0
57.5
.5
97 0
.
9 5 .5
92 0
.
90 5
.
87 0
.
85 5
.
82 0
.
80 5
.
77 0
.
75 5
.
7 2 .0
70 5
.
67 0
.
65 5
.
62 0
.
60
35.0
EXAM1PCT
Stopped here 1 Feb. 2007
65
Sixth International Congress of Comparative Physiology and Biochemistry Symposium Papers: Evolution and Advantages of
Endothermy
Frappell, P. B., and P. J. Butler. 2004. Minimal Metabolic Rate, What It Is, Its Usefulness, and Its Relationship to the Evolution of Endothermy:
A Brief Synopsis. Physiological and Biochemical Zoology 77:865-868.
Hulbert, A. J., and P. L. Else. 2004. Basal Metabolic Rate: History, Composition, Regulation, and Usefulness. Physiological and Biochemical
Zoology 77:869-876.
Cruz-Neto, A. P., and F. Bozinovic. 2004. The Relationship between Diet Quality and Basal Metabolic Rate in Endotherms: Insights from
Intraspecific Analysis. Physiological and Biochemical Zoology 77:877-889.
Ksiek, A., M. Konarzewski, and I. B. Lapo. 2004. Anatomic and Energetic Correlates of Divergent Selection for Basal Metabolic Rate in
Laboratory Mice Physiological and Biochemical Zoology 77:890-899.
Speakman, J. R., E. Król, and M. S. Johnson. 2004. The Functional Significance of Individual Variation in Basal Metabolic Rate. Physiological
and Biochemical Zoology 77:900-915.
Lovegrove, B. G. 2004. Locomotor Mode, Maximum Running Speed, and Basal Metabolic Rate in Placental Mammals. Physiological and
Biochemical Zoology 77:916-928.
White, C. R., and R. S. Seymour. 2004. Does Basal Metabolic Rate Contain a Useful Signal? Mammalian BMR Allometry and Correlations
with a Selection of Physiological, Ecological, and Life-History Variables. Physiological and Biochemical Zoology 77:929-941.
Schleucher, E. 2004. Torpor in Birds: Taxonomy, Energetics, and Ecology. Physiological and Biochemical Zoology 77:942-949.
Else, P. L., N. Turner, and A. J. Hulbert. 2004. The Evolution of Endothermy: Role for Membranes and Molecular Activity. Physiological and
Biochemical Zoology 77:950-958.
Pörtner, H. O. 2004. Climate Variability and the Energetic Pathways of Evolution: The Origin of Endothermy in Mammals and Birds.
Physiological and Biochemical Zoology 77:959-981.
Grigg, G. C., L. A. Beard, and M. L. Augee. 2004. The Evolution of Endothermy and Its Diversity in Mammals and Birds. Physiological and
Biochemical Zoology 77:982-997.
Dickson, K. A., and J. B. Graham. 2004. Evolution and Consequences of Endothermy in Fishes. Physiological and Biochemical Zoology
77:998-1018.
Hillenius, W. J., and J. A. Ruben. 2004. The Evolution of Endothermy in Terrestrial Vertebrates: Who? When? Why? Physiological and
Biochemical Zoology 77:1019-1042.
Koteja, P. 2004. The Evolution of Concepts on the Evolution of Endothermy in Birds and Mammals. Physiological and Biochemical Zoology
77:1043-1050.
Seymour, R. S., C. L. Bennett-Stamper, S. D. Johnston, D. R. Carrier, and G. C. Grigg. 2004. Evidence for Endothermic Ancestors of
Crocodiles at the Stem of Archosaur Evolution. Physiological and Biochemical Zoology 77:1051-1067.
Hillenius, W. J., and J. A. Ruben. 2004. Getting Warmer, Getting Colder: Reconstructing Crocodylomorph Physiology. Physiological and
Biochemical Zoology 77:1068-1072.
Seymour, R. S. 2004. Reply to Hillenius and Ruben. Physiological and Biochemical Zoology 77:1073-1075.
66
Good graphs, but no phylogenetic analysis.
Endothermy in African Platypleurine Cicadas: The Influence of Body Size and Habitat (Hemiptera: Cicadidae)
Author(s) Allen F. Sanborn, Martin H. Villet, and Polly K. Phillips
Identifiers Physiological and Biochemical Zoology, volume 77 (2004), pages 816–823
DOI: 10.1086/422226
PubMed ID: 15547799
Abstract The platypleurine cicadas have a wide distribution across Africa and southern Asia. We investigate
endothermy as a thermoregulatory strategy in 11 South African species from five genera, with comparisons to the
lone ectothermic platypleurine we found, in an attempt to ascertain any influence that habitat and/or body size have
on the expression of endothermy in the platypleurine cicadas. Field measurements of body temperature (Tb) show
that these animals regulate Tb through endogenous heat production. Heat production in the laboratory elevated Tb
to the same range as in animals active in the field. Maximum Tb measured during calling activity when there was
no access to solar radiation ranged from 13.2° to 22.3°C above ambient temperature in the five species measured.
The mean Tb during activity without access to solar radiation did not differ from the mean Tb during diurnal
activity. All platypleurines exhibit a unique behavior for cicadas while warming endogenously, a temperaturedependent telescoping pulsation of the abdomen that probably functions in ventilation. Platypleurines generally call
from trunks and branches within the canopy and appear to rely on endothermy even when the sun is available to
elevate Tb, in contrast to the facultative endothermy exhibited by New World endothermic species. The two
exceptions to this generalization we found within the platypleurines are Platypleura wahlbergi and Albanycada
albigera, which were the smallest species studied. The small size of P. wahlbergi appears to have altered their
thermoregulatory strategy to one of facultative endothermy, whereby they use the sun when it is available to
facilitate increases in Tb. Albanycada albigera is the only ectothermic platypleurine we found. The habitat and host
plant association of A. albigera appear to have influenced the choice of ectothermy as a thermoregulatory strategy,
as the species possesses the metabolic machinery to elevate to the Tb range observed in the endothermic species.
Therefore, size and habitat appear to influence the expression of thermoregulatory strategies in African
platypleurine cicadas.
67
Intraspecific Relationships between Resting and Activity Metabolism in Anuran Amphibians: Influence
of Ecology and Behavior
Author(s) Fernando R. Gomes, José Guilherme Chauí-Berlinck, José Eduardo P. W. Bicudo, and Carlos
A. Navas
Identifiers Physiological and Biochemical Zoology, volume 77 (2004), pages 197–208
DOI: 10.1086/381471
PubMed ID: 15095240
Abstract The aerobic capacity model, as well as other models for the evolution of aerobic metabolism
and the origin of endothermy, requires a mechanistic link between rates of resting and activity oxygen
consumption (VN/Ao2rest and VN/Ao2act). The existence of such link is still controversial, but studies
with anuran amphibians support a correlation between VN/Ao2rest and VN/Ao2act at both the
intraspecific and interspecific levels. Because results at the intraspecific level are based only on a few
species, we test for the generality of a link between these two metabolic variables in anurans by
studying the intraspecific correlational patterns between mass-independent VN/Ao2rest and VN/Ao2act
in anurans. We focus on 21 Neotropical species from different geographical areas that include
remarkable diversity in behavior and thermal ecology. Although uncorrelated, VN/Ao2rest and
VN/Ao2act seem to be consistent among individuals. Diverse intraspecific phenotypic correlational
trends were detected, indicating that the intraspecific relationships between VN/Ao2rest and VN/Ao2act
might be very diverse in anurans. The three possible trends (positive, negative, and absent correlations)
were observed and appeared to be predictable from ecological and behavioral variables that relate to
evolutionary physiological shifts in anurans. Positive correlations between VN/Ao2rest and VN/Ao2act
were more common in species with active lifestyles (e.g., intense vocal activity) and in species that call
at low temperatures (e.g., winter or high-elevation specialists).
68
Seymour et al., 200469
Seymour et al., 200470
Seymour et al., 200471
Seymour et al., 200472
Seymour et al., 200473
Rezende, E. L., F. Bozinovic, and T. Garland, Jr. 2004. Climatic adaptation and the evolution
of basal and maximum rates of metabolism in rodents. Evolution 58:1361-1374.
74
Rezende, E. L., F. Bozinovic, and T. Garland, Jr. 2004. Climatic adaptation and the evolution
of basal and maximum rates of metabolism in rodents. Evolution 58:1361-1374.
75
From 41095LECT.DOC
Problems of defining 1st mammal:
(see Ridley, 1996, pages 582-587)
1. How do you define a mammal?
2. modern mammals have hair or fur, lactation, live birth, parental care, high metabolic rates,
ability to maintain high body temperature in face of cold via shivering, etc.
3. only skeletal characteristics can be seen in fossil record
4. so, define 1st mammals as having a single bone, the dentary, in the lower jaw
(TRANSPARENCY 1 from Lecture 14)
5. skulls may indicate presence of vibrissae
6. bone histology may give clues as to metabolic rate
7. were therapsids warm-blooded?
8. predator-prey relationships -- Bakker
9. were dinosaurs warm-blooded?
10. biomechanical/energetic arguments
a. must be warm-blooded to fly --> pterosaurs must have been --> ancestors of both
pterosaurs and
Archaeopteryx must have been???
11. Comparative Method may help,
and so must know evolutionary relationships!!!
Difficulties in defining "first" in a clade emphasize the gradual nature of evolutionary
change, even among major grades.
76
Species
Pear-
n
son's r
1-tailed Source
P
Amphibians
Bufo woodhousii
0.374
38
0.0104
Walton 1988
Callisaurus draconoides
0.224
20
0.1712
Garland, unpub. data
Chalcides ocellatus
0.089
28
0.3261
Pough and Andrews 1984
Cnemidophorus tigris
-0.010
24
0.5185
Garland, unpub. data
Ctenophorus nuchalis
0.219
56
0.0524
Garland and Else 1987
Ctenosaura similis
0.122
18
0.3148
Garland 1984
Dipsosaurus dorsalis
0.176
70
0.0725
John-Alder 1984
Sceloporus undulatus
0.318
47
0.0145
Pierce & John-Alder, pers. com.
0.11
250
0.0413
Walton, Bennett, Peterson, p.c.
Peromyscus maniculatus - cold exp.
0.318
50
0.0122
Hayes 1989
Spermophilus beldingi
0.31
95
0.0011
M. A. Chappell, pers. comm.
Spermophilus beldingi - cold exp.
0.005
95
0.4804
M. A. Chappell, pers. comm.
Lizards
Snakes
Thamnophis sirtalis
Mammals
77
Possible exam question:
Discuss two different models for the evolution of
mammalian and avian endothermy.
Who developed these models?
How do the components of the models fall into the
categories of ultimate and proximate explanation?
78