Thermoregulatory Model Crompton et al. 1978. Evolution of

1
Thermoregulatory Model

• Crompton et al. 1978. Evolution of homeothermy in
  mammals. Nature 272333-336.
• McNab, B. 1978. The evolution of homeothermy in
  the phylolgeny of mammals. Am. Nat. 1121-21.
• Grigg, G.C., L.A. Beard, and M.L. Augee. 2004.
  The evolution of endothermy and its diversity in
  mammals and birds. Physiol Biochem Zool
  77982-997.
• Bennett, A.F., J.W. Hicks, and A.J. Cullum. 2000.
  An experimental test of the thermoregulatory
  hypothesis for the evolution of endothermy.
  Evolution 541768-1773.

2
What is/are Selective Factor(s) for Evolution of
Endothermy

• Thermoregulation selection for higher Tb
• Enzyme stability and efficiency
• Independence of timing of daily activities
• Resistance to freezing
• These benefits all result from maintenance of
  high Tb
• Assumption immediate thermoregulatory benefits
  accrue for slight increase in MR

3
Crompton et al. 1978

• We propose that mammalian homeothermy
  (endothermy) was acquired in two steps.
• The first step enabled mammals to invade a
  nocturnal niche without an increase in BMR.
• The second step enabled them to invade a diurnal
  niche and involved the acquisition of higher body
  temperatures and metabolic rates.
• Selection for high body temperature per se in
  second step ? thermal nice expansion.
• First step not really applicable to birds.

4
Decreasing Body Size Hypothesis

• McNab (1978)
• Selection for small body size and nocturnal
  activity.
• Therapsid ancestors were large.
• Therapsid ancestors inertial homeotherms (large
  size plus warm climates constant Tb) ? enzyme
  operation adapted to high stable Tb.
• Mammalian ancestors constrained to high stable Tb
  to maintain efficient enzyme function.
• Cooling climate at origin of mammals, plus
  dinosaurs in large diurnal niche, led to small
  size and endothermy ? necessary to maintain
  stable enzyme operation.

5
Evolutionary Scenario

• Large Therapsid ectotherm ancestor was inertial
  homeotherm
• Respiratory turbinates present in several
  advanced therapsids suggest endothermy already
  present in mammal ancestors (Hillenius 1994 Evol
  48207-229)
• Evolution of insulative coat of fur reduces
  thermal conductance
• Evolution of small size with
• Reduced thermal conductance
• Gradual elevation of MR (MR ? more slowly than
  body size)

6
Body size decreases MR stays the same
Body size decreases MR ? at slower rate
7
Evolutionary Scenario (cont.)

• Trend toward decreasing body size present in
  mammalian lineage
• Decreasing body size trend also apparent in bird
  lineage
• Coelurosaurian theropod dinosaurs larger than
  Archaeopteryx

First evidence for nasal turbinates and elevated
MR, but no 2 palate initially. Slow progress
toward endothermy (Hillenius 1994).
8
Therapsid to mammal line Note decreasing body
size trend
Procynosuchus delaharpeae, a primitive cynodont
from the Late Permian of South Africa
9
Cynognathus, a cynodont from the Triassic of
South Africa
10
Tritylodon longaevus, a cynodont from the Early
Jurassic of South Africa
Oligokyphus, a trytilodont from the Early
Jurassic of England
11
Dinosaur to Bird line also characterized by
trend toward decreasing body size
12
Deinonychus (large) and Buitreraptor (small).
Deinonychus 3.4 meter- long early Cretaceous,
about 115 mya. Buitreraptor Rooster-sized mid
to late Cretaceous, about 90 mya.
13
When living, Bambiraptor would have stood no more
than 0.3 meter off the ground, reached 0.7 meter
in length, and weighed only two kilograms
14
Archaeopteryx lived in the late Jurassic,
150 mya, and was similar in size and shape to a
magpie. Archaeopteryx specimens are as large as
0.5 meters in length.
15
Confuciusornis is a genus of crow-sized,
primitive, birds from the Early Cretaceous of
China, approximately 120 million years ago.
16
Decreasing Body Size Hypothesis

• Body size did decrease in ancestral lineages for
  mammals and birds
• Evidence for nasal turbinates in therapsid
  lineage, suggests a slow trend toward increasing
  metabolic rates and endothermy
• Coelurosaurian dinosaurs without turbinates,
  little evidence for increased MR
• Doesnt explain selective advantage of small
  increases in MR

17
Heterothermic Intermediate Hypothesis

• Grigg et al. (2004)
• Heterothermy periodic decreases in Tb (e.g.,
  torpor and hibernation)
• Typically regarded as an evolutionary
  specialization, derived from endothermic
  condition
• Recent evidence suggests that heterothermy is
  widespread and occurs in many primitive groups
  of mammals and birds
• Hypothesis heterothermy is primitive condition
  for mammals and birds represents stage in
  evolution of full endothermic condition

18
Heterothermic Intermediate Hypothesis

• Reptile Thermoregulatory Patterns
• Tb variation in large crocodiles in tropics
• 2-3C daily variation
• 4-5C seasonal variation
• Grigg et al. (2004) argue that crocodiles are not
  tight inertial homeotherms
• Daily Tb variation in small birds similar though
• Therapsid ancestors to mammals with smaller body
  size, so not likely inertial homeotherms

19
Reptile Thermoregulatory Patterns (cont.)

• Shivering in pythons elevates Tb during
  incubation (Tb-Ta differential ? in cold)
• Reptiles (esp. lizards) good at controlling
  conductance via ? in peripheral circulation
• Behavioral thermoregulation important to reptiles
  and also to mammals and birds
• Protoendotherms may have also shown similar
  thermoregulatory patterns, with the addition of
  facultative endothermy

20
(No Transcript)
21
Echidnas as a Primitive Endotherm

• Belong to Subclass Monotremata
• Low Tb with relatively wide fluctuations
• Tb 32C with 2-5C daily Tb cycle
• Behavior important to thermoregulation
• Use short and long-term torpor bouts
• Tight regulation of Tb during incubation
• Capacity for normal activity at low Tb
• Emphasis on similarities in reptile and primitive
  endotherm thermoregulation

22
Heterothermic Intermediate HypothesisEvolutionar
y Scenario

• Selection favors enhancement of thermoregulatory
  patterns in reptiles (peripheral circulation,
  shivering) for tight control of Tb
• Reduced thermal conductance
• Facultative endothermy ( heterothermy)
• Full Endothermy

23
Heterotherm Model Grigg et al. (2004)
Still doesnt provide benefit for small increases
in MR
24
Problems with Thermoregulatory Model

• Advantages of high Tb from MR not applicable to
  all environmental circumstances in which
  endothermy evolved
• Quantum leap in MR required for thermoregulatory
  benefit what are advantages to intermediate
  steps?
• Mesozoic Period most thermally equable in earths
  history, so maintaining Tb by behavioral
  thermoregulation relatively easy difficult to
  explain high cost of endothermy

25
Testing the Assumption of the Thermoregulatory
Model

• Assumption immediate thermoregulatory benefits
  accrue for slight increase in MR
• Bennett et al. (2000) experimental test
• Idea increase metabolic rate in an ectotherm
• Measure thermoregulatory effects

26
Testing the Assumption of the Thermoregulatory
Model

• Model Varanid Lizards
• Typical RMR, but high aerobic scope for lizards
• Heat increment of feeding can dramatically
  increase MR after a large meal

27
Testing the Assumption of the Thermoregulatory
Model - Methods

• Fasted lizards to maximize caloric effect of a
  meal ( heat increment of feeding, HIF)
• Large meal given (18 of body mass) at 35C (
  preferred Tb)
• Tb measured by implanted rectal thermocouple
• MR measured by open-circuit respirometry
• Ta ? from 35C to 25C (Tb rate of ? recorded)
• Fasting vs. fed treatments
• Repeated experiments at constant 32C

28
Testing the Assumption of the Thermoregulatory
Model - Results

• Post-prandial MR ? by 3 to 4-fold ( BMR in
  hedgehog mammal of similar size and Tb)
• Tb ? by 0.4C at 35C 0.65C at 32C
• Cooling rates similar in fasted and 24-h
  post-prandial treatments
• Despite large ? in RMR, very little
  thermoregulatory benefit

29
(No Transcript)
30
(No Transcript)
31
Testing the Assumption of the Thermoregulatory
Model - Conclusions

• Little thermoregulatory benefit of 3 to 4-fold
  increase in RMR
• Data do not support thermoregulatory model (?MR
  represents a cost without a benefit)
• Biophysical models suggest similar lack of
  thermoregulatory benefit in larger therapsid
  ancestors

32
Testing the Assumption of the Thermoregulatory
Model - Conclusions

• Authors conclude that
• Endothermy probably evolved for reasons other
  than thermoregulation
• Endothermy developed after the evolution of ?MR