Lecture 9 & 10: Evolution of Endothermy

1. Lecture 9 & 10: Evolution of Endothermy

2. Endothermy has evolved multiple times in both animals and plants: birds and mammals, or their ancestors

3. Endothermy has evolved multiple times in both animals and plants: some reptiles (brooding pythons, large sea turtles, maybe dinosaurs, pterosaurs)

4. Endothermy has evolved multiple times in both animals and plants: scombrid fishes (e.g., tunas and billfishes) lamnid sharks

5. Endothermy has evolved multiple times in both animals and plants: insects (e.g., moths, bees some beetles)

6. Endothermy has evolved multiple times in both animals and plants: at least eight genera of plants within the family Araceae

7. 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).

8. 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:

9. Body Mass Distributions K. S. Kilburn,Old Dominion University … and small endotherms have severe problems with heat loss because of unfavorable surface/volume ratios.

10. 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

11. 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.

12. 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.

13. Legend for previous slide: Nagy, K. A. 2005. Field metabolic rate and body size. Journal of Experimental Biology 208:1621-1625.

14. Nagy, K. A. 2005. Field metabolic rate and body size. Journal of Experimental Biology 208:1621-1625.

15. 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

16. 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)

17. 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

18. Mammals similar to precocial birds; altricial birds are higher GRAMS 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.

19. Reptiles and fishes are lower than birds & mammals GRAMS Case, T. J. 1978. On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Q. Rev. Biol. 53:243-282.

20. 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 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?] Powered flight in relatively larger animals Intense feeding of offspring Enzymes can function more efficiently over a narrower temperature range

21. 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

22. 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 Live Birth Parental Care Lactation Large Brain 4-chambered Heart Most of these features are absent or unclear in the fossil record.

23. 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

24. 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.

25. 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.)

26. 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)

27. 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)

28. 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.

29. 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.

30. 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.

31. 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.

32. "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.

33. 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.

34. 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!

35. 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.

36. 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.

37. 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.

38. 3. What about the phenotypic correlation between VO2max and resting metabolic rate? Estimates of the phenotypic correlationswithin species are much easier to obtain. They were compiled in Hayes and Garland (1995), and the following table gives their results with some updates:

40. Take-home message: phenotypic correlations tend to be positive. However, the picture for anuran amphibians is much less consistently positive …

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. • 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 atlow temperatures (e.g., winter or high-elevation specialists)."

42. 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.

43. 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).

44. 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 ...

45. Rezende, E. L.,F. Bozinovic, andT. 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

46. Rezende, E. L.,F. Bozinovic, andT. 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

47. 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.

48. 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.

49. 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.

50. 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 …