Locomotor performance at low temperature and the evolution of nocturnality in geckos

Kellar Autumn, Devin Jindrich, Dale Denardo, Rachel Mueller

Research output: Contribution to journalArticle

68 Citations (Scopus)

Abstract

Nocturnal geckos are active at body temperatures 10-35°C below the thermal optima for maximum rate of aerobic metabolism (V̇(O2max)) of diurnal lizards. Therefore, given ancestral (diurnal) lizard physiology, nocturnality causes a substantial thermal handicap in locomotor performance. In prior studies, we hypothesized that a low minimum cost of locomotion (C(min)) in geckos was an adaptation that increased locomotor endurance capacity at low, nocturnal temperatures. However, C(min) is only part of an integrated system that, in conjunction with the maximum rate of oxygen consumption, sets the maximum speed that can be sustained aerobically (termed the maximum aerobic speed or MAS). We conducted the first phylogenetic analysis of MAS and V̇(O2max) in lizards and found that the greatest changes in MAS, C(min) and V̇(O2max) (at activity temperatures) in the evolutionary history of lizards all coincided with the evolution of nocturnality in geckos. Geckos active at 15-25°C did not become optimized for nocturnal temperatures, or fully offset the thermal effects of nocturnality by evolving maximal rates of oxygen consumption comparable to diurnal lizards active at 35°C. Geckos did evolve MAS twice that of diurnal lizards running at low temperatures by evolving a remarkably low C(min). Allometric analysis and phylogenetically independent contrasts of V̇(O2max), C(min), and MAS indicate a 72% evolutionary decrease in V̇(O2max) (at activity temperatures) and a 50% evolutionary decrease in C(min) concordant with the evolution of nocturnality in geckos. Experimental measurements show that decreased C(min) in six species of gecko increased MAS by 50-120% compared to diurnal lizards at low temperatures. Thus, geckos sufficiently overcame the near paralyzing effects of nocturnal temperatures, but only offset about 50% of the decrease in MAS resulting from the low maximum rate of oxygen consumption. Although the nocturnal environment remains severely suboptimal, the evolution of a low cost of locomotion in the ancestor of geckos was highly adaptive for nocturnality. We also present a generalized approach to ecophysiological evolution that integrates phylogeny with the causal relationships among environment, physiology, and performance capacity. With respect to a clade, two hypotheses are central to our integrative approach: (1) a change of an environmental variable (e.g., temperature) causes a performance handicap; and (2) evolution of a physiological variable (e.g., minimum cost of locomotion [C(min)]) increases performance in the derived environment. To test the hypothesis that evolution of a physiological variable is adaptive in nature, we suggest determining if individuals in nature perform at levels exceeding the performance capacity of their hypothetical ancestors and if this additional performance capacity is due to the evolution of the physiological variable in question.

Original languageEnglish (US)
Pages (from-to)580-599
Number of pages20
JournalEvolution
Volume53
Issue number2
StatePublished - Apr 1999
Externally publishedYes

Fingerprint

MAS
Lizards
Gekkonidae
lizard
lizards
Temperature
locomotion
oxygen consumption
temperature
ancestry
physiology
heat
cost
Locomotion
Oxygen Consumption
body temperature
Hot Temperature
temperature effect
phylogeny
Costs and Cost Analysis

Keywords

  • Energetics
  • Exercise
  • Integrative biology
  • Lizard
  • Locomotion
  • Optimality
  • Physiology

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)
  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Ecology
  • Genetics(clinical)

Cite this

Locomotor performance at low temperature and the evolution of nocturnality in geckos. / Autumn, Kellar; Jindrich, Devin; Denardo, Dale; Mueller, Rachel.

In: Evolution, Vol. 53, No. 2, 04.1999, p. 580-599.

Research output: Contribution to journalArticle

Autumn, K, Jindrich, D, Denardo, D & Mueller, R 1999, 'Locomotor performance at low temperature and the evolution of nocturnality in geckos', Evolution, vol. 53, no. 2, pp. 580-599.
Autumn, Kellar ; Jindrich, Devin ; Denardo, Dale ; Mueller, Rachel. / Locomotor performance at low temperature and the evolution of nocturnality in geckos. In: Evolution. 1999 ; Vol. 53, No. 2. pp. 580-599.
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