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Ecological diversification often encompasses exposure to new thermal regimes given by the use of specific spatial (microhabitat) and temporal (activity periods) niches. Empirical evidence provides links between temperature and physiology (e.g. rates of oxygen consumption), fostering predictions of evolutionary changes in metabolic rates coupled with ecological shifts. One example of such correspondence is the evolution of fossoriality and nocturnality in vertebrate ectotherms, where changes in metabolic rates coupled with niche transitions are expected. Because most studies address single transitions (fossoriality or nocturnality), metabolic changes associated with concomitant shifts in spatial and temporal components of habitat usage are underestimated, and it remains unclear which transition plays a major role for metabolic evolution. Integrating multiple ecological aspects that affect the evolution of thermosensitive traits is essential for a proper understanding of physiological correlates in niche transitions. Here, we provide the first phylogenetic multidimensional description of effects from ecological niche transitions both in space (origin of fossorial lineages) and in time (origin of nocturnal lineages) on the evolution of microteiid lizard (Gymnophthalmidae) metabolic rates. We found that evolution of resting metabolic rates was affected by both niche transitions, but with opposite trends. Evolution of fossoriality in endemic diurnal microteiids is coupled with a less thermally sensitive metabolism and higher metabolic rates. In contrast, a reduction in metabolic rates was detected in the endemic fossorial-nocturnal lineage, although metabolic thermal sensitivity remained as high as that observed in epigeal species, a pattern that likely reduces locomotion costs at lower temperatures and also favors thermoregulation in subsuperficial sand layers.

Shifts in space and time: ecological transitions affect the evolution of resting metabolic rates in microteiid lizards