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

Abstract

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.

Evolution of diel activity patterns in skinks (Squamata: Scincidae), the world's second‐largest family of terrestrial vertebrates

“…Nocturnal habits are often associated with unique adaptations. These can range from greater reliance on acoustic or olfactory sensory information and communication (Healy and Guilford 1990;Barton 2006;Chen and Wiens 2020), and improved locomotion at low temperatures (Autumn et al 1999;Bars-Closel et al 2018), to visual adaptations for low-light conditions such as large eyes, lack of foveae, or rod-like receptors in the retina without oil droplets (Walls 1942;Underwood 1951;Underwood 1970;Pinto et al 2019;Röll 2000a, b). Fossorial habits offer low-light conditions and, at least during hot days, reduced temperatures, much like nocturnal habits (Wu et al 2009).…”

“…Fossorial habits offer low-light conditions and, at least during hot days, reduced temperatures, much like nocturnal habits (Wu et al 2009). Some fossorial reptiles exhibit similar metabolic adaptations to nocturnal reptiles (Withers 1981;Andrews and Pough 1985;Wu et al 2009;Bars-Closel et al 2018), and fossoriality and nocturnality have often been thought to be strongly correlated in reptiles (Thomas and Thomas 1978;Vitt and Caldwell 2014), although this hypothesized correlation was never formally tested. Fossorial reptiles are often (Brandley et al 2008;Skinner et al 2008;Siler and Brown 2011;Camaiti et al 2021), but not always (Wiens et al 2006), limbless or limb reduced.…”

“…1999; Bars‐Closel et al. 2018), to visual adaptations for low‐light conditions such as large eyes, lack of foveae, or rod‐like receptors in the retina without oil droplets (Walls 1942; Underwood 1951; Underwood 1970; Pinto et al. 2019; Röll 2000a, b).…”

“…2009; Bars‐Closel et al. 2018), and fossoriality and nocturnality have often been thought to be strongly correlated in reptiles (Thomas and Thomas 1978; Vitt and Caldwell 2014), although this hypothesized correlation was never formally tested. Fossorial reptiles are often (Brandley et al.…”

Ecomorphological evolution of South-American Colubroidea snakes (Squamata: Serpentes)

“…The trait S/V has never been directly estimated in Serpentes, although snakes offer an excellent model to obtain these measurements because of their limbless and elongated cylindrical form. Furthermore, the clade Serpentes comprises a remarkable diversity in morphology and ecology, being also very species-rich, which turns the lineage ideal for to ecomorphological studies (Bars-Closel et al 2018;Harrington et al 2018). In particular, Colubridae and Dipsadidae are two snake families that comprise highest diversity levels of microhabitat occupation and activity periods.…”