Living on the edge: Lower thermal quality but greater survival probability at a high altitude mountain for the mesquite lizard (Sceloporus grammicus)

Domínguez-Godoy, Miguel A.; Hudson, Robyn; Pérez-Mendoza, Hibraim Adán; Ancona, Sergio; Vega‐Pérez, Aníbal H. Díaz de la

doi:10.1016/j.jtherbio.2020.102757

Cited by 21 publications

(20 citation statements)

References 61 publications

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“…Given these premises and assuming steady-state populations—populations in which energy invested into production (birth rates) equals energy lost by predation (death rates) 19 , 25 —viviparity in phrynosomatids is a high-survivorship, low-fecundity phenotype positioned on the slow end of the fast-slow continuum. This ‘slow’ life-history strategy is characterized by the reduction in mortality afforded by in utero embryonic development (in comparison to eggs deposited in nests) against abiotic and biotic hazards 2 – 5 , 8 , 26 – 31 and is favored in colder environments such as high elevation 8 , 20 , 21 , where predation risk for phrynosomatids and other ectotherms is lower 32 – 34 . Furthermore, when compared to their oviparous counterparts, viviparous phrynosomatids are more common in tropical environments with lower temperature seasonality 21 , where selection could favor allocating energy in fewer, fitter offspring, rather than higher productivity 35 .…”

Section: Resultsmentioning

confidence: 99%

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards

et al. 2022

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Viviparity, an innovation enhancing maternal control over developing embryos, has evolved >150 times in vertebrates, and has been proposed as an adaptation to inhabit cold habitats. Yet, the behavioral, physiological, morphological, and life history features associated with live-bearing remain unclear. Here, we capitalize on repeated origins of viviparity in phrynosomatid lizards to tease apart the phenotypic patterns associated with this innovation. Using data from 125 species and phylogenetic approaches, we find that viviparous phrynosomatids repeatedly evolved a more cool-adjusted thermal physiology than their oviparous relatives. Through precise thermoregulatory behavior viviparous phrynosomatids are cool-adjusted even in warm environments, and oviparous phrynosomatids warm-adjusted even in cool environments. Convergent behavioral shifts in viviparous species reduce energetic demand during activity, which may help offset the costs of protracted gestation. Whereas dam and offspring body size are similar among both parity modes, annual fecundity repeatedly decreases in viviparous lineages. Thus, viviparity is associated with a lower energetic allocation into production. Together, our results indicate that oviparity and viviparity are on opposing ends of the fast-slow life history continuum in both warm and cool environments. In this sense, the ‘cold climate hypothesis’ fits into a broader range of energetic/life history trade-offs that influence transitions to viviparity.

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Section: Resultsmentioning

confidence: 99%

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards

et al. 2022

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“…Given these premises and assuming steady-state populations-populations in which energy invested into production (birth rates) equals energy lost by predation (death rates) 10,12,18 -we infer that viviparity in phrynosomatids is a high-survivorship, low-fecundity phenotype positioned on the slow end of the fast-slow continuum. This notion is supported by the inherent maternal protection and mortality reduction afforded by in utero embryonic development (in comparison to eggs laid in nests) against abiotic and biotic hazards 2,3,4,19,20,21,22 and with the common distribution of viviparous species in colder environments such as high elevation 13,22 , where predation risk for ectotherms is lower 23,24,25 . Whereas viviparous females can replace themselves each generation by allocating less energy into maintenance and production (normalized by body mass), oviparous females must instead expend greater energy into producing more offspring per year (Fig.…”

Section: Resultsmentioning

confidence: 99%

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards

Domínguez‐Guerrero

Cruz

Manríquez–Morán

et al. 2021

Preprint

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Viviparity is an evolutionary innovation that enhances maternal protection of developing embryos relative to egg-laying ancestors. The behavioral, physiological, morphological, and life history pathways underpinning this innovation, however, remain unclear. We capitalized on the repeated origin of viviparity in phrynosomatid lizards to tease apart the phenotypic patterns associated with evolutionary transitions to live birth. We detected tandem reductions in mass-specific metabolic rate and mass-specific production in viviparous lineages, in turn reflecting decreases in thermal physiology and fecundity, respectively. These pathways reduce the energetic burden of viviparity without concomitant reductions in offspring body size. Although viviparous lizards are more prevalent in cold environments, transitions in thermal habitat only weakly predict parity mode evolution. Likewise, only cold tolerance adapts rapidly to thermal environment. Heat tolerance and preferred body temperatures track the thermal environment, but with a lag at million-year timescales. This lag likely reflects behavioral buffering: viviparous lizards thermoregulate to low body temperatures, regardless of ambient conditions. Rather than representing an adaptation to cold climates, the lower thermal and metabolic physiology of viviparous species are likely an energetic adjustment for reproduction that facilitated their prolific colonization of cooler environments.

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“…We also found that species from high elevations have more restricted activity hours (Kubisch et al, 2016), and exhibited a weak tendency to have lower warming tolerances than lowland species. In current climatic scenarios, these patterns might be caused by cold temperatures, which drive limited thermoregulatory opportunities, and sometimes increased body temperatures, at highlands and high latitudes (Anderson, Alton, et al, 2022; Domínguez‐Godoy et al, 2020; Hertz et al, 1993; Kubisch et al, 2016; Vickers et al, 2011; Wu et al, 2018). Lizards in these environments (highlands and temperate zones) exhibited reduced hours of activity when compared to lowland and tropical species (Kubisch et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

The biogeography of warming tolerance in lizards

Anderson

Meiri

Chapple

2022

Journal of Biogeography

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Aim Many ectotherms are at risk from climate change as temperatures are increasingly exceeding their thermal limits. Many evaluations of the vulnerability of ectotherms to climate change have relied on statistical metrics derived from coarse‐scale climatic data, which may result in misleading predictions. By applying an integrative approach, we investigated geographical correlates of the vulnerability of lizards to climate change. Location Globally. Taxon Lizards. Methods We combined data on lizard thermal physiology and ecology, with high‐resolution climate data and biophysical modelling to assess lizards’ vulnerability to climate change. We calculated warming tolerance (difference between their body temperatures and upper thermal limits) and number of hours of activity. We investigated associations between warming tolerance and activity time with latitude, altitude and biome types. We compared our approach with traditional methods to calculate warming tolerance (using solely macroclimatic data). Results We found no latitudinal trend in the warming tolerance of lizards calculated from body temperature, but there was a weak negative correlation with altitude. We found associations between hours of activity and latitude and altitude. Desert species showed narrower warming tolerance than tropical and temperate species. Desert species and temperate species had reduced hours of activity when compared to tropical species. When warming tolerance was calculated from macroclimatic data, however, it was positively correlated with latitude and altitude, and species from tropical forested biomes showed narrow warming tolerances. Main Conclusions Vulnerability metrics calculated from macroclimatic data can produce divergent outcomes to those observed from fine‐scale climatic data. Our work indicates that the ability of desert and temperate lizard species to cope with heat stress by thermoregulating is more constrained than that of tropical species. Integrative assessments of ectotherms' vulnerability to climate change can highlight species and regions that should be prioritised for conservation management.

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Living on the edge: Lower thermal quality but greater survival probability at a high altitude mountain for the mesquite lizard (Sceloporus grammicus)

Cited by 21 publications

References 61 publications

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards

The biogeography of warming tolerance in lizards

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