Relationship between oxidative stress and sexual coloration of lizards depends on thermal habitat.

Sexual signals serve as an honest indicator of individual quality, reflecting either developmental and/or maintenance costs. A possible underlying physiological mechanism is oxidative stress, which could mediate energy trade-offs between sexual signals and other quality traits. In ectotherms, thermal performance acts as a key indicator of individual quality and influence signal intensity. We investigated how oxidative state is reflected in visual signals of lizards from different thermal habitats. According to our hypothesis, efficient thermoregulation requires different strategies in different thermal environments. In a habitat with predictable temperature changes, animals are less exposed to suboptimal temperature ranges and selection will, therefore, be stronger on the maximum oxidative damage at optimal body temperature. Contrarily, in a habitat with rather stochastic thermal shifts, individuals are often constricted by suboptimal thermal conditions, and oxidative damage can be limiting on a wide temperature range. We used Iberolacerta cyreni and Psammodromus algirus inhabiting stochastic and predictable thermal environments respectively. We examined two aspects of oxidative stress: the level of reactive oxygen metabolites at the preferred temperature (maximal ROM) and the temperature range in which animals produce at least 80% of the maximum level of reactive oxygen metabolites (effective ROM range). In I. cyreni, we found that duller coloration was related to a wider effective ROM range, while expression of coloration in P. algirus was negatively correlated with the maximal ROM. Our results suggest that different thermal constraints affect different aspects of oxidative damage which can indicate individual quality and are, therefore, represented in sexual ornaments.

Evolutionary dynamics of two satellite DNA families in rock lizards of the genus Iberolacerta (Squamata, Lacertidae): different histories but common traits.

Satellite DNAs compose a large portion of all higher eukaryotic genomes. The turnover of these highly repetitive sequences is an important element in genome organization and evolution. However, information about the structure and dynamics of reptilian satellite DNA is still scarce. Two satellite DNA families, HindIII and TaqI, have been previously characterized in four species of the genus Iberolacerta. These families showed different chromosomal locations, abundances, and evolutionary rates. Here, we extend the study of both satellite DNAs (satDNAs) to the remaining Iberolacerta species, with the aim to investigate the patterns of variability and factors influencing the evolution of these repetitive sequences. Our results revealed disparate patterns but also common traits in the evolutionary histories of these satellite families: (i) each satellite DNA is made up of a library of monomer variants or subfamilies shared by related species; (ii) species-specific profiles of satellite repeats are shaped by expansions and/or contractions of different variants from the library; (iii) different turnover rates, even among closely related species, result in great differences in overall sequence homogeneity and in concerted or non-concerted evolution patterns, which may not reflect the phylogenetic relationships among taxa. Contrasting turnover rates are possibly related to genomic constraints such as karyotype architecture and the interspersed organization of diverging repeat variants in satellite arrays. Moreover, rapid changes in copy number, especially in the centromeric HindIII satDNA, may have been associated with chromosomal rearrangements and even contributed to speciation within Iberolacerta.

Adaptive seasonal shifts in the thermal preferences of the lizard Iberolacerta galani (Squamata, Lacertidae).

The León rock lizard, Iberolacerta galani, lives in isolated mountains of Spain. We studied the seasonal changes in the thermal biology of I. galani between spring and summer. We calculated precision, accuracy and effectiveness of thermoregulation and the habitat thermal quality for spring, and compared with the values of summer. In addition, we studied how the shift in the thermal preferences of lizards would contribute to achieve a higher effectiveness of thermoregulation. Thermal preferences of León rock lizards are among the lowest in lacertids, and are also very narrow, maintaining the narrowness among seasons. As for summer (27.90-29.70°C, mean value =28.76°C), the thermal preferences of I. galani are also low in spring (29.60-31.10°C, mean value =30.38°C), supporting the idea that this species is adapted to cold environments. The habitat thermal quality is lower in spring (10.99°C) than in summer (9.36°C), while the effectiveness of thermoregulation is higher in spring (0.92) than in summer (0.80). We found that the seasonal shift in thermal preferences contributes significantly to enhance the effectiveness of thermoregulation in both seasons, more in spring (0.45°C) than in summer (0.16°C). Because I. galani inhabits isolated mountains, where the activity period is reduced from April to October, we hypothesize that the observed adaptation of the thermal preferences, which enhance thermoregulation to a larger extent in spring, may evolved to maximize performance during the reproductive season.

The peak of thermoregulation effectiveness: Thermal biology of the Pyrenean rock lizard, Iberolacerta bonnali (Squamata, Lacertidae).

We studied, at 2200m altitude, the thermal biology of the Pyrenean rock lizard, Iberolacerta bonnali, in the glacial cirque of Cotatuero (National Park of Ordesa, Huesca, Spain). The preferred thermal range (PTR) of I. bonnali indicates that it is a cold-adapted ectotherm with a narrow PTR (29.20-32.77°C). However, its PTR (3.57°C) is twice as wide as other Iberolacerta lizards, which may be explained by its broader historical distribution. The studied area is formed by a mosaic of microhabitats which offer different operative temperatures, so that lizards have, throughout their entire daily period of activity, the opportunity to choose the most thermally suitable substrates. I. bonnali achieves an effectiveness of thermoregulation of 0.95, which makes it the highest value found to date among the Lacertidae, and one of the highest among lizards. Their relatively wide distribution, their wider PTR, and their excellent ability of thermoregulation, would make I. bonnali lizards less vulnerable to climate change than other species of Iberolacerta. Thanks to its difficult access, the studied area is not visited by a large number of tourists, as are other areas of the National Park. Thus, it is a key area for the conservation of the Pyrenean rock lizard. By shuttling between suitable microhabitats, lizards achieve suitable body temperatures during all day. However, such thermally suitable microhabitats should vary in other traits than thermal quality, such as prey availability or predation risk. Hence, it seems that these not-thermal traits are not constraining habitat selection and thermoregulation in this population. Therefore, future research in this population may study the causes that would lead lizards to prioritize thermoregulation to such extent in this population.

The role of metabolism in understanding the altitudinal segregation pattern of two potentially interacting lizards.

Sympatric species from the same ecological guild, that exhibit partial altitudinal segregation, can potentially interact in areas of syntopic occurrence. Besides general species' ecology, physiology can provide important answers about species interactions reflected in altitudinal patterns. Lizards Podarcis muralis and Iberolacerta horvathi exhibit partial altitudinal segregation, while they strongly resemble in overall morphology and ecology (diet, daily and seasonal activity pattern), but show certain degree of physiological dissimilarity. They have similar mean preferred body temperatures and patterns of seasonal and daily variations but differ in the magnitude of seasonal variation. Since an ectotherm metabolism is highly dependent on body temperature, thermoregulation is expected to directly affect their metabolism. We compared metabolic rates of adult males from an area of sympatry, measured under two temperature regimes (20°C and 28°C). Both species increased metabolic rates with temperature in a similar pattern. We also compared electron transport activity from tail tissues which provide values of species' potential metabolic activity (enzymatic capacity). Species clearly differed in potential metabolic activity; I. horvathi attained higher values than P. muralis. No difference was detected in how species exploited this potential (calculated from the ratio of electron transport activity and metabolic rates). However, we observed higher potential metabolic activity I. horvathi which together with the ability to thermoregulate more precisely could represent a higher competitive advantage over P. muralis in thermally more restrictive environments such as higher altitudes. Understanding of metabolism seems to provide valuable information for understanding recent distributional patterns as well as species interactions.

Behavioral buffering of global warming in a cold-adapted lizard.

Alpine lizards living in restricted areas might be particularly sensitive to climate change. We studied thermal biology of Iberolacerta cyreni in high mountains of central Spain. Our results suggest that I. cyreni is a cold-adapted thermal specialist and an effective thermoregulator. Among ectotherms, thermal specialists are more threatened by global warming than generalists. Alpine lizards have no chance to disperse to new suitable habitats. In addition, physiological plasticity is unlikely to keep pace with the expected rates of environmental warming. Thus, lizards might rely on their behavior in order to deal with ongoing climate warming. Plasticity of thermoregulatory behavior has been proposed to buffer the rise of environmental temperatures. Therefore, we studied the change in body and environmental temperatures, as well as their relationships, for I. cyreni between the 1980s and 2012. Air temperatures have increased more than 3.5°C and substrate temperatures have increased by 6°C in the habitat of I. cyreni over the last 25 years. However, body temperatures of lizards have increased less than 2°C in the same period, and the linear relationship between body and environmental temperatures remains similar. These results show that alpine lizards are buffering the potential impact of the increase in their environmental temperatures, most probably by means of their behavior. Body temperatures of I. cyreni are still cold enough to avoid any drop in fitness. Nonetheless, if warming continues, behavioral buffering might eventually become useless, as it would imply spending too much time in shelter, losing feeding, and mating opportunities. Eventually, if body temperature exceeds the thermal optimum in the near future, fitness would decrease abruptly.

Are mountain habitats becoming more suitable for generalist than cold-adapted lizards thermoregulation?

Mountain lizards are highly vulnerable to climate change, and the continuous warming of their habitats could be seriously threatening their survival. We aim to compare the thermal ecology and microhabitat selection of a mountain lizard, Iberolacerta galani, and a widely distributed lizard, Podarcis bocagei, in a montane area. Both species are currently in close syntopy in the study area, at 1,400 m above the sea level. We determined the precision, accuracy and effectiveness of thermoregulation, and the thermal quality of habitat for both species. We also compared the selection of thermal microhabitats between both species. Results show that I. galani is a cold-adapted thermal specialist with a preferred temperature range of 27.9-29.7 °C, while P. bocagei would be a thermal generalist, with a broader and higher preferred temperature range (30.1-34.5 °C). In addition, I. galani selects rocky substrates while P. bocagei selects warmer soil and leaf litter substrates. The thermal quality of the habitat is higher for P. bocagei than for I. galani. Finally, P. bocagei achieves a significantly higher effectiveness of thermoregulation (0.87) than I. galani (0.80). Therefore, these mountain habitat conditions seem currently more suitable for performance of thermophilic generalist lizards than for cold-specialist lizards.