Transplanting gravid lizards to high elevation alters maternal and embryonic oxygen physiology, but not reproductive success or hatchling phenotype

Abstract

Increased global temperatures have opened previously inhospitable habitats, such as at higher elevations. However, the reduction of oxygen partial pressure with increase in elevation represents an important physiological constraint that may limit colonization of such habitats, even if the thermal niche is appropriate. To test the mechanisms underlying the response to ecologically relevant levels of hypoxia, we performed a translocation experiment with the common wall lizard (Podarcis muralis), a widespread European lizard amenable to establishing populations outside its natural range. We investigated the impacts of hypoxia on the oxygen physiology and reproductive output of gravid common wall lizards and the subsequent development and morphology of their offspring. Lowland females transplanted to high elevations increased their haematocrit and haemoglobin concentration within days and maintained routine metabolism compared with lizards kept at native elevations. However, transplanted lizards suffered from increased reactive oxygen metabolite production near the oviposition date, suggesting a cost of reproduction at high elevation. Transplanted females and females native to different elevations did not differ in reproductive output (clutch size, egg mass, relative clutch mass or embryonic stage at oviposition) or in post-oviposition body condition. Developing embryos reduced heart rates and prolonged incubation times at high elevations within the native range and at extreme high elevations beyond the current range, but this reduced oxygen availability did not affect metabolic rate, hatching success or hatchling size. These results suggest that this opportunistic colonizer is capable of successfully responding to novel environmental constraints in these important life-history stages.

Water availability and temperature induce changes in oxidative status during pregnancy in a viviparous lizard

“…They were therefore likely to acclimatize and/or adapt their physiology to current local conditions (Dupoué, Rutschmann, Le Galliard, Miles, et al, ). Further experimental translocations and common garden experiments will therefore help depicting how natural constraints may shape reproductive investment, oxidative status and breeding success (Kouyoumdjian et al, ).…”

High‐elevation hypoxia impacts perinatal physiology and performance in a potential montane colonizer

“…Typical physiological adjustments to hypoxia in other taxa include suppressed embryo metabolism, often measured as reduced heart rate (Laughlin 1978;Monge & Leon-Velarde 1991;Crossley & Altimiras 2005;Crossley & Burggren 2009;Du et al 2011;Cordero et al 2017a,b;Kouyoumdjian et al 2019). However, heart rates of developing viperine snake embryos exhibited the opposite trend: their heart rates increased at EHE (Fig.…”

“…For instance, even short exposures to hypoxia can have lasting effects on subsequent growth and development of turtle embryos, including reduced mass at hatching, decreased oxygen consumption, and depressed metabolism, despite a comparable incubation period (Kam 1993;Cordero et al 2017a). Incubation in hypoxic conditions is known to reduce embryo heart rates (in lizards: Cordero et al 2017b;Kouyoumdjian et al 2019), produce smaller juveniles with decreased growth rate during the first months of life (in alligators: Owerkowicz et al 2009;in turtles: Wearing et al 2015), and increase heart and lung size at birth (in alligators: Owerkowicz et al 2009, andlizards: Cordero et al 2017b). Chronic hypoxia specifically elicits changes in the cardio-respiratory pathways (increases lung and heart size, higher blood pressure; Crossley & Altimiras 2005;Iungman & Piña 2013;Wearing et al 2015;Cordero et al 2017b), increases hematocrit and hemoglobin concentration (Vinegar & Hillyard 1972;Weathers & White 1972;Newlin & Ballinger 1976;González-Morales et al 2015;Lu et al 2015;Gangloff et al 2019), and alters muscle physiology (increases vascularization and myoglobin concentration; Jochmans-Lemoine & Joseph 2018).…”

“…2017b; Kouyoumdjian et al . 2019), produce smaller juveniles with decreased growth rate during the first months of life (in alligators: Owerkowicz et al . 2009; in turtles: Wearing et al .…”

A high mountain lizard from Peru: The world’s highest-altitude reptile

“…Adaptation to high elevation life in reptiles implicates different specialised anatomical and physiological strategies (Huey 1982;He et al 2013;Reguera et al 2014;Kouyoumdjian et al 2019), which scientists are recently beginning to understand at the genetic level (Yang et al 2014;Yang et al 2015;Li et al 2018). Factors identified as important in reptiles for allowing survival at the upper altitudinal limits relate to food availability and capacities for tolerating hypoxia and low temperatures (Navas 2002;Lu et al 2018;Gangloff et al 2019).…”