Seasonal reproductive endothermy in tegu lizards

Abstract

With some notable exceptions, small ectothermic vertebrates are incapable of endogenously sustaining a body temperature substantially above ambient temperature. This view was challenged by our observations of nighttime body temperatures sustained well above ambient (up to 10°C) during the reproductive season in tegu lizards (~2 kg). This led us to hypothesize that tegus have an enhanced capacity to augment heat production and heat conservation. Increased metabolic rates and decreased thermal conductance are the same mechanisms involved in body temperature regulation in those vertebrates traditionally acknowledged as "true endotherms": the birds and mammals. The appreciation that a modern ectotherm the size of the earliest mammals can sustain an elevated body temperature through metabolic rates approaching that of endotherms enlightens the debate over endothermy origins, providing support for the parental care model of endothermy, but not for the assimilation capacity model of endothermy. It also indicates that, contrary to prevailing notions, ectotherms can engage in facultative endothermy, providing a physiological analog in the evolutionary transition to true endothermy.

Keywords: Evolution; Life sciences; animal science; breeding season; endothermy; lizard; parental care; reptile; thermogenesis.

Fig. 1. Life cycle and seasonal changes in the daily profile of body temperature variation in the tegu lizard, with concomitant changes in the outside and burrow temperatures.

(A to C) The annual cycle (A) of tegu lizards is characterized by a reproductive season of mating and egg laying, a postreproductive season during the wet, warm summer months, a period of prolonged entrance into burrows during inclement weather, before a dormant period during the dry winter months. Averaged (±SEM; n = 4) monthly values (B) of tegu, burrow, and sunlight are shown plotted against hour of the day for the four periods of the year. The temperature difference (ΔT) between tegu and burrow temperature at the coldest time of the day (typically 4:00 a.m. to 6:00 a.m.) when tegus are inside their burrows is shown for the four different months (C). The temperature difference between tegu and burrow was greatest during the reproductive period in the month of October, as denoted by the asterisk (F_3,9 = 43.2; P < 0.001).

Fig. 2. Infrared thermal images of tegu lizards following prolonged absence of solar heat gain.

(A and B) A tegu lizard viewed before emerging from its burrow at first light in the morning (6:00 a.m.) during the reproductive season, demonstrating thermogenesis in an outside burrow (A). On a separate occasion, tegu lizards were imaged (10:00 a.m.) after extensive equilibration in a constant temperature environmental chamber, demonstrating cool skin temperature (B) whereas the core temperature, recovered from implanted data loggers, was much warmer.

Fig. 3. Body temperature–ambient temperature differences in outdoor burrows and under indoor conditions in male and female tegus.

Temperature differentials (mean daily values from the coldest period of the day: 4:00 a.m.) for individual tegus held under seminatural outdoor conditions for 7 days (T_b − T_burrow) and subsequently after transfer to constant temperature conditions indoors for 7 days (T_b − T_chamber). The thermogenic response observed indoors shows strong correlations with the thermogenic response observed outdoors as well as with sex, but not with body mass (r² = 0.352; outdoor P = 0.016; sex P = 0.037; mass P = 0.85), with males having an indoor ΔT 0.29°C cooler than females.

Fig. 4. Thermogenesis correlates with HRs in tegus in natural enclosures.

(A) Average (±SEM; shaded area) daily ΔT values (T_tegu − T_burrow) obtained during the daily minimum body temperature period (between 4:00 a.m. and 6:00 a.m.) from tegu lizards (n = 4) free to behave within outdoor enclosures. (B) Continuous records of average HRs (± SEM; shaded area) from the same time period of each day are also shown. Discrete feeding events are marked by small vertical lines in (A). The elevation in ΔT shows a strong correspondence (r² = 0.56) to the seasonal elevation in HR that cannot be explained strictly on the basis of biochemical Q₁₀ effects alone (that is, HR from July to November increases from 3 to 18 beats/min, whereas body temperature itself only changes from 16° to 26°C; the estimated Q₁₀ for this would be 6, which far exceeds normal biochemical Q₁₀ values of 2 to 3). Inset figure shows ΔT correlation with HR [type II Wald χ²_{df = 1} = 129; P < 0.0001] for the fed (gray symbol) and unfed (open symbols) periods; neither feeding status [type II Wald χ²_{df = 1} = 1.93; P = 0.16] nor body mass [type II Wald χ²_{df = 1} = 1.74; P < 0.18] had effects on ΔT.

Fig. 5. Thermogenesis in tegu lizards depends on changes in metabolism and in whole-body thermal conductance.

(A and B) Proposed model of seasonal endothermy in tegu lizards obtained from monthly averaged (early morning, predawn; n = 4 animals, two males and two females; 344 days of observations) HR values (A) and associated predicted metabolic rates (B) [from Piercy et al. (34)] from the postreproductive period (PR), entrance into dormancy period (EN), dormancy period (DR), and reproductive season (RS). Between the winter dormant period and the reproductive season, HR increases more than sixfold (despite body temperature changing by less than 10°C; see mean temperature ± SEM). (C) Graphical representation of the calculated relationship between thermal conductance and ΔT at different levels of metabolic rate for lizards. The thermal conductance for tegus (see fig. S6) is plotted against the ΔT values obtained for the nonreproductive tegus (solid circle; April) and reproductive tegus (open circle; October). Isopleths (gray lines) indicate the fold increase from the dormancy metabolic rate (of a tegu at T_b = 25°C) needed to produce the observed change in ΔT. The values calculated are consistent with those measured. Small changes in thermal conductance can have large effects on the ΔT. Squares represent conductance values (for comparison) from 300-g agamid lizards with ectothermic rates of metabolism, showing that a change from high air flow (filled) to low air flow (open) conditions in a burrow would have little effect on ΔT.