Manipulating plasma thyroid hormone levels alters development of endothermy and ventilation in nestling red-winged blackbirds

Abstract

Thyroid hormones are key regulators of development and metabolism in vertebrates. During the nestling period, young of altricial species transition from an ectothermic phenotype to an endothermic phenotype. Red-winged blackbirds are an altricial species that exhibit an increase in plasma 3,3’, 5-triiodo-L-thyronine (T3) levels during the first 5 days post-hatch (dph), begin to develop endothermic metabolic responses by 7 dph, and fledge within 10 days of hatching. We propose that thyroid hormones play an important role in regulating development of endothermy during the nestling period in altricial birds. To better understand the effects of thyroid hormones on endothermic metabolic development in an altricial species, we treated nestling red-winged blackbirds on 2, 3, and 5 dph with either methimazole (MMI) to induce hypothyroidism or supplemental T3 to induce hyperthyroidism. We then measured on 5, 7, and 9 dph morphology and whole animal O2 consumption (V˙o2) and ventilation in the thermal neutral zone and during gradual cooling. Treatment of nestlings with MMI resulted in lower plasma T3 levels on 5 dph that recovered by 7 dph, while supplementing with T3 did not affect plasma T3 levels on 5, 7 and 9 dph. Treatment with MMI resulted in smaller nestlings with smaller hearts and structural characters such as wing chord and femur length, but larger lungs and kidneys. Treatment with T3 produced smaller nestlings with smaller body masses and shorter femur and tarsus lengths. The development of V˙o2 and ventilation endothermic responses to gradual cooling in MMI treated nestlings were delayed when compared with control nestlings. In 9 dph nestlings, hypothyroidism resulted in alterations in the responses of ventilation frequency and tidal volume to cooling when compared with the control nestlings. Supplemental T3 had no effect on the development of V˙o2 and ventilation in the thermal neutral zone or in response to cooling. Our data suggest plasma thyroid hormone levels play an active role in the systemic development of endothermic capacity and the development of ventilatory control. In the nestling avian, multiple systems develop in concert to produce an endothermic phenotype, but reduced thyroid hormone delays maturation of endothermic capacity.

Mitochondrial function is enhanced by thyroid hormones during zebra finch development

“…As expected, T3 levels in the TH-chicks were statistically marginally higher than in the control group (pmol ml −1 estimate [95% CrI], P(ß > 0): 0.127 [−0.016; 0.268], 0.962) and meaningfully higher when TH-validation chicks and TH-chicks were analysed together (pmol ml −1 estimate [95% CrI], P(ß > 0): 0.206 [0.066; 0.348], 0.997) (see figure 2, electronic supplementary material, table S2). Furthermore, T3-levels were similar to those observed in nestlings of other passerine species, red-winged blackbirds (Agelaius phoenicius) [33] and great tits [78].…”

“…For this reason, T3 was administered every second day (i.e. on dph 5, 7, 9, 11 and 13 with a 200 μl pipette, adjusted to the exact body mass of each chick, ± 0.01 g) to obtain peaks of elevated T3 levels throughout the main growth period between 5 and 14 dph [ 33 , 59 ]. Blood sampling was done at 14 dph ( ca 20 h after T3 administration in the experimental group) to measure circulating T3 concentrations and mitochondria function.…”

“…In the TH-chicks, the last T3 dose was given at noon on 13 dph and blood sampling (see §2.6) was done at 14 dph at around 09.00. Hence, it is likely that T3 given on 13 dph had been metabolized in large parts before blood sampling [ 33 , 59 , 60 ], and therefore T3 plasma levels at that time point do not reflect the full extent to which T3 plasma levels where raised on multiple occasions throughout the treatment period. To confirm that the treatment did in fact raise T3 plasma levels as expected, we added the so-called ‘TH-validation’ group ( n = 7) to our experiment.…”

“…However, in altricial hatchlings, TH levels have been shown to rise steadily in the first week after hatching and reach adult levels around fledging-in parallel with the hatchlings' growth patterns, and thus, post-hatching TH and growth patterns should be studied [25]. Although some studies have addressed the effects of TH on growth in altricial nestlings, results across studies are inconclusive [25][26][27][28][29][30][31][32][33][34][35][36]. In great tits, prenatal TH manipulations had no effect on growth at any stage [26].…”

“…These studies show that both hypo- and hyper-thyroidal conditions reduce growth and development [ 6 , 37 – 39 ]. Furthermore, in red-winged blackbird ( Agelaius phoenicius ) nestlings, hyper- and hypo-thyroidal conditions led to reduced skeletal growth, compared with unmanipulated nestlings [ 33 ] and in the zebra finch ( Taeniopygia guttata ), TH-inhibition was related to decreased growth [ 34 ]. However, it has remained unclear whether these relationships are induced by pharmacological TH concentrations or in fact do occur at physiological TH concentrations as well.…”