Thyroid Development in Relation to the Development of Endothermy in the Red-Winged Blackbird (Agelaius phoeniceus)

Olson, John M.; McNabb, F. M. Anne; Jablonski, Miroslawa S.; Ferris, David V.

doi:10.1006/gcen.1999.7363

Cited by 22 publications

(22 citation statements)

References 24 publications

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“…Interestingly, the age-related rises in myofiber and isolated mitochondria respiration occurred in parallel with increasing expression of an avian uncoupling protein (14b) suggesting processes favoring mitochondrial heat generation during development in Adelie penguin pectoralis muscle. Mechanisms controlling muscle bioenergetics in Adélie penguin chicks are unknown but may possibly involve thyroid hormones that control mitochondrial biogenesis and oxidative metabolism in mammals and birds (53,57) and showing parallel development during the ontogenesis of thermoregulation and muscle oxidative capacity in altricial birds (34,35,53,57). Transcriptional regulators such as peroxisome proliferator-activated receptor coactivator-1␣ (PGC-1␣) that control mitochondrial biogenesis and oxidative metabolism (30), with specific effects on SS mitochondria at modest muscle overexpression (7), may also be involved.…”

Section: Discussionmentioning

confidence: 99%

Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae)

Fongy

Romestaing

Blanc

et al. 2013

American Journal of Physiology-Regulatory, Integrative and Comp

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The ontogeny of pectoralis muscle bioenergetics was studied in growing Adélie penguin chicks during the first month after hatching and compared with adults using permeabilized fibers and isolated mitochondria. With pyruvate-malate-succinate or palmitoyl-carnitine as substrates, permeabilized fiber respiration markedly increased during chick growth (3-fold) and further rose in adults (1.4-fold). Several markers of muscle fiber oxidative activity (cytochrome oxidase, citrate synthase, hydroxyl-acyl-CoA dehydrogenase) increased 6- to 19-fold with age together with large rises in intermyofibrillar (IMF) and subsarcolemmal (SS) mitochondrial content (3- to 5-fold) and oxidative activities (1.5- to 2.4-fold). The proportion of IMF relative to SS mitochondria increased with chick age but markedly dropped in adults. Differences in oxidative activity between mitochondrial fractions were reduced in adults compared with hatched chicks. Extrapolation of mitochondrial to muscle respirations revealed similar figures with isolated mitochondria and permeabilized fibers with carbohydrate-derived but not with lipid-derived substrates, suggesting diffusion limitations of lipid substrates with permeabilized fibers. Two immunoreactive fusion proteins, mitofusin 2 (Mfn2) and optic atrophy 1 (OPA1), were detected by Western blots on mitochondrial extracts and their relative abundance increased with age. Muscle fiber respiration was positively related with Mfn2 and OPA1 relative abundance. Present data showed by two complementary techniques large ontogenic increases in muscle oxidative activity that may enable birds to face thermal emancipation and growth in childhood and marine life in adulthood. The concomitant rise in mitochondrial fusion protein abundance suggests a role of mitochondrial networks in the skeletal muscle processes of bioenergetics that enable penguins to overcome harsh environmental constraints.

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Section: Discussionmentioning

confidence: 99%

Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae)

Fongy

Romestaing

Blanc

et al. 2013

American Journal of Physiology-Regulatory, Integrative and Comp

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“…In precocial species, plasma thyroid levels peak at hatching and decline markedly during the first 3 weeks after hatch whereas altricial species show a rapid post-hatching increase in levels of thyroid hormone that parallels body growth (McNabb et al 1984). Olson et al (1999) found that plasma thyroid levels in Redwinged Blackbirds increased after hatching, peaked around 7-8 dph and then declined, a time-course consistent with development of endothermy in this species and parallel with the upregulation of PGC-1α observed during this experiment.…”

Section: Developmental Patterns Of Gene Expressionmentioning

confidence: 99%

The 12-day thermoregulatory metamorphosis of Red-winged Blackbirds (Agelaius phoeniceus)

Sirsat

Crossley

et al. 2016

J Comp Physiol B

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We examined development of endothermy in altricial Red-winged Blackbirds (Agelaius phoeniceus) by measuring oxygen consumption [Formula: see text], body temperature and ventilation at ambient temperatures from 35 to 15 °C. Mitochondrial respiration of permeabilized skeletal muscle was also measured from breast (pectoralis) and thigh (femorotibialis) muscles. Animals were studied from the first day of hatching through fledging (12 days post-hatch, dph). Nestling whole-body metabolic rate began to show an endothermic response to cold temperature midway between hatching and fledging. Nestlings less than 5 dph were unable to maintain elevated [Formula: see text] and body temperature when exposed to gradually decreasing temperature, whereas 7 dph nestlings maintained [Formula: see text] until ~25 °C, after which [Formula: see text] decreased. From 10 dph to fledging, animals maintained elevated [Formula: see text] and body temperature when exposed to gradual cooling; full endothermic capacity was achieved. Ventilation followed a similar developmental trend to that of [Formula: see text], with increases in 10 dph fledglings occurring in tidal volume rather than ventilation frequency. LEAK respiration and oxidative phosphorylation (OXPHOS) through complex I of breast muscle mitochondria increased significantly after 3 dph. Expression of avUCP and PCG-1α mRNA increased significantly at 3 dph and remained elevated in both skeletal muscle types. Increased metabolic capacity at the cellular level occurred prior to that of the whole animal. This change in whole animal metabolic capacity increased steadily upon hatching as evidenced by the shift of metabolic rate from an ectothermic to endothermic phenotype and the increase of mitochondrial OXPHOS activity of the shivering muscles of this altricial avian species.

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“…They hatch naked, show no thermoregulatory responses until some days or even weeks after hatching, and they are fully dependent on parental care (Figure 2). Although the distinction between precocial and altricial birds is largely based on morphological and behavioral traits, there are some marked differences in thyroid physiology as well: the perihatch peak of circulating THs is absent in ring doves ( Streptopelia risoria ) and in passerines like European starlings ( Sturnus vulgaris ), red-winged blackbirds ( Agelaius phoeniceus ), and great tits ( Parus major ) (Schew et al, 1996; Silverin and Rudas, 1996; Výboh et al, 1996; Olson et al, 1999; reviewed by McNabb, 2006), suggesting that this is the common pattern for altricial birds. Typically, circulating TH concentrations in these birds are very low during embryonic life, and then increase gradually to reach adult concentrations some days or weeks post-hatch (Figure 1B).…”

Section: Thyroid Hormone Levels In the Perihatch Periodmentioning

confidence: 99%

Hatching the Cleidoic Egg: The Role of Thyroid Hormones

Groef¹,

Grommen²,

Darras³

2013

Front. Endocrinol.

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A major life stage transition in birds and other oviparous sauropsids is the hatching of the cleidoic egg. Not unlike amphibian metamorphosis, hatching in these species can be regarded as a transition from a relatively well-protected “aqueous” environment to a more hazardous and terrestrial life outside the egg, a transition in which thyroid hormones (THs) (often in concert with glucocorticoids) play an important role. In precocial birds such as the chicken, the perihatch period is characterized by peak values of THs. THs are implicated in the control of muscle development, lung maturation and the switch from chorioallantoic to pulmonary respiration, yolk sac retraction, gut development and induction of hepatic genes to accommodate the change in dietary energy source, initiation of thermoregulation, and the final stages of brain maturation as well as early post-hatch imprinting behavior. There is evidence that, at least for some of these processes, THs may have similar roles in non-avian sauropsids. In altricial birds such as passerines on the other hand, THs do not rise significantly until well after hatching and peak values coincide with the development of endothermy. It is not known how hatching-associated processes are regulated by hormones in these animals or how this developmental mode evolved from TH-dependent precocial hatching.

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Thyroid Development in Relation to the Development of Endothermy in the Red-Winged Blackbird (Agelaius phoeniceus)

Cited by 22 publications

References 24 publications

Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae)

Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae)

The 12-day thermoregulatory metamorphosis of Red-winged Blackbirds (Agelaius phoeniceus)

Hatching the Cleidoic Egg: The Role of Thyroid Hormones

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