Oxygen Transport in the Avian Egg at High Altitude

Black, Craig Patrick; Snyder, Gregory K.

doi:10.1093/icb/20.2.461

Cited by 36 publications

(20 citation statements)

References 27 publications

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“…1). This finding is in agreement with previous studies, which have consistently shown chronic hypoxia to retard growth in embryos from all major clades of extant vertebrates: fish (Sundt-Hansen et al, 2007), amphibians (Bradford and Seymour, 1988;Mills and Barnhardt, 1999), mammals (Mortola et al, 2000;Zamudio et al, 2005;Julian et al, 2007); as well as reptiles: squamates (Herman and Ingermann, 1996;Andrews, 2001), turtles (Kam, 1993), crocodilians Crossley and Altimiras, 2005) and birds (Wangensteen et al, 1974;Black and Snyder, 1980;Xu and Mortola, 1988;Dzialowski et al, 2002;Crossley et al, 2003b) (reviewed by Chan and Burggren, 2005). Most recently, domestic chicken eggs have become a popular model to study the effects of chronic hypoxia on embryonic growth at altitude (Giussani et al, 2007).…”

Section: Growth Under Hypoxiasupporting

confidence: 93%

Atmospheric oxygen level affects growth trajectory, cardiopulmonary allometry and metabolic rate in the American alligator (Alligator mississippiensis)

Owerkowicz

Elsey

Hicks

2009

Journal of Experimental Biology

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SUMMARYRecent palaeoatmospheric models suggest large-scale fluctuations in ambient oxygen level over the past 550 million years. To better understand how global hypoxia and hyperoxia might have affected the growth and physiology of contemporary vertebrates, we incubated eggs and raised hatchlings of the American alligator. Crocodilians are one of few vertebrate taxa that survived these global changes with distinctly conservative morphology. We maintained animals at 30°C under chronic hypoxia (12% O 2 ), normoxia (21% O 2 ) or hyperoxia (30% O 2 ). At hatching, hypoxic animals were significantly smaller than their normoxic and hyperoxic siblings. Over the course of 3 months, post-hatching growth was fastest under hyperoxia and slowest under hypoxia. Hypoxia, but not hyperoxia, caused distinct scaling of major visceral organs -reduction of liver mass, enlargement of the heart and accelerated growth of lungs. When absorptive and post-absorptive metabolic rates were measured in juvenile alligators, the increase in oxygen consumption rate due to digestion/absorption of food was greatest in hyperoxic alligators and smallest in hypoxic ones. Hyperoxic alligators exhibited the lowest breathing rate and highest oxygen consumption per breath. We suggest that, despite compensatory cardiopulmonary remodelling, growth of hypoxic alligators is constrained by low atmospheric oxygen supply, which may limit their food utilisation capacity. Conversely, the combination of elevated metabolism and low cost of breathing in hyperoxic alligators allows for a greater proportion of metabolised energy to be available for growth. This suggests that growth and metabolic patterns of extinct vertebrates would have been significantly affected by changes in the atmospheric oxygen level.

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Section: Growth Under Hypoxiasupporting

confidence: 93%

Atmospheric oxygen level affects growth trajectory, cardiopulmonary allometry and metabolic rate in the American alligator (Alligator mississippiensis)

Owerkowicz

Elsey

Hicks

2009

Journal of Experimental Biology

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“…In addition, spatial changes in oxygen concentrations are known to exert major impacts on egg development. For example, it has consistently been shown in reptiles (Deeming & Ferguson, 1991;Kam, 1993;Warburton, Hastings & Wang, 1995;Andrews, 2002;Deeming, 2004) and birds (Black & Snyder, 1980;McCutcheon et al, 1982) that low levels of oxygen concentration reduce developmental success. Aspects such as embryonic differentiation and growth rates, water uptake, duration of incubation, growth of the chorioallantoic membrane, egg survival, and hatchling size are known to be negatively affected by hypoxia (Andrews, 2002;Parker, Andrews & Mathies, 2004).…”

Section: (D) the 'Bet-hedging Strategy' Hypothesismentioning

confidence: 99%

Fecundity selection theory: concepts and evidence

2015

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Fitness results from an optimal balance between survival, mating success and fecundity. The interactions between these three components of fitness vary depending on the selective context, from positive covariation between them, to antagonistic pleiotropic relationships when fitness increases in one reduce the fitness of others. Therefore, elucidating the routes through which selection shapes life history and phenotypic adaptations via these fitness components is of primary significance to understanding ecological and evolutionary dynamics. However, while the fitness components mediated by natural (survival) and sexual (mating success) selection have been debated extensively from most possible perspectives, fecundity selection remains considerably less studied. Here, we review the theoretical basis, evidence and implications of fecundity selection as a driver of sex-specific adaptive evolution. Based on accumulating literature on the life-history, phenotypic and ecological aspects of fecundity, we (i) suggest a re-arrangement of the concepts of fecundity, whereby we coin the term 'transient fecundity' to refer to brood size per reproductive episode, while 'annual' and 'lifetime fecundity' should not be used interchangeably with 'transient fecundity' as they represent different life-history parameters; (ii) provide a generalized re-definition of the concept of fecundity selection as a mechanism that encompasses any traits that influence fecundity in any direction (from high to low) and in either sex; (iii) review the (macro)ecological basis of fecundity selection (e.g. ecological pressures that influence predictable spatial variation in fecundity); (iv) suggest that most ecological theories of fecundity selection should be tested in organisms other than birds; (v) argue that the longstanding fecundity selection hypothesis of female-biased sexual size dimorphism (SSD) has gained inconsistent support, that strong fecundity selection does not necessarily drive female-biased SSD, and that this form of SSD can be driven by other selective pressures; and (vi) discuss cases in which fecundity selection operates on males. This conceptual analysis of the theory of fecundity selection promises to help illuminate one of the central components of fitness and its contribution to adaptive evolution.

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“…This 'hypoxia' hypothesis posits that decreasing oxygen availability creates natural selection for prolonged embryo retention within the female's body, where placental structures provide optimal levels of oxygen to complete development (Deeming, 2004;Lambert & Wiens, 2013). Numerous experimental studies on reptiles (Andrews, 2002;Deeming, 2004;Warburton, Hastings, & Wang, 1995) and birds (Black & Snyder, 1980;McCutcheon, Metcalfe, Metzenberg, & Ettinger, 1982) have consistently shown that low oxygen concentrations are detrimental to fitness via reduced developmental success. Developmental components such as embryonic differentiation and growth rates, water uptake, duration of incubation, growth of the chorioallantonic membrane, egg survival and hatchling size are known to be affected negatively by hypoxia (Andrews, 2002;Parker, Andrews, & Mathies, 2004).…”

Section: Introductionmentioning

confidence: 99%

Hypoxia and hypothermia as rival agents of selection driving the evolution of viviparity in lizards

Pincheira‐Donoso

Jara

Reaney

et al. 2017

Global Ecol Biogeogr

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Aim: The evolution of key innovations promotes adaptive radiations by opening access to novel ecological opportunity. The acquisition of viviparity (live-bearing reproduction) has emerged as one such innovation explaining reptile proliferations into extreme climates. By evolving viviparity, females provide embryos with internally stable environments to complete development. The classical hypothesis suggests that natural selection for viviparity arises from low temperatures in cold-climates, which promote prolonged egg retention in the mother’s body. An alternative hypothesis proposes that declines in atmospheric oxygen at high elevations create natural selection for embryo retention to provide them with optimal oxygen levels during development. However, although experimental studies support the negative effects of low oxygen on egg development, this ‘hypoxia’ hypothesis has never been tested quantitatively. Here, we compete the hypoxia hypothesis against the ‘cold-climate’ hypothesis, using a highly-diverse lizard genus.\ud Location: South America\ud Major taxa: Liolaemus lizards.\ud Methods: We employ a multivariate dataset covering 121-species varying extensively in geographic and climatic distribution (including extreme thermal and oxygen gradients), and parity mode. Based on a new molecular phylogeny for the genus, we use phylogenetic logistic regressions to generate a range of models ranking environmental factors as a function of their effects on parity mode transitions.\ud Results: Elevation and oxygen declines correlate nearly perfectly, and both were identified as the dominant predictors of oviparity-to-viviparity transitions, while the role for temperature (dominated by the coldest winter temperatures and daily fluctuations) is significant but secondary. Overall, we show that oxygen-deprivation and low temperatures both play a role in the evolution of viviparity.\ud Main conclusions: Our findings support the role for selection from declines in oxygen concentrations as the primary driver behind viviparity. However, selection arising from cold temperatures and from reduced fluctuations in daily temperatures contribute to the evolution of these transitions by creating multivariate selection on parity mode

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Oxygen Transport in the Avian Egg at High Altitude

Cited by 36 publications

References 27 publications

Atmospheric oxygen level affects growth trajectory, cardiopulmonary allometry and metabolic rate in the American alligator (Alligator mississippiensis)

Atmospheric oxygen level affects growth trajectory, cardiopulmonary allometry and metabolic rate in the American alligator (Alligator mississippiensis)

Fecundity selection theory: concepts and evidence

Hypoxia and hypothermia as rival agents of selection driving the evolution of viviparity in lizards

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