Oxygen supply limits the heat tolerance of lizard embryos

Smith, Colton D.; Telemeco, Rory S.; Angilletta, Michael J.; VandenBrooks, John M.

doi:10.1098/rsbl.2015.0113

Cited by 52 publications

(68 citation statements)

References 17 publications

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“…This was supported by experiments that induced hypoxia by simulating flood events (Kam 1994;Tucker et al 1997). Flooding also affects temperature and moisture, both of which exert combinatorial effects on the metabolism of reptilian embryos (Kam & Lillywhite 1994;Lungman & Piña 2013;Liang et al 2015;Smith et al 2015).…”

Section: Ecological and Evolutionary Implicationsmentioning

confidence: 99%

“…3 Fisher and Burggren 2007;Dunwoodie 2009;Liang et al 2015;Lungman and Piña 2013;Smith et al 2015). In oviparous tetrapods, embryo growth may be disrupted when gaseous O 2 in the egg incubation environment decreases below normal atmospheric conditions (< 21%; hypoxia hereafter) (Stock and Metcalfe 1987;Kam 1993a;Warburton et al 1995;Dzialowski et al 2002;Parker et al 2004;Chan and Burggren 2005;Eme et al 2013;Tate et al 2015).…”

Section: Introductionmentioning

confidence: 98%

“…Organisms are perhaps most vulnerable to environmental unpredictability during embryonic life stages. In addition to moisture and temperature, fluctuations in oxygen (O 2 ) may influence normal development of vital organs, survival and growth of vertebrate embryos (Kam & Lillywhite 1994;Fisher & Burggren 2007;Dunwoodie 2009;Lungman and Piña 2013;Liang et al 2015;Smith et al 2015). In oviparous tetrapods, embryo growth may be disrupted when gaseous O 2 in the egg incubation environment decreases below normal atmospheric conditions (<21%; hypoxia hereafter) (Stock & Metcalfe 1987;Kam 1993a;Warburton et al 1995;Dzialowski et al 2002;Parker et al 2004;Chan & Burggren 2005;Eme et al 2013;Tate et al 2015).…”

Section: Introductionmentioning

confidence: 99%

“…Flooding also affects temperature and moisture, both of which exert combinatorial effects on metabolism of reptilian embryos (Kam and Lillywhite 1994;Lungman and Piña 2013;Liang et al 2015;Smith et al 2015).…”

mentioning

confidence: 99%

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Effects of low‐oxygen conditions on embryo growth in the painted turtle, Chrysemys picta

Cordero

Karnatz

Svendsen

et al. 2017

Integrative Zoology

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Low-oxygen conditions (hypoxia; <21% O ) are considered unfavorable for growth; yet, embryos of many vertebrate taxa develop successfully in hypoxic subterranean environments. Although enhanced tolerance to hypoxia has been demonstrated in adult reptiles, such as in the painted turtle (Chrysemys picta), its effects on sensitive embryo life stages warrant attention. We tested the hypothesis that short-term hypoxia negatively affects growth during day 40 of development in C. picta, when O demands are highest in embryos. A brief, but severe, hypoxic event (5% O for 0.5 h) moderately affected embryo growth, causing a 13% reduction in mass (relative to a normoxic control). The same condition had no effect during day 27; instead, a nearly anoxic event (1% O for 72 h) caused a 5% mass reduction. All embryos survived the egg incubation period. Our study supports the assumption that reptilian embryos are resilient to intermittently low O in subterranean nests. Further work is needed to ascertain responses to suboptimal O levels while undergoing dynamic changes in developmental physiology.

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Section: Ecological and Evolutionary Implicationsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Effects of low‐oxygen conditions on embryo growth in the painted turtle, Chrysemys picta

Cordero

Karnatz

Svendsen

et al. 2017

Integrative Zoology

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“…This transient state could be physical connections between macromolecular structures, epigenetic state of the zygotic genome or metabolic states of the embryo and warrants further detailed investigations. For example, it has been shown that hypoxia lowers the temperature at which embryonic and organismal lethality occurs and hyperoxia enhances thermotolerance (Portner, 2002; Portner and Knust, 2007; Gendelman and Roth, 2012; Verberk et al, 2013; Smith et al, 2015). It may be interesting to connect the enhanced survival and reduced heat teratogenicity to mitochondrial divisions in the developing zebrafish embryo during the heat shocks, perhaps.…”

Section: Discussionmentioning

confidence: 99%

Transient window of resilience during early development minimizes teratogenic effects of heat in zebrafish embryos

Menon

Nair

2018

Developmental Dynamics

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Background: Transient heat shock during early development is an established experimental paradigm for doubling the genome of the zebrafish zygote, which has practical applications in expedited identification of recessive mutations in genetic screens. Despite the simplicity of the strategy and the genetic tractability of zebrafish, heat shock has not been used for genome doubling since the proof‐of‐principle experiments done in the 1980s. This is because of poor survival of embryos that ensue from transient heat shocks and gross developmental abnormalities in the few survivors, which is incompatible with phenotype driven screens. Results: We show that heat shocks during early zebrafish development uncouple the second cycle of DNA and centrosome duplication. Interestingly, the developmental time of the heat shock that triggers the dissociation between DNA and centrosome duplication cycles significantly affect the potential of embryos to survive and attain normal morphology. The potential to develop normally after a heat shock alters in a developmental time span of 2 min in zebrafish embryos, a phenomenon that has not been reported in any species. Conclusions: The existence of heat resilient developmental windows and reduced heat teratogenicity during these windows could be an effective step forward in practical application of transient heat for experimental manipulation of ploidy in zebrafish. More broadly, heat resilience before zygotic genome activation suggests that metazoan embryos may possess innate protective features against heat beyond the canonical heat shock response. Developmental Dynamics 247:992–1004, 2018. © 2018 Wiley Periodicals, Inc.

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Latitudinal embryonic thermal tolerance and plasticity shape the vulnerability of oviparous species to climate change

Sun

Wang

et al. 2021

Ecological Monographs

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Heat tolerance at the immobile embryonic stage is expected to be critical in determining species vulnerability to climate change. However, how the mean and developmental plasticity of embryonic heat tolerance vary geographically, and how these geographic variations affect species' vulnerability under climate change remain unknown. We experimentally determined the mean and developmental plasticity of embryonic acute heat tolerance (EAHT, i.e., heat shock temperature at which embryonic heartbeats ceased) for three latitudinally distributed populations of an oviparous lacertid lizard. The experimental results suggested that the mean EAHT decreased with decreasing latitude and that the reaction norms of EAHT in relation to developmental temperatures showed “flat,” “bell‐shaped,” and “decreasing” patterns at high, medium, and low latitudes, respectively. Based on the means and plasticity of EAHT and weather data across China, we project that the heat stress frequency would increase from the present to the future and increase toward low latitudes. Furthermore, heat stress becomes more extensive with the incorporation of developmental plasticity. Incorporating the mean EAHT during the embryonic development season, heat stress frequency, and climate variables in a species distribution model projects that suitable habitats could move northward in response to ongoing climate change and shrink due to the loss of southern habitat. Moreover, even lizards within the areas that are predicted to remain highly suitable are expected to experience increases in heat stress over time, particularly at medium and low latitudes. Our study reveals geographic variation in the mean and developmental plasticity of EAHT and highlights its importance for predicting species vulnerability and range shifts in response to climate change.

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Oxygen supply limits the heat tolerance of lizard embryos

Cited by 52 publications

References 17 publications

Effects of low‐oxygen conditions on embryo growth in the painted turtle, Chrysemys picta

Effects of low‐oxygen conditions on embryo growth in the painted turtle, Chrysemys picta

Transient window of resilience during early development minimizes teratogenic effects of heat in zebrafish embryos

Latitudinal embryonic thermal tolerance and plasticity shape the vulnerability of oviparous species to climate change

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