Literature DB >> 24619438

Improved heat tolerance in air drives the recurrent evolution of air-breathing.

Folco Giomi1, Marco Fusi, Alberto Barausse, Bruce Mostert, Hans-Otto Pörtner, Stefano Cannicci.   

Abstract

The transition to air-breathing by formerly aquatic species has occurred repeatedly and independently in fish, crabs and other animal phyla, but the proximate drivers of this key innovation remain a long-standing puzzle in evolutionary biology. Most studies attribute the onset of air-breathing to the repeated occurrence of aquatic hypoxia; however, this hypothesis leaves the current geographical distribution of the 300 genera of air-breathing crabs unexplained. Here, we show that their occurrence is mainly related to high environmental temperatures in the tropics. We also demonstrate in an amphibious crab that the reduced cost of oxygen supply in air extends aerobic performance to higher temperatures and thus widens the animal's thermal niche. These findings suggest that high water temperature as a driver consistently explains the numerous times air-breathing has evolved. The data also indicate a central role for oxygen- and capacity-limited thermal tolerance not only in shaping sensitivity to current climate change but also in underpinning the climate-dependent evolution of animals, in this case the evolution of air-breathing.

Entities:  

Keywords:  air-breathing evolution; heat tolerance; oxygen limitation; terrestrial colonization

Mesh:

Substances:

Year:  2014        PMID: 24619438      PMCID: PMC3973256          DOI: 10.1098/rspb.2013.2927

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  13 in total

1.  Evolutionary history of true crabs (Crustacea: Decapoda: Brachyura) and the origin of freshwater crabs.

Authors:  Ling Ming Tsang; Christoph D Schubart; Shane T Ahyong; Joelle C Y Lai; Eugene Y C Au; Tin-Yam Chan; Peter K L Ng; Ka Hou Chu
Journal:  Mol Biol Evol       Date:  2014-02-11       Impact factor: 16.240

2.  Oxygen limitation and thermal tolerance in two terrestrial arthropod species.

Authors:  Meagan M Stevens; Sue Jackson; Susan A Bester; John S Terblanche; Steven L Chown
Journal:  J Exp Biol       Date:  2010-07-01       Impact factor: 3.312

Review 3.  Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals.

Authors:  H O Pörtner
Journal:  Naturwissenschaften       Date:  2001-04

4.  Oxygen-limited thermal tolerance in Antarctic fish investigated by MRI and (31)P-MRS.

Authors:  F C Mark; C Bock; H O Pörtner
Journal:  Am J Physiol Regul Integr Comp Physiol       Date:  2002-11       Impact factor: 3.619

5.  Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado.

Authors:  M Frederich; H O Pörtner
Journal:  Am J Physiol Regul Integr Comp Physiol       Date:  2000-11       Impact factor: 3.619

6.  Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems.

Authors:  H-O Pörtner
Journal:  J Exp Biol       Date:  2010-03-15       Impact factor: 3.312

7.  Temperature-dependent oxygen extraction from the ventilatory current and the costs of ventilation in the cephalopod Sepia officinalis.

Authors:  Frank Melzner; Christian Bock; Hans O Pörtner
Journal:  J Comp Physiol B       Date:  2006-05-18       Impact factor: 2.200

Review 8.  Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals.

Authors:  H O Pörtner
Journal:  Comp Biochem Physiol A Mol Integr Physiol       Date:  2002-08       Impact factor: 2.320

9.  Running in the surf: hydrodynamics of the shore crab Grapsus tenuicrustatus.

Authors:  M M Martinez
Journal:  J Exp Biol       Date:  2001-09       Impact factor: 3.312

10.  A role for haemolymph oxygen capacity in heat tolerance of eurythermal crabs.

Authors:  Folco Giomi; Hans-Otto Pörtner
Journal:  Front Physiol       Date:  2013-05-15       Impact factor: 4.566

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  9 in total

1.  Cellular hallmarks reveal restricted aerobic metabolism at thermal limits.

Authors:  Aitana Neves; Coralie Busso; Pierre Gönczy
Journal:  Elife       Date:  2015-05-01       Impact factor: 8.140

2.  Oxygen-limited thermal tolerance is seen in a plastron-breathing insect and can be induced in a bimodal gas exchanger.

Authors:  Wilco C E P Verberk; David T Bilton
Journal:  J Exp Biol       Date:  2015-05-11       Impact factor: 3.312

3.  Physiological ecology meets climate change.

Authors:  Francisco Bozinovic; Hans-Otto Pörtner
Journal:  Ecol Evol       Date:  2015-02-05       Impact factor: 2.912

4.  The trade-off between heat tolerance and metabolic cost drives the bimodal life strategy at the air-water interface.

Authors:  Marco Fusi; Stefano Cannicci; Daniele Daffonchio; Bruce Mostert; Hans-Otto Pörtner; Folco Giomi
Journal:  Sci Rep       Date:  2016-01-13       Impact factor: 4.379

5.  Field and laboratory studies reveal interacting effects of stream oxygenation and warming on aquatic ectotherms.

Authors:  Wilco C E P Verberk; Isabelle Durance; Ian P Vaughan; Steve J Ormerod
Journal:  Glob Chang Biol       Date:  2016-02-29       Impact factor: 10.863

6.  Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra.

Authors:  Holger Kühnhold; Nuri Steinmann; Yi-Hsuan Huang; Lisa Indriana; Achim Meyer; Andreas Kunzmann
Journal:  PLoS One       Date:  2019-03-22       Impact factor: 3.240

7.  Morphological characteristics and abundance of prokaryotes associated with gills in mangrove brachyuran crabs living along a tidal gradient.

Authors:  Elisa Garuglieri; Jenny Marie Booth; Marco Fusi; Xinyuan Yang; Ramona Marasco; Tumeka Mbobo; Emanuela Clementi; Luciano Sacchi; Daniele Daffonchio
Journal:  PLoS One       Date:  2022-04-14       Impact factor: 3.752

Review 8.  Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence.

Authors:  Wilco C E P Verberk; Johannes Overgaard; Rasmus Ern; Mark Bayley; Tobias Wang; Leigh Boardman; John S Terblanche
Journal:  Comp Biochem Physiol A Mol Integr Physiol       Date:  2015-10-24       Impact factor: 2.320

9.  Thermal limits in native and alien freshwater peracarid Crustacea: The role of habitat use and oxygen limitation.

Authors:  Wilco C E P Verberk; Rob S E W Leuven; Gerard van der Velde; Friederike Gabel
Journal:  Funct Ecol       Date:  2018-02-06       Impact factor: 5.608

  9 in total

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