Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America

Autores
Coelho Faria, Samuel; Bianchini, Adalto; Machado Lauer, Mariana; Ribeiro Latorre Zimbardi, Ana Lúcia; Tapella, Federico; Romero, Maria Carolina; Campbell McNamara, John
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Temperature is an important abiotic factor that drives the evolution of ectotherms owing to its pervasive effects at all levels of organization. Although a species’ thermal tolerance is environmentally driven within a spatial cline, it may be constrained over time due to differential phylogenetic inheritance. At the limits of thermal tolerance, hemolymph oxygen is reduced and lactate formation is increased due to mismatch between oxygen supply and demand; imbalance between enzyme flexibility/stability also impairs the ability to generate energy. Here, we characterized the effects of lower (LL50) and upper (UL50) critical thermal limits on selected descriptors of aerobic and anaerobic metabolism in 12 intertidal crab species distributed from northern Brazil (≈7.8°S) to southern Patagonia (≈53.2°S), considering their phylogeny. We tested for (i) functional trade-offs regarding aerobic and anaerobic metabolism and LDH kinetics in shaping thermal tolerance; (ii) influence of shared ancestry and thermal province on metabolic evolution; and (iii) presence of evolutionary convergences and adaptive peaks in the crab phylogeny. The tropical and subtropical species showed similar systemic and kinetic responses, both differing from the sub-Antarctic crabs. The lower UL50’s of the sub-Antarctic crabs may reflect mismatch between the evolution of aerobic and anaerobic metabolism since these crabs exhibit lower oxygen consumption but higher lactate formation than tropical and subtropical species also at their respective UL50’s. LDH activity increased with temperature increase, while KmPyr remained fairly constant; catalytic coefficient correlated negatively with thermal niche. Thermal tolerance may rely on a putative evolutionary trade-off between aerobic and anaerobic metabolism regarding energy supply, while temperature compensation of kinetic performance is driven by thermal habitat as revealed by the LDH affinity/efficiency equilibrium. The overall physiological evolution revealed two homoplastic adaptive peaks in the sub-Antarctic crabs with a further shift in the tropical/subtropical clade. The physiological traits at UL50 have evolved in a phylogenetic manner while all others were more plastic. Thus, shared inheritance and thermal environment have driven the crabs’ thermal tolerance and metabolic evolution, revealing physiological transformations that have arisen in both colder and warmer climes, especially at higher levels of biological organization and phylogenetic diversity.
Fil: Coelho Faria, Samuel. Universidade de Sao Paulo; Brasil
Fil: Bianchini, Adalto. Universidade Federal Do Rio Grande.; Brasil
Fil: Machado Lauer, Mariana. Universidade Federal Do Rio Grande.; Brasil
Fil: Ribeiro Latorre Zimbardi, Ana Lúcia. Universidade de Sao Paulo; Brasil
Fil: Tapella, Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Austral de Investigaciones Científicas; Argentina
Fil: Romero, Maria Carolina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Austral de Investigaciones Científicas; Argentina
Fil: Campbell McNamara, John. Universidade de Sao Paulo; Brasil
Materia
BRACHYURA
CRITICAL LIMITS
EVOLUTIONARY PHYSIOLOGY
LACTATE
LDH
OXYGEN CONSUMPTION
THERMAL ADAPTATION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/141543

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repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South AmericaCoelho Faria, SamuelBianchini, AdaltoMachado Lauer, MarianaRibeiro Latorre Zimbardi, Ana LúciaTapella, FedericoRomero, Maria CarolinaCampbell McNamara, JohnBRACHYURACRITICAL LIMITSEVOLUTIONARY PHYSIOLOGYLACTATELDHOXYGEN CONSUMPTIONTHERMAL ADAPTATIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Temperature is an important abiotic factor that drives the evolution of ectotherms owing to its pervasive effects at all levels of organization. Although a species’ thermal tolerance is environmentally driven within a spatial cline, it may be constrained over time due to differential phylogenetic inheritance. At the limits of thermal tolerance, hemolymph oxygen is reduced and lactate formation is increased due to mismatch between oxygen supply and demand; imbalance between enzyme flexibility/stability also impairs the ability to generate energy. Here, we characterized the effects of lower (LL50) and upper (UL50) critical thermal limits on selected descriptors of aerobic and anaerobic metabolism in 12 intertidal crab species distributed from northern Brazil (≈7.8°S) to southern Patagonia (≈53.2°S), considering their phylogeny. We tested for (i) functional trade-offs regarding aerobic and anaerobic metabolism and LDH kinetics in shaping thermal tolerance; (ii) influence of shared ancestry and thermal province on metabolic evolution; and (iii) presence of evolutionary convergences and adaptive peaks in the crab phylogeny. The tropical and subtropical species showed similar systemic and kinetic responses, both differing from the sub-Antarctic crabs. The lower UL50’s of the sub-Antarctic crabs may reflect mismatch between the evolution of aerobic and anaerobic metabolism since these crabs exhibit lower oxygen consumption but higher lactate formation than tropical and subtropical species also at their respective UL50’s. LDH activity increased with temperature increase, while KmPyr remained fairly constant; catalytic coefficient correlated negatively with thermal niche. Thermal tolerance may rely on a putative evolutionary trade-off between aerobic and anaerobic metabolism regarding energy supply, while temperature compensation of kinetic performance is driven by thermal habitat as revealed by the LDH affinity/efficiency equilibrium. The overall physiological evolution revealed two homoplastic adaptive peaks in the sub-Antarctic crabs with a further shift in the tropical/subtropical clade. The physiological traits at UL50 have evolved in a phylogenetic manner while all others were more plastic. Thus, shared inheritance and thermal environment have driven the crabs’ thermal tolerance and metabolic evolution, revealing physiological transformations that have arisen in both colder and warmer climes, especially at higher levels of biological organization and phylogenetic diversity.Fil: Coelho Faria, Samuel. Universidade de Sao Paulo; BrasilFil: Bianchini, Adalto. Universidade Federal Do Rio Grande.; BrasilFil: Machado Lauer, Mariana. Universidade Federal Do Rio Grande.; BrasilFil: Ribeiro Latorre Zimbardi, Ana Lúcia. Universidade de Sao Paulo; BrasilFil: Tapella, Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Austral de Investigaciones Científicas; ArgentinaFil: Romero, Maria Carolina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Austral de Investigaciones Científicas; ArgentinaFil: Campbell McNamara, John. Universidade de Sao Paulo; BrasilFrontiers Media S.A.2020-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/141543Coelho Faria, Samuel; Bianchini, Adalto; Machado Lauer, Mariana; Ribeiro Latorre Zimbardi, Ana Lúcia; Tapella, Federico; et al.; Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America; Frontiers Media S.A.; Frontiers in Physiology; 11; 4-2020; 1-151664-042XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/article/10.3389/fphys.2020.00312/fullinfo:eu-repo/semantics/altIdentifier/doi/10.3389/fphys.2020.00312info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:09:40Zoai:ri.conicet.gov.ar:11336/141543instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:09:40.618CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America
title Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America
spellingShingle Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America
Coelho Faria, Samuel
BRACHYURA
CRITICAL LIMITS
EVOLUTIONARY PHYSIOLOGY
LACTATE
LDH
OXYGEN CONSUMPTION
THERMAL ADAPTATION
title_short Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America
title_full Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America
title_fullStr Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America
title_full_unstemmed Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America
title_sort Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America
dc.creator.none.fl_str_mv Coelho Faria, Samuel
Bianchini, Adalto
Machado Lauer, Mariana
Ribeiro Latorre Zimbardi, Ana Lúcia
Tapella, Federico
Romero, Maria Carolina
Campbell McNamara, John
author Coelho Faria, Samuel
author_facet Coelho Faria, Samuel
Bianchini, Adalto
Machado Lauer, Mariana
Ribeiro Latorre Zimbardi, Ana Lúcia
Tapella, Federico
Romero, Maria Carolina
Campbell McNamara, John
author_role author
author2 Bianchini, Adalto
Machado Lauer, Mariana
Ribeiro Latorre Zimbardi, Ana Lúcia
Tapella, Federico
Romero, Maria Carolina
Campbell McNamara, John
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv BRACHYURA
CRITICAL LIMITS
EVOLUTIONARY PHYSIOLOGY
LACTATE
LDH
OXYGEN CONSUMPTION
THERMAL ADAPTATION
topic BRACHYURA
CRITICAL LIMITS
EVOLUTIONARY PHYSIOLOGY
LACTATE
LDH
OXYGEN CONSUMPTION
THERMAL ADAPTATION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Temperature is an important abiotic factor that drives the evolution of ectotherms owing to its pervasive effects at all levels of organization. Although a species’ thermal tolerance is environmentally driven within a spatial cline, it may be constrained over time due to differential phylogenetic inheritance. At the limits of thermal tolerance, hemolymph oxygen is reduced and lactate formation is increased due to mismatch between oxygen supply and demand; imbalance between enzyme flexibility/stability also impairs the ability to generate energy. Here, we characterized the effects of lower (LL50) and upper (UL50) critical thermal limits on selected descriptors of aerobic and anaerobic metabolism in 12 intertidal crab species distributed from northern Brazil (≈7.8°S) to southern Patagonia (≈53.2°S), considering their phylogeny. We tested for (i) functional trade-offs regarding aerobic and anaerobic metabolism and LDH kinetics in shaping thermal tolerance; (ii) influence of shared ancestry and thermal province on metabolic evolution; and (iii) presence of evolutionary convergences and adaptive peaks in the crab phylogeny. The tropical and subtropical species showed similar systemic and kinetic responses, both differing from the sub-Antarctic crabs. The lower UL50’s of the sub-Antarctic crabs may reflect mismatch between the evolution of aerobic and anaerobic metabolism since these crabs exhibit lower oxygen consumption but higher lactate formation than tropical and subtropical species also at their respective UL50’s. LDH activity increased with temperature increase, while KmPyr remained fairly constant; catalytic coefficient correlated negatively with thermal niche. Thermal tolerance may rely on a putative evolutionary trade-off between aerobic and anaerobic metabolism regarding energy supply, while temperature compensation of kinetic performance is driven by thermal habitat as revealed by the LDH affinity/efficiency equilibrium. The overall physiological evolution revealed two homoplastic adaptive peaks in the sub-Antarctic crabs with a further shift in the tropical/subtropical clade. The physiological traits at UL50 have evolved in a phylogenetic manner while all others were more plastic. Thus, shared inheritance and thermal environment have driven the crabs’ thermal tolerance and metabolic evolution, revealing physiological transformations that have arisen in both colder and warmer climes, especially at higher levels of biological organization and phylogenetic diversity.
Fil: Coelho Faria, Samuel. Universidade de Sao Paulo; Brasil
Fil: Bianchini, Adalto. Universidade Federal Do Rio Grande.; Brasil
Fil: Machado Lauer, Mariana. Universidade Federal Do Rio Grande.; Brasil
Fil: Ribeiro Latorre Zimbardi, Ana Lúcia. Universidade de Sao Paulo; Brasil
Fil: Tapella, Federico. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Austral de Investigaciones Científicas; Argentina
Fil: Romero, Maria Carolina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Austral de Investigaciones Científicas; Argentina
Fil: Campbell McNamara, John. Universidade de Sao Paulo; Brasil
description Temperature is an important abiotic factor that drives the evolution of ectotherms owing to its pervasive effects at all levels of organization. Although a species’ thermal tolerance is environmentally driven within a spatial cline, it may be constrained over time due to differential phylogenetic inheritance. At the limits of thermal tolerance, hemolymph oxygen is reduced and lactate formation is increased due to mismatch between oxygen supply and demand; imbalance between enzyme flexibility/stability also impairs the ability to generate energy. Here, we characterized the effects of lower (LL50) and upper (UL50) critical thermal limits on selected descriptors of aerobic and anaerobic metabolism in 12 intertidal crab species distributed from northern Brazil (≈7.8°S) to southern Patagonia (≈53.2°S), considering their phylogeny. We tested for (i) functional trade-offs regarding aerobic and anaerobic metabolism and LDH kinetics in shaping thermal tolerance; (ii) influence of shared ancestry and thermal province on metabolic evolution; and (iii) presence of evolutionary convergences and adaptive peaks in the crab phylogeny. The tropical and subtropical species showed similar systemic and kinetic responses, both differing from the sub-Antarctic crabs. The lower UL50’s of the sub-Antarctic crabs may reflect mismatch between the evolution of aerobic and anaerobic metabolism since these crabs exhibit lower oxygen consumption but higher lactate formation than tropical and subtropical species also at their respective UL50’s. LDH activity increased with temperature increase, while KmPyr remained fairly constant; catalytic coefficient correlated negatively with thermal niche. Thermal tolerance may rely on a putative evolutionary trade-off between aerobic and anaerobic metabolism regarding energy supply, while temperature compensation of kinetic performance is driven by thermal habitat as revealed by the LDH affinity/efficiency equilibrium. The overall physiological evolution revealed two homoplastic adaptive peaks in the sub-Antarctic crabs with a further shift in the tropical/subtropical clade. The physiological traits at UL50 have evolved in a phylogenetic manner while all others were more plastic. Thus, shared inheritance and thermal environment have driven the crabs’ thermal tolerance and metabolic evolution, revealing physiological transformations that have arisen in both colder and warmer climes, especially at higher levels of biological organization and phylogenetic diversity.
publishDate 2020
dc.date.none.fl_str_mv 2020-04
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/141543
Coelho Faria, Samuel; Bianchini, Adalto; Machado Lauer, Mariana; Ribeiro Latorre Zimbardi, Ana Lúcia; Tapella, Federico; et al.; Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America; Frontiers Media S.A.; Frontiers in Physiology; 11; 4-2020; 1-15
1664-042X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/141543
identifier_str_mv Coelho Faria, Samuel; Bianchini, Adalto; Machado Lauer, Mariana; Ribeiro Latorre Zimbardi, Ana Lúcia; Tapella, Federico; et al.; Living on the Edge: Physiological and Kinetic Trade-Offs Shape Thermal Tolerance in Intertidal Crabs From Tropical to Sub-Antarctic South America; Frontiers Media S.A.; Frontiers in Physiology; 11; 4-2020; 1-15
1664-042X
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/article/10.3389/fphys.2020.00312/full
info:eu-repo/semantics/altIdentifier/doi/10.3389/fphys.2020.00312
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Frontiers Media S.A.
publisher.none.fl_str_mv Frontiers Media S.A.
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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