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Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses

Vertebrate sex is typically determined genetically, but in many ectotherms sex can be determined by genes (genetic sex determination, GSD), temperature (temperature-dependent sex determination, TSD), or interactions between genes and temperature during development. TSD may involve GSD systems with e...

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Autores principales: Wild, Kristoffer H., Roe, John H., Schwanz, Lisa, Rodgers, Essie, Dissanayake, Duminda S. B., Georges, Arthur, Sarre, Stephen D., Noble, Daniel W. A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10357012/
https://www.ncbi.nlm.nih.gov/pubmed/37309620
http://dx.doi.org/10.1242/jeb.245657
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author Wild, Kristoffer H.
Roe, John H.
Schwanz, Lisa
Rodgers, Essie
Dissanayake, Duminda S. B.
Georges, Arthur
Sarre, Stephen D.
Noble, Daniel W. A.
author_facet Wild, Kristoffer H.
Roe, John H.
Schwanz, Lisa
Rodgers, Essie
Dissanayake, Duminda S. B.
Georges, Arthur
Sarre, Stephen D.
Noble, Daniel W. A.
author_sort Wild, Kristoffer H.
collection PubMed
description Vertebrate sex is typically determined genetically, but in many ectotherms sex can be determined by genes (genetic sex determination, GSD), temperature (temperature-dependent sex determination, TSD), or interactions between genes and temperature during development. TSD may involve GSD systems with either male or female heterogamety (XX/XY or ZZ/ZW) where temperature overrides chromosomal sex determination to cause a mismatch between genetic sex and phenotypic sex (sex reversal). In these temperature-sensitive lineages, phylogenetic investigations point to recurrent evolutionary shifts between genotypic and temperature-dependent sex determination. These evolutionary transitions in sex determination can occur rapidly if selection favours the reversed sex over the concordant phenotypic sex. To investigate the consequences of sex reversal on offspring phenotypes, we measured two energy-driven traits (metabolism and growth) and 6 month survival in two species of reptile with different patterns of temperature-induced sex reversal. Male sex reversal occurs in Bassiana duperreyi when chromosomal females (female XX) develop male phenotypes (male(SR) XX), while female sex reversal occurs in Pogona vitticeps when chromosomal males (male ZZ) develop female phenotypes (female(SR) ZZ). We show metabolism in male(SR) XX was like that of male XY; that is, reflective of phenotypic sex and lower than genotypic sex. In contrast, for Pogona vitticeps, female(SR) ZZ metabolism was intermediate between male ZZ and female ZW metabolic rate. For both species, our data indicate that differences in metabolism become more apparent as individuals become larger. Our findings provide some evidence for an energetic advantage from sex reversal in both species but do not exclude energetic processes as a constraint on the distribution of sex reversal in nature.
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spelling pubmed-103570122023-07-21 Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses Wild, Kristoffer H. Roe, John H. Schwanz, Lisa Rodgers, Essie Dissanayake, Duminda S. B. Georges, Arthur Sarre, Stephen D. Noble, Daniel W. A. J Exp Biol Research Article Vertebrate sex is typically determined genetically, but in many ectotherms sex can be determined by genes (genetic sex determination, GSD), temperature (temperature-dependent sex determination, TSD), or interactions between genes and temperature during development. TSD may involve GSD systems with either male or female heterogamety (XX/XY or ZZ/ZW) where temperature overrides chromosomal sex determination to cause a mismatch between genetic sex and phenotypic sex (sex reversal). In these temperature-sensitive lineages, phylogenetic investigations point to recurrent evolutionary shifts between genotypic and temperature-dependent sex determination. These evolutionary transitions in sex determination can occur rapidly if selection favours the reversed sex over the concordant phenotypic sex. To investigate the consequences of sex reversal on offspring phenotypes, we measured two energy-driven traits (metabolism and growth) and 6 month survival in two species of reptile with different patterns of temperature-induced sex reversal. Male sex reversal occurs in Bassiana duperreyi when chromosomal females (female XX) develop male phenotypes (male(SR) XX), while female sex reversal occurs in Pogona vitticeps when chromosomal males (male ZZ) develop female phenotypes (female(SR) ZZ). We show metabolism in male(SR) XX was like that of male XY; that is, reflective of phenotypic sex and lower than genotypic sex. In contrast, for Pogona vitticeps, female(SR) ZZ metabolism was intermediate between male ZZ and female ZW metabolic rate. For both species, our data indicate that differences in metabolism become more apparent as individuals become larger. Our findings provide some evidence for an energetic advantage from sex reversal in both species but do not exclude energetic processes as a constraint on the distribution of sex reversal in nature. The Company of Biologists Ltd 2023-07-14 /pmc/articles/PMC10357012/ /pubmed/37309620 http://dx.doi.org/10.1242/jeb.245657 Text en © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0 (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Wild, Kristoffer H.
Roe, John H.
Schwanz, Lisa
Rodgers, Essie
Dissanayake, Duminda S. B.
Georges, Arthur
Sarre, Stephen D.
Noble, Daniel W. A.
Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses
title Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses
title_full Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses
title_fullStr Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses
title_full_unstemmed Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses
title_short Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses
title_sort metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10357012/
https://www.ncbi.nlm.nih.gov/pubmed/37309620
http://dx.doi.org/10.1242/jeb.245657
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