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Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus

The marine copepod, Tigriopus californicus, produces the red carotenoid pigment astaxanthin from yellow dietary precursors. This ‘bioconversion’ of yellow carotenoids to red is hypothesized to be linked to individual condition, possibly through shared metabolic pathways with mitochondrial oxidative...

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Autores principales: Powers, Matthew J., Martz, Lucas D., Burton, Ronald S., Hill, Geoffrey E., Weaver, Ryan J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8575244/
https://www.ncbi.nlm.nih.gov/pubmed/34748608
http://dx.doi.org/10.1371/journal.pone.0259371
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author Powers, Matthew J.
Martz, Lucas D.
Burton, Ronald S.
Hill, Geoffrey E.
Weaver, Ryan J.
author_facet Powers, Matthew J.
Martz, Lucas D.
Burton, Ronald S.
Hill, Geoffrey E.
Weaver, Ryan J.
author_sort Powers, Matthew J.
collection PubMed
description The marine copepod, Tigriopus californicus, produces the red carotenoid pigment astaxanthin from yellow dietary precursors. This ‘bioconversion’ of yellow carotenoids to red is hypothesized to be linked to individual condition, possibly through shared metabolic pathways with mitochondrial oxidative phosphorylation. Experimental inter-population crosses of lab-reared T. californicus typically produces low-fitness hybrids is due in large part to the disruption of coadapted sets nuclear and mitochondrial genes within the parental populations. These hybrid incompatibilities can increase variability in life history traits and energy production among hybrid lines. Here, we tested if production of astaxanthin was compromised in hybrid copepods and if it was linked to mitochondrial metabolism and offspring development. We observed no clear mitonuclear dysfunction in hybrids fed a limited, carotenoid-deficient diet of nutritional yeast. However, when yellow carotenoids were restored to their diet, hybrid lines produced less astaxanthin than parental lines. We observed that lines fed a yeast diet produced less ATP and had slower offspring development compared to lines fed a more complete diet of algae, suggesting the yeast-only diet may have obscured effects of mitonuclear dysfunction. Astaxanthin production was not significantly associated with development among lines fed a yeast diet but was negatively related to development in early generation hybrids fed an algal diet. In lines fed yeast, astaxanthin was negatively related to ATP synthesis, but in lines fed algae, the relationship was reversed. Although the effects of the yeast diet may have obscured evidence of hybrid dysfunction, these results suggest that astaxanthin bioconversion may still be related to mitochondrial performance and reproductive success.
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spelling pubmed-85752442021-11-09 Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus Powers, Matthew J. Martz, Lucas D. Burton, Ronald S. Hill, Geoffrey E. Weaver, Ryan J. PLoS One Research Article The marine copepod, Tigriopus californicus, produces the red carotenoid pigment astaxanthin from yellow dietary precursors. This ‘bioconversion’ of yellow carotenoids to red is hypothesized to be linked to individual condition, possibly through shared metabolic pathways with mitochondrial oxidative phosphorylation. Experimental inter-population crosses of lab-reared T. californicus typically produces low-fitness hybrids is due in large part to the disruption of coadapted sets nuclear and mitochondrial genes within the parental populations. These hybrid incompatibilities can increase variability in life history traits and energy production among hybrid lines. Here, we tested if production of astaxanthin was compromised in hybrid copepods and if it was linked to mitochondrial metabolism and offspring development. We observed no clear mitonuclear dysfunction in hybrids fed a limited, carotenoid-deficient diet of nutritional yeast. However, when yellow carotenoids were restored to their diet, hybrid lines produced less astaxanthin than parental lines. We observed that lines fed a yeast diet produced less ATP and had slower offspring development compared to lines fed a more complete diet of algae, suggesting the yeast-only diet may have obscured effects of mitonuclear dysfunction. Astaxanthin production was not significantly associated with development among lines fed a yeast diet but was negatively related to development in early generation hybrids fed an algal diet. In lines fed yeast, astaxanthin was negatively related to ATP synthesis, but in lines fed algae, the relationship was reversed. Although the effects of the yeast diet may have obscured evidence of hybrid dysfunction, these results suggest that astaxanthin bioconversion may still be related to mitochondrial performance and reproductive success. Public Library of Science 2021-11-08 /pmc/articles/PMC8575244/ /pubmed/34748608 http://dx.doi.org/10.1371/journal.pone.0259371 Text en © 2021 Powers et al 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/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Powers, Matthew J.
Martz, Lucas D.
Burton, Ronald S.
Hill, Geoffrey E.
Weaver, Ryan J.
Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus
title Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus
title_full Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus
title_fullStr Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus
title_full_unstemmed Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus
title_short Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus
title_sort evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate tigriopus californicus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8575244/
https://www.ncbi.nlm.nih.gov/pubmed/34748608
http://dx.doi.org/10.1371/journal.pone.0259371
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