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...

Full description

Bibliographic Details
Main Authors: Matthew J. Powers, Lucas D. Martz, Ronald S. Burton, Geoffrey E. Hill, Ryan J. Weaver
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8575244/?tool=EBI
_version_ 1818928338741231616
author Matthew J. Powers
Lucas D. Martz
Ronald S. Burton
Geoffrey E. Hill
Ryan J. Weaver
author_facet Matthew J. Powers
Lucas D. Martz
Ronald S. Burton
Geoffrey E. Hill
Ryan J. Weaver
author_sort Matthew J. Powers
collection DOAJ
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.
first_indexed 2024-12-20T03:27:20Z
format Article
id doaj.art-dd75ab0a4dab4daaaeefb2bdbcebe01d
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-20T03:27:20Z
publishDate 2021-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-dd75ab0a4dab4daaaeefb2bdbcebe01d2022-12-21T19:55:03ZengPublic Library of Science (PLoS)PLoS ONE1932-62032021-01-011611Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicusMatthew J. PowersLucas D. MartzRonald S. BurtonGeoffrey E. HillRyan J. WeaverThe 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.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8575244/?tool=EBI
spellingShingle Matthew J. Powers
Lucas D. Martz
Ronald S. Burton
Geoffrey E. Hill
Ryan J. Weaver
Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus
PLoS ONE
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
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8575244/?tool=EBI
work_keys_str_mv AT matthewjpowers evidenceforhybridbreakdowninproductionofredcarotenoidsinthemarineinvertebratetigriopuscalifornicus
AT lucasdmartz evidenceforhybridbreakdowninproductionofredcarotenoidsinthemarineinvertebratetigriopuscalifornicus
AT ronaldsburton evidenceforhybridbreakdowninproductionofredcarotenoidsinthemarineinvertebratetigriopuscalifornicus
AT geoffreyehill evidenceforhybridbreakdowninproductionofredcarotenoidsinthemarineinvertebratetigriopuscalifornicus
AT ryanjweaver evidenceforhybridbreakdowninproductionofredcarotenoidsinthemarineinvertebratetigriopuscalifornicus