Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects

Author:

Prokkola Jenni M.123ORCID,Chew Kuan Kiat1,Anttila Katja4ORCID,Maamela Katja S.135,Yildiz Atakan6,Åsheim Eirik R.135ORCID,Primmer Craig R.15ORCID,Aykanat Tutku1ORCID

Affiliation:

1. Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, PO Box 56, 00014 Helsinki, Finland

2. Natural Resources Institute Finland (Luke), Paavo Havaksen tie 3, 90570 Oulu, Finland

3. Lammi Biological Station, University of Helsinki, Pääjärventie 320, 16900 Lammi, Finland

4. Department of Biology, University of Turku, 20014 Turku, Finland

5. Institute of Biotechnology, Helsinki Institute of Life Sciences (HiLIFE), University of Helsinki, 00014 Helsinki, Finland

6. Biotechnology Institute, Ankara University, Ankara 06135, Turkey

Abstract

Metabolic rates, including standard (SMR) and maximum (MMR) metabolic rate have often been linked with life-history strategies. Variation in context- and tissue-level metabolism underlying SMR and MMR may thus provide a physiological basis for life-history variation. This raises a hypothesis that tissue-specific metabolism covaries with whole-animal metabolic rates and is genetically linked to life history. In Atlantic salmon ( Salmo salar ), variation in two loci, vgll3 and six6 , affects life history via age-at-maturity as well as MMR. Here, using individuals with known SMR and MMR with different vgll3 and six6 genotype combinations, we measured proxies of mitochondrial density and anaerobic metabolism, i.e. maximal activities of the mitochondrial citrate synthase (CS) and lactate dehydrogenase (LDH) enzymes, in four tissues (heart, intestine, liver, white muscle) across low- and high-food regimes. We found enzymatic activities were related to metabolic rates, mainly SMR, in the intestine and heart. Individual loci were not associated with the enzymatic activities, but we found epistatic effects and genotype-by-environment interactions in CS activity in the heart and epistasis in LDH activity in the intestine. These effects suggest that mitochondrial density and anaerobic capacity in the heart and intestine may partly mediate variation in metabolic rates and life history via age-at-maturity. This article is part of the theme issue ‘The evolutionary significance of variation in metabolic rates’.

Funder

Natural Resources Institute Finland

Societas pro Fauna et Flora Fennica

Academy of Finland

H2020 European Research Council

Helsingin Yliopisto

Publisher

The Royal Society

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