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      Diet and mitonuclear haplotype interactions affect growth rate in a slime mould

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          Abstract

          Trait expression in metazoans is strongly influenced by the balance of macronutrients (i.e. protein, carbohydrate and fat) in the diet. At the same time, an individual's genetic background seems to regulate the magnitude of phenotypic response to a particular diet. It needs to be better understood whether interactions between diet, genetic background and trait expression are found in unicellular eukaryotes. A protist—the slime mould, Physarum polycephalum can choose diets based on protein‐to‐carbohydrate (P:C) content to support optimal growth rate. Yet, the role of genetic background (variation in the mitochondrial and nuclear DNAs) in mediating growth rate response to dietary P:C ratios in the slime mould is unknown. Here, we studied the effects of interactions between mitochondrial and nuclear DNA haplotypes and diet (i.e. G × G × E interactions) on the growth rate of P. polycephalum. A genetic panel of six distinct strains of P. polycephalum that differ in their mitochondrial and nuclear DNA haplotypes was used to measure growth rate across five diets that varied in their P:C ratio and total calories. We first determined the strains' growth rate (total biomass and surface area) when grown on a set menu with access to a particular diet. We then assessed whether the growth rate of strains increased on a buffet menu with access to all diets. Our findings show that the growth rate of P. polycephalum is generally higher on diets containing more carbohydrates than protein and that total calories negatively affect the growth rate. Three‐way interactions between mitochondrial, nuclear haplotypes and dietary P:C ratios affected the strains' surface area of growth but not biomass. Intriguingly, strains did not increase their surface area and biomass when they had access to all diets on the buffet menu. Our findings have broad implications for our understanding of the effect of mitonuclear interactions on trait expression across diverse eukaryotic lineages.

          Abstract

          Three‐way interactions between mitochondrial, nuclear haplotypes and dietary P:C ratios affected the slime mould's surface area of growth but not biomass. Our findings have broad implications for our understanding of the effect of mitonuclear interactions on trait expression across diverse eukaryotic lineages.

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          Most cited references67

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          lmerTest Package: Tests in Linear Mixed Effects Models

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            Fitting Linear Mixed-Effects Models Using lme4

            Maximum likelihood or restricted maximum likelihood (REML) estimates of the parameters in linear mixed-effects models can be determined using the lmer function in the lme4 package for R. As for most model-fitting functions in R, the model is described in an lmer call by a formula, in this case including both fixed- and random-effects terms. The formula and data together determine a numerical representation of the model from which the profiled deviance or the profiled REML criterion can be evaluated as a function of some of the model parameters. The appropriate criterion is optimized, using one of the constrained optimization functions in R, to provide the parameter estimates. We describe the structure of the model, the steps in evaluating the profiled deviance or REML criterion, and the structure of classes or types that represents such a model. Sufficient detail is included to allow specialization of these structures by users who wish to write functions to fit specialized linear mixed models, such as models incorporating pedigrees or smoothing splines, that are not easily expressible in the formula language used by lmer. Journal of Statistical Software, 67 (1) ISSN:1548-7660
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              Mitochondrial evolution.

              The serial endosymbiosis theory is a favored model for explaining the origin of mitochondria, a defining event in the evolution of eukaryotic cells. As usually described, this theory posits that mitochondria are the direct descendants of a bacterial endosymbiont that became established at an early stage in a nucleus-containing (but amitochondriate) host cell. Gene sequence data strongly support a monophyletic origin of the mitochondrion from a eubacterial ancestor shared with a subgroup of the alpha-Proteobacteria. However, recent studies of unicellular eukaryotes (protists), some of them little known, have provided insights that challenge the traditional serial endosymbiosis-based view of how the eukaryotic cell and its mitochondrion came to be. These data indicate that the mitochondrion arose in a common ancestor of all extant eukaryotes and raise the possibility that this organelle originated at essentially the same time as the nuclear component of the eukaryotic cell rather than in a separate, subsequent event.
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                Author and article information

                Contributors
                venkatesh.nagarajan.radha@gmail.com
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                04 September 2023
                September 2023
                : 13
                : 9 ( doiID: 10.1002/ece3.v13.9 )
                : e10508
                Affiliations
                [ 1 ] Behaviour, Ecology and Evolution Lab, School of Life and Environmental Sciences The University of Sydney Camperdown New South Wales Australia
                Author notes
                [*] [* ] Correspondence

                Venkatesh Nagarajan‐Radha, Postdoctoral Fellow (SERB‐India), St. John's College, Palayamkottai 627 002, Tamil Nadu, India.

                Email: venkatesh.nagarajan.radha@ 123456gmail.com

                Author information
                https://orcid.org/0000-0002-2386-4093
                https://orcid.org/0000-0002-9040-3756
                Article
                ECE310508 ECE-2023-04-00579.R1
                10.1002/ece3.10508
                10477482
                37674651
                87f443b0-84b3-49d0-803d-3974c6e03b42
                © 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 12 August 2023
                : 10 April 2023
                : 24 August 2023
                Page count
                Figures: 7, Tables: 3, Pages: 14, Words: 8503
                Funding
                Funded by: Australian Research Council , doi 10.13039/501100000923;
                Award ID: DP190101583
                Categories
                Evolutionary Ecology
                Functional Ecology
                Genetics
                Research Article
                Research Articles
                Custom metadata
                2.0
                September 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.3 mode:remove_FC converted:05.09.2023

                Evolutionary Biology
                decision‐making,diet choice,dietary macronutrient ratio,intergenomic interactions,mitonuclear ecology,physarum polycephalum,unicellular eukaryotes

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