Effects of the Mitochondrial and Nuclear Genomes on Nonshivering Thermogenesis in a Wild Derived Rodent

Pierre Bize (Corresponding Author), Imogen Lowe, Mikko Lehto Hürlimann, Gerald Heckel

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

A key adaptation of mammals to their environment is their ability to maintain a constant high body temperature, even at rest, under a wide range of ambient temperatures. In cold climates, this is achieved by an adaptive production of endogenous heat, known as nonshivering thermogenesis (NST), in the brown adipose tissue (BAT). This organ, unique to mammals, contains a very high density of mitochondria, and BAT correct functioning relies on the correct functioning of its mitochondria. Mitochondria enclose proteins encoded both in the maternally inherited mitochondrial genome and in the biparentally inherited nuclear genome, and one overlooked hypothesis is that both genomes and their interaction may shape NST. By housing under standardised conditions wild-derived common voles (Microtus arvalis) from two distinct evolutionary lineages (Western and Central), we show that Western voles had greater NST than Central voles. By introgressing those two lineages over at least 9 generations, we then experimentally tested the influence of the nuclear and mitochondrial genomes on NST and related phenotypic traits. We found that between-lineage variation in NST and BAT size were significantly influenced by the mitochondrial and nuclear genomes, respectively, with the Western mitochondrial genotype being associated with higher NST and the Western nuclear genotype with a larger BAT. There were significant mito-nuclear interactions on whole animal body weight and resting metabolic rate. Hybrid voles were lighter and had higher resting metabolic rate. Overall, our findings turn new light on the influence of the mitochondrial and nuclear genomes on thermogenesis and building adaptation to the environment in mammals.
Original languageEnglish
Pages (from-to)532-543
Number of pages12
JournalIntegrative and Comparative Biology
Volume58
Issue number3
Early online date18 Jul 2018
DOIs
Publication statusPublished - Sep 2018

Fingerprint

heat production
nuclear genome
rodents
brown adipose tissue
Microtus arvalis
mitochondria
resting metabolic rate
mammals
genotype
cold zones
mitochondrial genome
body temperature
ambient temperature
heat
body weight
genome
voles
animals
proteins

Cite this

Effects of the Mitochondrial and Nuclear Genomes on Nonshivering Thermogenesis in a Wild Derived Rodent. / Bize, Pierre (Corresponding Author); Lowe, Imogen ; Hürlimann, Mikko Lehto ; Heckel, Gerald.

In: Integrative and Comparative Biology, Vol. 58, No. 3, 09.2018, p. 532-543.

Research output: Contribution to journalArticle

Bize, Pierre ; Lowe, Imogen ; Hürlimann, Mikko Lehto ; Heckel, Gerald. / Effects of the Mitochondrial and Nuclear Genomes on Nonshivering Thermogenesis in a Wild Derived Rodent. In: Integrative and Comparative Biology. 2018 ; Vol. 58, No. 3. pp. 532-543.
@article{3200091b19b34666af093c3e4dc64037,
title = "Effects of the Mitochondrial and Nuclear Genomes on Nonshivering Thermogenesis in a Wild Derived Rodent",
abstract = "A key adaptation of mammals to their environment is their ability to maintain a constant high body temperature, even at rest, under a wide range of ambient temperatures. In cold climates, this is achieved by an adaptive production of endogenous heat, known as nonshivering thermogenesis (NST), in the brown adipose tissue (BAT). This organ, unique to mammals, contains a very high density of mitochondria, and BAT correct functioning relies on the correct functioning of its mitochondria. Mitochondria enclose proteins encoded both in the maternally inherited mitochondrial genome and in the biparentally inherited nuclear genome, and one overlooked hypothesis is that both genomes and their interaction may shape NST. By housing under standardised conditions wild-derived common voles (Microtus arvalis) from two distinct evolutionary lineages (Western and Central), we show that Western voles had greater NST than Central voles. By introgressing those two lineages over at least 9 generations, we then experimentally tested the influence of the nuclear and mitochondrial genomes on NST and related phenotypic traits. We found that between-lineage variation in NST and BAT size were significantly influenced by the mitochondrial and nuclear genomes, respectively, with the Western mitochondrial genotype being associated with higher NST and the Western nuclear genotype with a larger BAT. There were significant mito-nuclear interactions on whole animal body weight and resting metabolic rate. Hybrid voles were lighter and had higher resting metabolic rate. Overall, our findings turn new light on the influence of the mitochondrial and nuclear genomes on thermogenesis and building adaptation to the environment in mammals.",
author = "Pierre Bize and Imogen Lowe and H{\"u}rlimann, {Mikko Lehto} and Gerald Heckel",
note = "This work was supported by the Swiss National Science Foundation [31003A_144203 to PB] and by the University of Aberdeen [start-up funding to PB]. PB thank the National Science Foundation (grant IOS-1738378 to W.R.H. and K.S.), SICB’s division of Comparative Physiology and Biochemistry and Comparative Endocrinology, and The Society of Experimental Biology for funding to attend the 2018 SICB conference.",
year = "2018",
month = "9",
doi = "10.1093/icb/icy072",
language = "English",
volume = "58",
pages = "532--543",
journal = "Integrative and Comparative Biology",
issn = "1540-7063",
publisher = "OXFORD UNIV PRESS INC",
number = "3",

}

TY - JOUR

T1 - Effects of the Mitochondrial and Nuclear Genomes on Nonshivering Thermogenesis in a Wild Derived Rodent

AU - Bize, Pierre

AU - Lowe, Imogen

AU - Hürlimann, Mikko Lehto

AU - Heckel, Gerald

N1 - This work was supported by the Swiss National Science Foundation [31003A_144203 to PB] and by the University of Aberdeen [start-up funding to PB]. PB thank the National Science Foundation (grant IOS-1738378 to W.R.H. and K.S.), SICB’s division of Comparative Physiology and Biochemistry and Comparative Endocrinology, and The Society of Experimental Biology for funding to attend the 2018 SICB conference.

PY - 2018/9

Y1 - 2018/9

N2 - A key adaptation of mammals to their environment is their ability to maintain a constant high body temperature, even at rest, under a wide range of ambient temperatures. In cold climates, this is achieved by an adaptive production of endogenous heat, known as nonshivering thermogenesis (NST), in the brown adipose tissue (BAT). This organ, unique to mammals, contains a very high density of mitochondria, and BAT correct functioning relies on the correct functioning of its mitochondria. Mitochondria enclose proteins encoded both in the maternally inherited mitochondrial genome and in the biparentally inherited nuclear genome, and one overlooked hypothesis is that both genomes and their interaction may shape NST. By housing under standardised conditions wild-derived common voles (Microtus arvalis) from two distinct evolutionary lineages (Western and Central), we show that Western voles had greater NST than Central voles. By introgressing those two lineages over at least 9 generations, we then experimentally tested the influence of the nuclear and mitochondrial genomes on NST and related phenotypic traits. We found that between-lineage variation in NST and BAT size were significantly influenced by the mitochondrial and nuclear genomes, respectively, with the Western mitochondrial genotype being associated with higher NST and the Western nuclear genotype with a larger BAT. There were significant mito-nuclear interactions on whole animal body weight and resting metabolic rate. Hybrid voles were lighter and had higher resting metabolic rate. Overall, our findings turn new light on the influence of the mitochondrial and nuclear genomes on thermogenesis and building adaptation to the environment in mammals.

AB - A key adaptation of mammals to their environment is their ability to maintain a constant high body temperature, even at rest, under a wide range of ambient temperatures. In cold climates, this is achieved by an adaptive production of endogenous heat, known as nonshivering thermogenesis (NST), in the brown adipose tissue (BAT). This organ, unique to mammals, contains a very high density of mitochondria, and BAT correct functioning relies on the correct functioning of its mitochondria. Mitochondria enclose proteins encoded both in the maternally inherited mitochondrial genome and in the biparentally inherited nuclear genome, and one overlooked hypothesis is that both genomes and their interaction may shape NST. By housing under standardised conditions wild-derived common voles (Microtus arvalis) from two distinct evolutionary lineages (Western and Central), we show that Western voles had greater NST than Central voles. By introgressing those two lineages over at least 9 generations, we then experimentally tested the influence of the nuclear and mitochondrial genomes on NST and related phenotypic traits. We found that between-lineage variation in NST and BAT size were significantly influenced by the mitochondrial and nuclear genomes, respectively, with the Western mitochondrial genotype being associated with higher NST and the Western nuclear genotype with a larger BAT. There were significant mito-nuclear interactions on whole animal body weight and resting metabolic rate. Hybrid voles were lighter and had higher resting metabolic rate. Overall, our findings turn new light on the influence of the mitochondrial and nuclear genomes on thermogenesis and building adaptation to the environment in mammals.

U2 - 10.1093/icb/icy072

DO - 10.1093/icb/icy072

M3 - Article

VL - 58

SP - 532

EP - 543

JO - Integrative and Comparative Biology

JF - Integrative and Comparative Biology

SN - 1540-7063

IS - 3

ER -