Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to fixed incompatibilities between species of Drosophila

Kristi L. Montooth, Colin D Meiklejohn, Dawn N. Abt, David M. Rand

Research output: Contribution to journalArticle

62 Citations (Scopus)

Abstract

Efficient mitochondrial function requires physical interactions between the proteins encoded by the mitochondrial and nuclear genomes. Coevolution between these genomes may result in the accumulation of incompatibilities between divergent lineages. We test whether mitochondrial-nuclear incompatibilities have accumulated within the Drosophila melanogaster species subgroup by combining divergent mitochondrial and nuclear lineages and quantifying the effects on relative fitness. Precise placement of nine mtDNAs from D. melanogaster, D. simulans, and D. mauritiana into two D. melanogaster nuclear genetic backgrounds reveals significant mitochondrial-nuclear epistasis affecting fitness in females. Combining the mitochondrial genomes with three different D. melanogaster X chromosomes reveals significant epistasis for male fitness between X-linked and mitochondrial variation. However, we find no evidence that the more than 500 fixed differences between the mitochondrial genomes of D. melanogaster and the D. simulans species complex are incompatible with the D. melanogaster nuclear genome. Rather, the interactions of largest effect occur between mitochondrial and nuclear polymorphisms that segregate within species of the D. melanogaster species subgroup. We propose that a low mitochondrial substitution rate, resulting from a low mutation rate and/or efficient purifying selection, precludes the accumulation of mitochondrial-nuclear incompatibilities among these Drosophila species.

Original languageEnglish (US)
Pages (from-to)3364-3379
Number of pages16
JournalEvolution
Volume64
Issue number12
DOIs
StatePublished - Dec 1 2010

Fingerprint

epistasis
incompatibility
Drosophila melanogaster
Drosophila
fitness
genome
Mitochondrial Genome
nuclear genome
coevolution
species complex
Genome
chromosome
mutation
polymorphism
substitution
X Chromosome
X chromosome
Mutation Rate
Nuclear Proteins
genetic background

Keywords

  • Epistasis
  • MtDNA evolution
  • Polymorphism
  • X chromosome

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Agricultural and Biological Sciences(all)

Cite this

Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to fixed incompatibilities between species of Drosophila. / Montooth, Kristi L.; Meiklejohn, Colin D; Abt, Dawn N.; Rand, David M.

In: Evolution, Vol. 64, No. 12, 01.12.2010, p. 3364-3379.

Research output: Contribution to journalArticle

@article{43c2f1d6debc4c5686b0b48b2942ef0b,
title = "Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to fixed incompatibilities between species of Drosophila",
abstract = "Efficient mitochondrial function requires physical interactions between the proteins encoded by the mitochondrial and nuclear genomes. Coevolution between these genomes may result in the accumulation of incompatibilities between divergent lineages. We test whether mitochondrial-nuclear incompatibilities have accumulated within the Drosophila melanogaster species subgroup by combining divergent mitochondrial and nuclear lineages and quantifying the effects on relative fitness. Precise placement of nine mtDNAs from D. melanogaster, D. simulans, and D. mauritiana into two D. melanogaster nuclear genetic backgrounds reveals significant mitochondrial-nuclear epistasis affecting fitness in females. Combining the mitochondrial genomes with three different D. melanogaster X chromosomes reveals significant epistasis for male fitness between X-linked and mitochondrial variation. However, we find no evidence that the more than 500 fixed differences between the mitochondrial genomes of D. melanogaster and the D. simulans species complex are incompatible with the D. melanogaster nuclear genome. Rather, the interactions of largest effect occur between mitochondrial and nuclear polymorphisms that segregate within species of the D. melanogaster species subgroup. We propose that a low mitochondrial substitution rate, resulting from a low mutation rate and/or efficient purifying selection, precludes the accumulation of mitochondrial-nuclear incompatibilities among these Drosophila species.",
keywords = "Epistasis, MtDNA evolution, Polymorphism, X chromosome",
author = "Montooth, {Kristi L.} and Meiklejohn, {Colin D} and Abt, {Dawn N.} and Rand, {David M.}",
year = "2010",
month = "12",
day = "1",
doi = "10.1111/j.1558-5646.2010.01077.x",
language = "English (US)",
volume = "64",
pages = "3364--3379",
journal = "Evolution; international journal of organic evolution",
issn = "0014-3820",
publisher = "Society for the Study of Evolution",
number = "12",

}

TY - JOUR

T1 - Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to fixed incompatibilities between species of Drosophila

AU - Montooth, Kristi L.

AU - Meiklejohn, Colin D

AU - Abt, Dawn N.

AU - Rand, David M.

PY - 2010/12/1

Y1 - 2010/12/1

N2 - Efficient mitochondrial function requires physical interactions between the proteins encoded by the mitochondrial and nuclear genomes. Coevolution between these genomes may result in the accumulation of incompatibilities between divergent lineages. We test whether mitochondrial-nuclear incompatibilities have accumulated within the Drosophila melanogaster species subgroup by combining divergent mitochondrial and nuclear lineages and quantifying the effects on relative fitness. Precise placement of nine mtDNAs from D. melanogaster, D. simulans, and D. mauritiana into two D. melanogaster nuclear genetic backgrounds reveals significant mitochondrial-nuclear epistasis affecting fitness in females. Combining the mitochondrial genomes with three different D. melanogaster X chromosomes reveals significant epistasis for male fitness between X-linked and mitochondrial variation. However, we find no evidence that the more than 500 fixed differences between the mitochondrial genomes of D. melanogaster and the D. simulans species complex are incompatible with the D. melanogaster nuclear genome. Rather, the interactions of largest effect occur between mitochondrial and nuclear polymorphisms that segregate within species of the D. melanogaster species subgroup. We propose that a low mitochondrial substitution rate, resulting from a low mutation rate and/or efficient purifying selection, precludes the accumulation of mitochondrial-nuclear incompatibilities among these Drosophila species.

AB - Efficient mitochondrial function requires physical interactions between the proteins encoded by the mitochondrial and nuclear genomes. Coevolution between these genomes may result in the accumulation of incompatibilities between divergent lineages. We test whether mitochondrial-nuclear incompatibilities have accumulated within the Drosophila melanogaster species subgroup by combining divergent mitochondrial and nuclear lineages and quantifying the effects on relative fitness. Precise placement of nine mtDNAs from D. melanogaster, D. simulans, and D. mauritiana into two D. melanogaster nuclear genetic backgrounds reveals significant mitochondrial-nuclear epistasis affecting fitness in females. Combining the mitochondrial genomes with three different D. melanogaster X chromosomes reveals significant epistasis for male fitness between X-linked and mitochondrial variation. However, we find no evidence that the more than 500 fixed differences between the mitochondrial genomes of D. melanogaster and the D. simulans species complex are incompatible with the D. melanogaster nuclear genome. Rather, the interactions of largest effect occur between mitochondrial and nuclear polymorphisms that segregate within species of the D. melanogaster species subgroup. We propose that a low mitochondrial substitution rate, resulting from a low mutation rate and/or efficient purifying selection, precludes the accumulation of mitochondrial-nuclear incompatibilities among these Drosophila species.

KW - Epistasis

KW - MtDNA evolution

KW - Polymorphism

KW - X chromosome

UR - http://www.scopus.com/inward/record.url?scp=78650025486&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=78650025486&partnerID=8YFLogxK

U2 - 10.1111/j.1558-5646.2010.01077.x

DO - 10.1111/j.1558-5646.2010.01077.x

M3 - Article

VL - 64

SP - 3364

EP - 3379

JO - Evolution; international journal of organic evolution

JF - Evolution; international journal of organic evolution

SN - 0014-3820

IS - 12

ER -