Interactions between cytoplasmic and nuclear genomes confer sex-specific effects on lifespan in Drosophila melanogaster.
Wolbachia
Mother’s Curse
mito-nuclear
mitochondria
mtDNA
Journal
Journal of evolutionary biology
ISSN: 1420-9101
Titre abrégé: J Evol Biol
Pays: Switzerland
ID NLM: 8809954
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
14
11
2019
revised:
04
02
2020
accepted:
06
02
2020
pubmed:
14
2
2020
medline:
3
7
2021
entrez:
14
2
2020
Statut:
ppublish
Résumé
Genetic variation outside of the cell nucleus can affect the phenotype. The cytoplasm is home to the mitochondria, and in arthropods often hosts intracellular bacteria such as Wolbachia. Although numerous studies have implicated epistatic interactions between cytoplasmic and nuclear genetic variation as mediators of phenotypic expression, two questions remain. Firstly, it remains unclear whether outcomes of cyto-nuclear interactions will manifest differently across the sexes, as might be predicted given that cytoplasmic genomes are screened by natural selection only through females as a consequence of their maternal inheritance. Secondly, the relative contribution of mitochondrial genetic variation to other cytoplasmic sources of variation, such as Wolbachia infection, in shaping phenotypic outcomes of cyto-nuclear interactions remains unknown. Here, we address these questions, creating a fully crossed set of replicated cyto-nuclear populations derived from three geographically distinct populations of Drosophila melanogaster, measuring the lifespan of males and females from each population. We observed that cyto-nuclear interactions shape lifespan and that the outcomes of these interactions differ across the sexes. Yet, we found no evidence that placing the cytoplasms from one population alongside the nuclear background of others (generating putative cyto-nuclear mismatches) leads to decreased lifespan in either sex. Although it was difficult to partition mitochondrial from Wolbachia effects, our results suggest at least some of the cytoplasmic genotypic contribution to lifespan was directly mediated by an effect of sequence variation in the mtDNA. Future work should explore the degree to which cyto-nuclear interactions result in sex differences in the expression of other components of organismal life history.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
694-713Informations de copyright
© 2020 European Society For Evolutionary Biology. Journal of Evolutionary Biology © 2020 European Society For Evolutionary Biology.
Références
Adineh, S., & Ross, J. (2019). The ebb and flow of heteroplasmy during intra-species hybridization in Caenorhabditis briggsae. bioRxiv, 623207. https://doi.org/10.1101/623207
Ågren, J. A., Munasinghe, M., & Clark, A. G. (2019). Sexual conflict through mother’s curse and father’s curse. Theoretical Population Biology, 129, 9-17. https://doi.org/10.1016/j.tpb.2018.12.007
Alexandrov, I. D., Alexandrova, M. V., Goryacheva, I. I., Rochina, N. V., Shaikevich, E. V., & Zakharov, I. A. (2007). Removing endosymbiotic Wolbachia specifically decreases lifespan of females and competitiveness in a laboratory strain of Drosophila melanogaster. Russian Journal of Genetics, 43(10), 1147-1152. https://doi.org/10.1134/S1022795407100080
Arnqvist, G., Dowling, D. K., Eady, P., Gay, L., Tregenza, T., Tuda, M., & Hosken, D. J. (2010). Genetic architecture of metabolic rate: Environment specific epistasis between mitochondrial and nuclear genes in an insect. Evolution, 64(12), 3354-3363. https://doi.org/10.1111/j.1558-5646.2010.01135.x
Avise, J. C. (1986). Mitochondrial DNA and the evolutionary genetics of higher animals. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 312(1154), 325-342. https://doi.org/10.1098/rstb.1986.0011
Aw, W. C., Garvin, M. R., Melvin, R. G., & Ballard, J. W. O. (2017). Sex-specific influences of mtDNA mitotype and diet on mitochondrial functions and physiological traits in Drosophila melanogaster. PLoS ONE, 12(11), e0187554. https://doi.org/10.1371/journal.pone.0187554
Ballard, J. W., & Kreitman, M. (1994). Unraveling selection in the mitochondrial genome of Drosophila. Genetics, 138(3), 757-772.
Ballard, J. W. O., & Kreitman, M. (1995). Is mitochondrial DNA a strictly neutral marker? Trends in Ecology and Evolution, 10(12), 485-488. https://doi.org/10.1016/S0169-5347(00)89195-8
Ballard, J. W. O., & Melvin, R. G. (2010). Linking the mitochondrial genotype to the organismal phenotype. Molecular Ecology, 19(8), 1523-1539. https://doi.org/10.1111/j.1365-294X.2010.04594.x
Ballard, J. W. O., & Pichaud, N. (2014). Mitochondrial DNA: More than an evolutionary bystander. Functional Ecology, 28(1), 218-231. https://doi.org/10.1111/1365-2435.12177
Ballard, J. W. O., & Rand, D. M. (2005). The population biology of mitochondrial DNA and its phylogenetic implications. Annual Review of Ecology, Evolution, and Systematics, 36, 621-642. https://doi.org/10.1146/annurev.ecolsys.36.091704.175513
Ballard, J. W. O., & Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology, 13(4), 729-744. https://doi.org/10.1046/j.1365-294X.2003.02063.x
Barreto, F. S., & Burton, R. S. (2013). Elevated oxidative damage is correlated with reduced fitness in interpopulation hybrids of a marine copepod. Proceedings of the Royal Society B: Biological Sciences, 280(1767), 20131521. https://doi.org/10.1098/rspb.2013.1521
Barreto, F. S., Watson, E. T., Lima, T. G., Willett, C. S., Edmands, S., Li, W., & Burton, R. S. (2018). Genomic signatures of mitonuclear coevolution across populations of Tigriopus californicus. Nature Ecology and Evolution, 2(8), 1250-1257. https://doi.org/10.1038/s41559-018-0588-1
Barrientos, A., Kenyon, L., & Moraes, C. T. (1998). Human xenomitochondrial cybrids cellular models of mitochondrial complex I deficiency. Journal of Biological Chemistry, 273(23), 14210-14217. https://doi.org/10.1074/jbc.273.23.14210
Bar-Yaacov, D., Blumberg, A., & Mishmar, D. (2012). Mitochondrial-nuclear co-evolution and its effects on OXPHOS activity and regulation. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 1819(9-10), 1107-1111. https://doi.org/10.1016/j.bbagrm.2011.10.008
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2014). Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823.
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57(1), 289-300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Blier, P. U., Dufresne, F., & Burton, R. S. (2001). Natural selection and the evolution of mtDNA-encoded peptides: Evidence for intergenomic co-adaptation. Trends in Genetics, 17(7), 400-406. https://doi.org/10.1016/S0168-9525(01)02338-1
Breeuwer, J. A., & Werren, J. H. (1995). Hybrid breakdown between two haplodiploid species: The role of nuclear and cytoplasmic genes. Evolution, 49(4), 705-717. https://doi.org/10.1111/j.1558-5646.1995.tb02307.x
Burton, R. S., & Barreto, F. S. (2012). A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Molecular Ecology, 21(20), 4942-4957. https://doi.org/10.1111/mec.12006
Burton, R. S., Pereira, R. J., & Barreto, F. S. (2013). Cytonuclear genomic interactions and hybrid breakdown. Annual Review of Ecology, Evolution, and Systematics, 44, 281-302. https://doi.org/10.1146/annurev-ecolsys-110512-135758
Camus, M. F., Clancy, D. J., & Dowling, D. K. (2012). Mitochondria, maternal inheritance, and male aging. Current Biology, 22(18), 1717-1721. https://doi.org/10.1016/j.cub.2012.07.018
Camus, M. F., & Dowling, D. K. (2018). Mitochondrial genetic effects on reproductive success: Signatures of positive intrasexual, but negative intersexual pleiotropy. Proceedings of the Royal Society B: Biological Sciences, 285(1879), 20180187. https://doi.org/10.1098/rspb.2018.0187
Camus, M. F., Wolff, J. N., Sgro, C. M., & Dowling, D. K. (2017). Experimental support that natural selection has shaped the latitudinal distribution of mitochondrial haplotypes in Australian Drosophila melanogaster. Molecular Biology and Evolution, 34(10), 2600-2612. https://doi.org/10.1093/molbev/msx184
Capobianco, F. III, Nandkumar, S., & Parker, J. D. (2018). Wolbachia affects survival to different oxidative stressors dependent upon the genetic background in Drosophila melanogaster. Physiological Entomology, 43(3), 239-244. https://doi.org/10.1111/phen.12252
Cazares-Navarro, E., & Ross, J. A. (2019). Temperature-dependent mitochondrial-nuclear epistasis. Micropublication Biology. https://doi.org/10.17912/micropub.biology.000147
Chang, C. C., Rodriguez, J., & Ross, J. (2016). Mitochondrial-nuclear epistasis impacts fitness and mitochondrial physiology of interpopulation Caenorhabditis briggsae hybrids. G3: Genes, Genomes, Genetics, 6(1), 209-219. https://doi.org/10.1534/g3.115.022970
Chou, J. Y., Hung, Y. S., Lin, K. H., Lee, H. Y., & Leu, J. Y. (2010). Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biology, 8(7), e1000432. https://doi.org/10.1371/journal.pbio.1000432
Chou, J. Y., & Leu, J. Y. (2010). Speciation through cytonuclear incompatibility: Insights from yeast and implications for higher eukaryotes. BioEssays, 32(5), 401-411. https://doi.org/10.1002/bies.200900162
Clancy, D. J. (2008). Variation in mitochondrial genotype has substantial lifespan effects which may be modulated by nuclear background. Aging Cell, 7(6), 795-804. https://doi.org/10.1111/j.1474-9726.2008.00428.x
Clancy, D. J., Hime, G. R., & Shirras, A. D. (2011). Cytoplasmic male sterility in Drosophila melanogaster associated with a mitochondrial CYTB variant. Heredity, 107(4), 374. https://doi.org/10.1038/hdy.2011.12
Connallon, T., Camus, M. F., Morrow, E. H., & Dowling, D. K. (2018). Coadaptation of mitochondrial and nuclear genes, and the cost of mother's curse. Proceedings of the Royal Society B: Biological Sciences, 285(1871), 20172257. https://doi.org/10.1098/rspb.2017.2257
Cooper, B. S., Burrus, C. R., Ji, C., Hahn, M. W., & Montooth, K. L. (2015). Similar efficacies of selection shape mitochondrial and nuclear genes in both Drosophila melanogaster and Homo sapiens. G3: Genes, Genomes, Genetics, 5(10), 2165-2176. https://doi.org/10.1534/g3.114.016493
Correa, C. C., & Ballard, J. W. O. (2016). Wolbachia associations with insects: Winning or losing against a master manipulator. Frontiers in Ecology and Evolution, 3, 153. https://doi.org/10.3389/fevo.2015.00153
Cosmides, L. M., & Tooby, J. (1981). Cytoplasmic inheritance and intragenomic conflict. Journal of Theoretical Biology, 89(1), 83-129. https://doi.org/10.1016/0022-5193(81)90181-8
Dobler, R., Dowling, D. K., Morrow, E. H., & Reinhardt, K. (2018). A systematic review and meta-analysis reveals pervasive effects of germline mitochondrial replacement on components of health. Human Reproduction Update, 24(5), 519-534. https://doi.org/10.1093/humupd/dmy018
Dobler, R., Rogell, B., Budar, F., & Dowling, D. K. (2014). A meta-analysis of the strength and nature of cytoplasmic genetic effects. Journal of Evolutionary Biology, 27(10), 2021-2034. https://doi.org/10.1111/jeb.12468
Dong, W., Dobler, R., Dowling, D. K., & Moussian, B. (2019). The cuticle inward barrier in Drosophila melanogaster is shaped by mitochondrial and nuclear genotypes and a sex-specific effect of diet. PeerJ, 7, e7802. https://doi.org/10.7717/peerj.7802
Đorđević, M., Savković, U., Lazarević, J., Tucić, N., & Stojković, B. (2015). Intergenomic interactions in hybrids between short-lived and long-lived lines of a seed beetle: Analyses of life history traits. Evolutionary Biology, 42(4), 461-472. https://doi.org/10.1007/s11692-015-9340-9
Đorđević, M., Stojković, B., Savković, U., Immonen, E., Tucić, N., Lazarević, J., & Arnqvist, G. (2017). Sex-specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics, ageing, and life history in seed beetles. Evolution, 71(2), 274-288. https://doi.org/10.1111/evo.13109
Dowling, D. K. (2014). Evolutionary perspectives on the links between mitochondrial genotype and disease phenotype. Biochimica et Biophysica Acta (BBA) - General Subjects, 1840(4), 1393-1403. https://doi.org/10.1016/j.bbagen.2013.11.013
Dowling, D. K., Abiega, K. C., & Arnqvist, G. (2007). Temperature-specific outcomes of cytoplasmic-nuclear interactions on egg-to-adult development time in seed beetles. Evolution, 61(1), 194-201. https://doi.org/10.1111/j.1558-5646.2007.00016.x
Dowling, D. K., & Adrian, R. E. (2019). Challenges and prospects for testing the Mother’s Curse hypothesis. Integrative and Comparative Biology, 59(4), 875-889. https://doi.org/10.1093/icb/icz110
Dowling, D. K., Friberg, U., Hailer, F., & Arnqvist, G. (2007). Intergenomic epistasis for fitness: Within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster. Genetics, 175(1), 235-244. https://doi.org/10.1534/genetics.105.052050
Dowling, D. K., Friberg, U., & Lindell, J. (2008). Evolutionary implications of non-neutral mitochondrial genetic variation. Trends in Ecology and Evolution, 23(10), 546-554. https://doi.org/10.1016/j.tree.2008.05.011
Dowling, D. K., Meerupati, T., & Arnqvist, G. (2010). Cytonuclear interactions and the economics of mating in seed beetles. The American Naturalist, 176(2), 131-140. https://doi.org/10.1086/653671
Drummond, E., Short, E., & Clancy, D. (2019). Mitonuclear gene X environment effects on lifespan and health: How common, how big? Mitochondrion, 49, 12-18. https://doi.org/10.1016/j.mito.2019.06.009
Ellison, C. K., & Burton, R. S. (2008). Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution, 62(3), 631-638. https://doi.org/10.1111/j.1558-5646.2007.00305.x
Ellison, C. K., Niehuis, O., & Gadau, J. (2008). Hybrid breakdown and mitochondrial dysfunction in hybrids of Nasonia parasitoid wasps. Journal of Evolutionary Biology, 21(6), 1844-1851. https://doi.org/10.1111/j.1420-9101.2008.01608.x
Fox, J., Weisberg, S., Adler, D., Bates, D., Baud-Bovy, G., Ellison, S., … Heiberger, R. (2012). Package ‘car’. Vienna, Austria: R Foundation for Statistical Computing.
Frank, S. A., & Hurst, L. D. (1996). Mitochondria and male disease. Nature, 383(6597), 224. https://doi.org/10.1038/383224a0
Friberg, U., & Dowling, D. K. (2008). No evidence of mitochondrial genetic variation for sperm competition within a population of Drosophila melanogaster. Journal of Evolutionary Biology, 21(6), 1798-1807. https://doi.org/10.1111/j.1420-9101.2008.01581.x
Fry, A. J., Palmer, M. R., & Rand, D. M. (2004). Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity, 93(4), 379. https://doi.org/10.1038/sj.hdy.6800514
Fry, A. J., & Rand, D. M. (2002). Wolbachia interactions that determine Drosophila melanogaster survival. Evolution, 56(10), 1976-1981. https://doi.org/10.1111/j.0014-3820.2002.tb00123.x
Gemmell, N. J., Metcalf, V. J., & Allendorf, F. W. (2004). Mother's curse: The effect of mtDNA on individual fitness and population viability. Trends in Ecology and Evolution, 19(5), 238-244. https://doi.org/10.1016/j.tree.2004.02.002
Gershoni, M., Templeton, A. R., & Mishmar, D. (2009). Mitochondrial bioenergetics as a major motive force of speciation. BioEssays, 31(6), 642-650. https://doi.org/10.1002/bies.200800139
Grunau, C., Voigt, S., Dobler, R., Dowling, D., & Reinhardt, K. (2018). The cytoplasm affects the epigenome in Drosophila melanogaster. Epigenomes, 2(3), 17. https://doi.org/10.3390/epigenomes2030017
Haddad, R., Meter, B., & Ross, J. A. (2018). The genetic architecture of intra-species hybrid mito-nuclear epistasis. Frontiers in Genetics, 9, 481. https://doi.org/10.3389/fgene.2018.00481
Havird, J. C., Forsythe, E. S., Williams, A. M., Werren, J. H., Dowling, D. K., & Sloan, D. B. (2019). Selfish mitonuclear conflict. Current Biology, 29(11), R496-R511. https://doi.org/10.1016/j.cub.2019.03.020
Havird, J. C., Hall, M. D., & Dowling, D. K. (2015). The evolution of sex: A new hypothesis based on mitochondrial mutational erosion: Mitochondrial mutational erosion. BioEssays, 37(9), 951-958. https://doi.org/10.1002/bies.201500057
Healy, T. M., & Burton, R. S. (2019). Mitochondrial DNA has strong selective effects across the nuclear genome. bioRxiv, 643056. https://doi.org/10.1101/643056
Hill, G. E. (2015). Mitonuclear ecology. Molecular Biology and Evolution, 32(8), 1917-1927. https://doi.org/10.1093/molbev/msv104
Hill, G. E. (2016). Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap. Ecology and Evolution, 6(16), 5831-5842. https://doi.org/10.1002/ece3.2338
Hill, G. E. (2017). The mitonuclear compatibility species concept. The Auk: Ornithological Advances, 134(2), 393-409. https://doi.org/10.1642/AUK-16-201.1
Hill, G. E., Havird, J. C., Sloan, D. B., Burton, R. S., Greening, C., & Dowling, D. K. (2019). Assessing the fitness consequences of mitonuclear interactions in natural populations. Biological Reviews, 94(3), 1089-1104. https://doi.org/10.1111/brv.12493
Hill, G. E., & Johnson, J. D. (2013). The mitonuclear compatibility hypothesis of sexual selection. Proceedings of the Royal Society B: Biological Sciences, 280(1768), 20131314. https://doi.org/10.1098/rspb.2013.1314
Hoekstra, L. A., Julick, C. R., Mika, K. M., & Montooth, K. L. (2018). Energy demand and the context-dependent effects of genetic interactions underlying metabolism. Evolution Letters, 2(2), 102-113. https://doi.org/10.1002/evl3.47
Hoekstra, L. A., Siddiq, M. A., & Montooth, K. L. (2013). Pleiotropic effects of a mitochondrial-nuclear incompatibility depend upon the accelerating effect of temperature in Drosophila. Genetics, 195(3), 1129-1139. https://doi.org/10.1534/genetics.113.154914
Holmbeck, M. A., Donner, J. R., Villa-Cuesta, E., & Rand, D. M. (2015). A Drosophila model for mito-nuclear diseases generated by an incompatible interaction between tRNA and tRNA synthetase. Disease Models and Mechanisms, 8(8), 843-854. https://doi.org/10.1242/dmm.019323
Horan, M. P., Gemmell, N. J., & Wolff, J. N. (2013). From evolutionary bystander to master manipulator: The emerging roles for the mitochondrial genome as a modulator of nuclear gene expression. European Journal of Human Genetics, 21(12), 1335. https://doi.org/10.1038/ejhg.2013.75
Hudson, R. R., Slatkin, M., & Maddison, W. P. (1992). Estimation of levels of gene flow from DNA sequence data. Genetics, 132(2), 583-589.
Immonen, E., Collet, M., Goenaga, J., & Arnqvist, G. (2016). Direct and indirect genetic effects of sex-specific mitonuclear epistasis on reproductive ageing. Heredity, 116(3), 338. https://doi.org/10.1038/hdy.2015.112
Innocenti, P., Morrow, E. H., & Dowling, D. K. (2011). Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science, 332(6031), 845-848. https://doi.org/10.1126/science.1201157
James, A. C., & Ballard, J. W. O. (2003). Mitochondrial genotype affects fitness in Drosophila simulans. Genetics, 164(1), 187-194.
James, J. E., Piganeau, G., & Eyre-Walker, A. (2016). The rate of adaptive evolution in animal mitochondria. Molecular Ecology, 25(1), 67-78. https://doi.org/10.1111/mec.13475
Jelić, M., Arnqvist, G., Novičić, Z. K., Kenig, B., Tanasković, M., Anđelković, M., & Stamenković-Radak, M. (2015). Sex-specific effects of sympatric mitonuclear variation on fitness in Drosophila subobscura. BMC Evolutionary Biology, 15(1), 135. https://doi.org/10.1186/s12862-015-0421-2
Jhuang, H. Y., Lee, H. Y., & Leu, J. Y. (2017). Mitochondrial-nuclear co-evolution leads to hybrid incompatibility through pentatricopeptide repeat proteins. EMBO Reports, 18(1), 87-101. https://doi.org/10.15252/embr.201643311
Kenyon, L., & Moraes, C. T. (1997). Expanding the functional human mitochondrial DNA database by the establishment of primate xenomitochondrial cybrids. Proceedings of the National Academy of Sciences of the United States of America, 94(17), 9131-9135. https://doi.org/10.1073/pnas.94.17.9131
Kimber, C. M., & Chippindale, A. K. (2013). Mutation, condition, and the maintenance of extended lifespan in Drosophila. Current Biology, 23(22), 2283-2287. https://doi.org/10.1016/j.cub.2013.09.049
Kofler, R., Pandey, R. V., & Schlötterer, C. (2011). PoPoolation2: Identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics, 27(24), 3435-3436. https://doi.org/10.1093/bioinformatics/btr589
Lajbner, Z., Pnini, R., Camus, M. F., Miller, J., & Dowling, D. K. (2018). Experimental evidence that thermal selection shapes mitochondrial genome evolution. Scientific Reports, 8(1), 9500. https://doi.org/10.1038/s41598-018-27805-3
Lane, N. (2011). Mitonuclear match: Optimizing fitness and fertility over generations drives ageing within generations. BioEssays, 33(11), 860-869. https://doi.org/10.1002/bies.201100051
Latorre-Pellicer, A., Moreno-Loshuertos, R., Lechuga-Vieco, A. V., Sánchez-Cabo, F., Torroja, C., Acín-Pérez, R., … Enríquez, J. A. (2016). Mitochondrial and nuclear DNA matching shapes metabolism and healthy ageing. Nature, 535(7613), 561. https://doi.org/10.1038/nature18618
Lee, H. Y., Chou, J. Y., Cheong, L., Chang, N. H., Yang, S. Y., & Leu, J. Y. (2008). Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell, 135(6), 1065-1073. https://doi.org/10.1016/j.cell.2008.10.047
Levin, L., Blumberg, A., Barshad, G., & Mishmar, D. (2014). Mito-nuclear co-evolution: The positive and negative sides of functional ancient mutations. Frontiers in Genetics, 5, 448. https://doi.org/10.3389/fgene.2014.00448
Li, H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint arXiv:1303.3997.
Lima, T. G., Burton, R. S., & Willett, C. S. (2019). Genomic scans reveal multiple mito-nuclear incompatibilities in population crosses of the copepod Tigriopus californicus. Evolution, 73(3), 609-620. https://doi.org/10.1111/evo.13690
Lunter, G., & Goodson, M. (2011). Stampy: A statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Research, 21(6), 936-939. https://doi.org/10.1101/gr.111120.110
Ma, H., Marti Gutierrez, N., Morey, R., Van Dyken, C., Kang, E., Hayama, T., … Mitalipov, S. (2016). Incompatibility between nuclear and mitochondrial genomes contributes to an interspecies reproductive barrier. Cell Metabolism, 24(2), 283-294. https://doi.org/10.1016/j.cmet.2016.06.012
MacLellan, K., Whitlock, M. C., & Rundle, H. D. (2009). Sexual selection against deleterious mutations via variable male search success. Biology Letters, 5(6), 795-797. https://doi.org/10.1098/rsbl.2009.0475
Maistrenko, O. M., Serga, S. V., Vaiserman, A. M., & Kozeretska, I. A. (2016). Longevity-modulating effects of symbiosis: Insights from Drosophila-Wolbachia interaction. Biogerontology, 17(5-6), 785-803. https://doi.org/10.1007/s10522-016-9653-9
Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., … Visscher, P. M. (2009). Finding the missing heritability of complex diseases. Nature, 461(7265), 747. https://doi.org/10.1038/nature08494
McKenzie, J. L., Chung, D. J., Healy, T. M., Brennan, R. S., Bryant, H. J., Whitehead, A., & Schulte, P. M. (2019). Mitochondrial ecophysiology: Assessing the evolutionary forces that shape mitochondrial variation. Integrative and Comparative Biology, 59(4), 925-937. https://doi.org/10.1093/molbev/msg132
McKenzie, M., Chiotis, M., Pinkert, C. A., & Trounce, I. A. (2003). Functional respiratory chain analyses in murid xenomitochondrial cybrids expose coevolutionary constraints of cytochrome b and nuclear subunits of complex III. Molecular Biology and Evolution, 20(7), 1117-1124. https://doi.org/10.1093/molbev/msg132
McKenzie, M., Lazarou, M., Thorburn, D. R., & Ryan, M. T. (2007). Analysis of mitochondrial subunit assembly into respiratory chain complexes using Blue Native polyacrylamide gel electrophoresis. Analytical Biochemistry, 364(2), 128-137. https://doi.org/10.1016/j.ab.2007.02.022
Meiklejohn, C. D., Holmbeck, M. A., Siddiq, M. A., Abt, D. N., Rand, D. M., & Montooth, K. L. (2013). An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genetics, 9(1), e1003238. https://doi.org/10.1371/journal.pgen.1003238
Meiklejohn, C. D., Montooth, K. L., & Rand, D. M. (2007). Positive and negative selection on the mitochondrial genome. Trends in Genetics, 23(6), 259-263. https://doi.org/10.1016/j.tig.2007.03.008
Milot, E., Moreau, C., Gagnon, A., Cohen, A. A., Brais, B., & Labuda, D. (2017). Mother’s curse neutralizes natural selection against a human genetic disease over three centuries. Nature Ecology and Evolution, 1(9), 1400. https://doi.org/10.1038/s41559-017-0276-6
Mishmar, D., Ruiz-Pesini, E., Golik, P., Macaulay, V., Clark, A. G., Hosseini, S., … Wallace, D. C. (2003). Natural selection shaped regional mtDNA variation in humans. Proceedings of the National Academy of Sciences of the United States of America, 100(1), 171-176. https://doi.org/10.1073/pnas.0136972100
Montooth, K. L., Dhawanjewar, A. S., & Meiklejohn, C. D. (2019). Temperature-sensitive reproduction and the physiological and evolutionary potential for Mother's Curse. Integrative and Comparative Biology, https://doi.org/10.1093/icb/icz091
Montooth, K. L., Meiklejohn, C. D., Abt, D. N., & Rand, D. M. (2010). Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to fixed incompatibilities between species of Drosophila. Evolution, 64(12), 3364-3379. https://doi.org/10.1111/j.1558-5646.2010.01077.x
Morales, H. E., Pavlova, A., Amos, N., Major, R., Kilian, A., Greening, C., & Sunnucks, P. (2018). Concordant divergence of mitogenomes and a mitonuclear gene cluster in bird lineages inhabiting different climates. Nature Ecology and Evolution, 2(8), 1258. https://doi.org/10.1038/s41559-018-0606-3
Mossman, J. A., Biancani, L. M., Zhu, C. T., & Rand, D. M. (2016). Mitonuclear epistasis for development time and its modification by diet in Drosophila. Genetics, 203(1), 463-484. https://doi.org/10.1534/genetics.116.187286
Mossman, J. A., Jennifer, Y. G., Navarro, F., & Rand, D. M. (2019). Mitochondrial DNA fitness depends on nuclear genetic background in Drosophila. G3: Genes, Genomes, Genetics, 9(4), 1175-1188. https://doi.org/10.1534/g3.119.400067
Mossman, J. A., Tross, J. G., Jourjine, N. A., Li, N., Wu, Z., & Rand, D. M. (2017). Mitonuclear interactions mediate transcriptional responses to hypoxia in Drosophila. Molecular Biology and Evolution, 34(2), 447-466. https://doi.org/10.1093/molbev/msw246
Mossman, J. A., Tross, J. G., Li, N., Wu, Z., & Rand, D. M. (2016). Mitochondrial-nuclear interactions mediate sex-specific transcriptional profiles in Drosophila. Genetics, 204(2), 613-630. https://doi.org/10.1534/genetics.116.192328
Moya, A., Peretó, J., Gil, R., & Latorre, A. (2008). Learning how to live together: Genomic insights into prokaryote-animal symbioses. Nature Reviews Genetics, 9(3), 218. https://doi.org/10.1038/nrg2319
Nagao, Y., Totsuka, Y., Atomi, Y., Kaneda, H., Lindahl, K. F., Imai, H., & Yonekawa, H. (1998). Decreased physical performance of congenic mice with mismatch between the nuclear and the mitochondrial genome. Genes and Genetic Systems, 73(1), 21-27. https://doi.org/10.1266/ggs.73.21
Nakada, K., Sato, A., Yoshida, K., Morita, T., Tanaka, H., Inoue, S.-I., … Hayashi, J.-I. (2006). Mitochondria-related male infertility. Proceedings of the National Academy of Sciences of the United States of America, 103(41), 15148-15153. https://doi.org/10.1073/pnas.0604641103
Osada, N., & Akashi, H. (2012). Mitochondrial-nuclear interactions and accelerated compensatory evolution: Evidence from the primate cytochrome c oxidase complex. Molecular Biology and Evolution, 29(1), 337-346. https://doi.org/10.1093/molbev/msr211
Partridge, L., & Andrews, R. (1985). The effect of reproductive activity on the longevity of male Drosophila melanogaster is not caused by an acceleration of ageing. Journal of Insect Physiology, 31(5), 393-395. https://doi.org/10.1016/0022-1910(85)90084-8
Patel, M. R., Miriyala, G. K., Littleton, A. J., Yang, H., Trinh, K., Young, J. M., … Malik, H. S. (2016). A mitochondrial DNA hypomorph of cytochrome oxidase specifically impairs male fertility in Drosophila melanogaster. Elife, 5, e16923. https://doi.org/10.7554/eLife.16923.001
Pesole, G., Allen, J. F., Lane, N., Martin, W., Rand, D. M., Schatz, G., & Saccone, C. (2012). The neglected genome. EMBO Reports, 13(6), 473-474. https://doi.org/10.1038/embor.2012.57
Pichaud, N., Bérubé, R., Côté, G., Belzile, C., Dufresne, F., Morrow, G., … Blier, P. (2019). How much mitonuclear mismatch can mitochondria tolerate? Frontiers in Genetics, 10, 130. https://doi.org/10.3389/fgene.2019.00130
Popadin, K. Y., Nikolaev, S. I., Junier, T., Baranova, M., & Antonarakis, S. E. (2012). Purifying selection in mammalian mitochondrial protein-coding genes is highly effective and congruent with evolution of nuclear genes. Molecular Biology and Evolution, 30(2), 347-355. https://doi.org/10.1093/molbev/mss219
Priest, N. K., Roach, D. A., & Galloway, L. F. (2007). Mating-induced recombination in fruit flies. Evolution, 61(1), 160-167. https://doi.org/10.1111/j.1558-5646.2007.00013.x
R Development Core Team (2013). R: A language and environment for statistical computing.
Radzvilavicius, A. L. (2016). Evolutionary dynamics of cytoplasmic segregation and fusion: Mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes. Journal of Theoretical Biology, 404, 160-168. https://doi.org/10.1016/j.jtbi.2016.05.037
Radzvilavicius, A. L., & Blackstone, N. W. (2015). Conflict and cooperation in eukaryogenesis: Implications for the timing of endosymbiosis and the evolution of sex. Journal of the Royal Society Interface, 12(111), 20150584. https://doi.org/10.1098/rsif.2015.0584
Ramsey, A. J., McCauley, D. E., & Mandel, J. R. (2019). Heteroplasmy and patterns of cytonuclear linkage disequilibrium in wild carrot. Integrative and Comparative Biology, 59(4), 1005-1015. https://doi.org/10.1093/icb/icz102
Rand, D. M. (2001). The units of selection on mitochondrial DNA. Annual Review of Ecology and Systematics, 32(1), 415-448. https://doi.org/10.1146/annurev.ecolsys.32.081501.114109
Rand, D. M., Fry, A., & Sheldahl, L. (2006). Nuclear-mitochondrial epistasis and Drosophila aging: Introgression of Drosophila simulans mtDNA modifies longevity in D. melanogaster nuclear backgrounds. Genetics, 172(1), 329-341. https://doi.org/10.1534/genetics.105.046698
Rand, D. M., Haney, R. A., & Fry, A. J. (2004). Cytonuclear coevolution: The genomics of cooperation. Trends in Ecology and Evolution, 19(12), 645-653. https://doi.org/10.1016/j.tree.2004.10.003
Rand, D. M., Mossman, J. A., Zhu, L., Biancani, L. M., & Ge, J. Y. (2018). Mitonuclear epistasis, genotype-by-environment interactions, and personalized genomics of complex traits in Drosophila. IUBMB Life, 70(12), 1275-1288. https://doi.org/10.1002/iub.1954
Rice, W. R., Linder, J. E., Friberg, U., Lew, T. A., Morrow, E. H., & Stewart, A. D. (2005). Inter-locus antagonistic coevolution as an engine of speciation: Assessment with hemiclonal analysis. Proceedings of the National Academy of Sciences of the United States of America, 102(suppl 1), 6527-6534. https://doi.org/10.1073/pnas.0501889102
Richardson, M. F., Weinert, L. A., Welch, J. J., Linheiro, R. S., Magwire, M. M., Jiggins, F. M., & Bergman, C. M. (2012). Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genetics, 8(12), e1003129. https://doi.org/10.1371/journal.pgen.1003129
Roubertoux, P. L., Sluyter, F., Carlier, M., Marcet, B., Maarouf-Veray, F., Chérif, C., … Cohen-Salmon, C. (2003). Mitochondrial DNA modifies cognition in interaction with the nuclear genome and age in mice. Nature Genetics, 35(1), 65. https://doi.org/10.1038/ng1230
Ruiz-Pesini, E., Mishmar, D., Brandon, M., Procaccio, V., & Wallace, D. C. (2004). Effects of purifying and adaptive selection on regional variation in human mtDNA. Science, 303(5655), 223-226. https://doi.org/10.1126/science.1088434
Sackton, T. B., Haney, R. A., & Rand, D. M. (2003). Cytonuclear coadaptation in Drosophila: Disruption of cytochrome c oxidase activity in backcross genotypes. Evolution, 57(10), 2315-2325. https://doi.org/10.1111/j.0014-3820.2003.tb00243.x
Salvucci, E. (2016). Microbiome, holobiont and the net of life. Critical Reviews in Microbiology, 42(3), 485-494. https://doi.org/10.3109/1040841X.2014.962478
Seong, S. Y., Choi, M. S., & Kim, I. S. (2001). Orientia tsutsugamushi infection: Overview and immune responses. Microbes and Infection, 3(1), 11-21. https://doi.org/10.1016/S1286-4579(00)01352-6
Shtolz, N., & Mishmar, D. (2019). The mitochondrial genome-on selective constraints and signatures at the organism, cell, and single mitochondrion levels. Frontiers in Ecology and Evolution, 7, 342. https://doi.org/10.3389/fevo.2019.00342
Sloan, D. B., Fields, P. D., & Havird, J. C. (2015). Mitonuclear linkage disequilibrium in human populations. Proceedings of the Royal Society B: Biological Sciences, 282(1815), 20151704. https://doi.org/10.1098/rspb.2015.1704
Sloan, D. B., Havird, J. C., & Sharbrough, J. (2017). The on-again, off-again relationship between mitochondrial genomes and species boundaries. Molecular Ecology, 26(8), 2212-2236. https://doi.org/10.1111/mec.13959
Sloan, D. B., Triant, D. A., Forrester, N. J., Bergner, L. M., Wu, M., & Taylor, D. R. (2014). A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae). Molecular Phylogenetics and Evolution, 72, 82-89. https://doi.org/10.1016/j.ympev.2013.12.004
Smith, S., Turbill, C., & Suchentrunk, F. (2010). Introducing mother’s curse: Low male fertility associated with an imported mtDNA haplotype in a captive colony of brown hares. Molecular Ecology, 19(1), 36-43. https://doi.org/10.1111/j.1365-294X.2009.04444.x
St. John, J. C. (2019). Genomic balance: Two genomes establishing synchrony to modulate cellular fate and function. Cells, 8(11), 1306. https://doi.org/10.3390/cells8111306
Stojković, B., & Đorđević, M. (2017). Interaction between mitochondrial and nuclear genomes: The role in life-history evolution. Biologia Serbica, 39(1), 32-40. https://doi.org/10.5281/zenodo.826619
Taanman, J. W. (1999). The mitochondrial genome: Structure, transcription, translation and replication. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1410(2), 103-123. https://doi.org/10.1016/S0005-2728(98)00161-3
Tobler, M., Barts, N., & Greenway, R. (2019). Mitochondria and the origin of species: Bridging genetic and ecological perspectives on speciation processes. Integrative and Comparative Biology, 59(4), 900-911. https://doi.org/10.1093/icb/icz025
Tourmente, M., Hirose, M., Ibrahim, S., Dowling, D. K., Tompkins, D. M., Roldan, E. R., & Gemmell, N. J. (2017). mtDNA polymorphism and metabolic inhibition affect sperm performance in conplastic mice. Reproduction, 154(4), 341-354. https://doi.org/10.1530/REP-17-0206
Turelli, M. (1994). Evolution of incompatibility-inducing microbes and their hosts. Evolution, 48(5), 1500-1513. https://doi.org/10.1111/j.1558-5646.1994.tb02192.x
Vaught, R. C., & Dowling, D. K. (2018). Maternal inheritance of mitochondria: Implications for male fertility? Reproduction, 155(4), R159-R168. https://doi.org/10.1530/REP-17-0600
Wade, M. J. (2014). Paradox of mother's curse and the maternally provisioned offspring microbiome. Cold Spring Harbor Perspectives in Biology, 6(10), a017541. https://doi.org/10.1101/cshperspect.a017541
Werren, J. H. (1997). Biology of Wolbachia. Annual Review of Entomology, 42(1), 587-609. https://doi.org/10.1146/annurev.ento.42.1.587
Werren, J. H., Baldo, L., & Clark, M. E. (2008). Wolbachia: Master manipulators of invertebrate biology. Nature Reviews Microbiology, 6(10), 741-751. https://doi.org/10.1038/nrmicro1969
Williams, B. R., Van Heerwaarden, B., Dowling, D. K., & Sgro, C. M. (2012). A multivariate test of evolutionary constraints for thermal tolerance in Drosophila melanogaster. Journal of Evolutionary Biology, 25(7), 1415-1426. https://doi.org/10.1111/j.1420-9101.2012.02536.x
Wolff, J. N., & Gemmell, N. J. (2013). Mitochondria, maternal inheritance, and asymmetric fitness: Why males die younger. BioEssays, 35(2), 93-99. https://doi.org/10.1002/bies.201200141
Wolff, J. N., Ladoukakis, E. D., Enríquez, J. A., & Dowling, D. K. (2014). Mitonuclear interactions: Evolutionary consequences over multiple biological scales. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1646), 20130443. https://doi.org/10.1098/rstb.2013.0443
Xu, H., DeLuca, S. Z., & O'Farrell, P. H. (2008). Manipulating the metazoan mitochondrial genome with targeted restriction enzymes. Science, 321(5888), 575-577. https://doi.org/10.1126/science.1160226
Yan, Z., Ye, G. Y., & Werren, J. (2018). Evolutionary rate coevolution between mitochondria and mitochondria-associated nuclear-encoded proteins in insects. bioRxiv, 288456. https://doi.org/10.1101/288456
Yee, W. K., Sutton, K. L., & Dowling, D. K. (2013). In vivo male fertility is affected by naturally occurring mitochondrial haplotypes. Current Biology, 23(2), R55-R56. https://doi.org/10.1016/j.cub.2012.12.002
Zeyl, C., Andreson, B., & Weninck, E. (2005). Nuclear-mitochondrial epistasis for fitness in Saccharomyces cerevisiae. Evolution, 59(4), 910-914. https://doi.org/10.1111/j.0014-3820.2005.tb01764.x
Zhu, C. T., Ingelmo, P., & Rand, D. M. (2014). G×G×E for lifespan in Drosophila: Mitochondrial, nuclear, and dietary interactions that modify longevity. PLoS Genetics, 10(5), e1004354. https://doi.org/10.1371/journal.pgen.1004354
Zhu, Z., Han, X., Wang, Y., Liu, W., Lu, Y., Xu, C., … Han, C. (2019). Identification of specific nuclear genetic loci and genes that interact with the mitochondrial genome and contribute to fecundity in Caenorhabditis elegans. Frontiers in Genetics, 10, 28. https://doi.org/10.3389/fgene.2019.00028
Zhu, Z., Lu, Q., Zeng, F., Wang, J., & Huang, S. (2015). Compatibility between mitochondrial and nuclear genomes correlates with the quantitative trait of lifespan in Caenorhabditis elegans. Scientific Reports, 5, 17303. https://doi.org/10.1038/srep17303
Zug, R., & Hammerstein, P. (2015). Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews, 90(1), 89-111. https://doi.org/10.1111/brv.12098