Do mito-nuclear interactions impact life-history traits? Rank et al. (2020) found that these genomic interactions are of great importance in wild populations of the leaf beetle Chrysomela aeneicollis and may explain why populations are highly differentiated

Camus, MF

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UCL Discovery

Digest: Mito-nuclear interactions modulate life-history phenotypes in the wild 1 M. Florencia Camus1 2  3 1 Research Department of Genetics, Evolution and Environment, University College  4 London, Gower Street, London, WC1E 6BT, United Kingdom 5  6 Email: f.camus@ucl.ac.uk 7  8 Footnote: This article corresponds to Rank, NE, Mardulyn P, Heidl SJ, Roberts KT, 9 Zavala NA, Smiley JT, Dahlhoff EP. 2020. Mitonuclear mismatch alters 10 performance and reproductive success in naturally‐introgressed populations 11 of a montane leaf beetle. Evolution. doi:10.1111/evo.13962. 12 https://onlinelibrary.wiley.com/doi/10.1111/evo.13962 13  14  15 Abstract: Do mito-nuclear interactions impact life-history traits? Rank et al. (2020) 16 found that these genomic interactions are of great importance in wild populations of 17 the leaf beetle Chrysomela aeneicollis and may explain why populations are highly 18 differentiated.  19  20 Main Text: 21 Mitochondria are essential organelles for life in eukaryotes, taking center stage in the 22 process of cellular respiration. This process is regulated via a series of finely 23 coordinated obligate interactions of molecules encoded by two genomes: nuclear 24 and mitochondrial. Both genomes are required to work harmoniously to provide 25 cellular energy, and thus their interaction is vital for the maintenance of mitochondrial 26 integrity and the viability of eukaryote life (Lane 2005). For the past two decades, 27 many studies have shown high levels of phenotype-changing genetic variation within 28 the mtDNA genome. These findings run counter to the traditional paradigm in which 29 mitochondrial genetic variation was expected to be evolving neutrally (Rand 2001; 30 Burton, et al. 2013). It remains unclear whether mitochondrial genetic variation is 31 accumulating adaptively under selection, or non-adaptively under mutation-selection 32 balance. 33  34 A series of observations has led to the hypothesis that genetic variation found within 35 the mitochondrial genome has been shaped by natural selection imposed by the 36 prevailing thermal climate (Mishmar, et al. 2003; Ruiz-Pesini, et al. 2004). For 37 instance, some studies have detected positive selective sweeps in the mitochondrial 38 genome (Meiklejohn et al. 2007), while others have found that the frequencies of 39 particular mtDNA haplotypes change with latitudinal or altitudinal variation (Silva et 40 al. 2014; Camus et al. 2017). While a few studies have shown evidence for mito-41 nuclear coadaptation (Immonen et al. 2016; Morales et al. 2018; Healy and Burton 42 2020), obtaining evidence from natural populations is a complex endeavor. 43  44 In this issue, Rank et al. (2020) investigated links between mito-nuclear genotype 45 and components of fitness in natural populations of the leaf beetle Chrysomela 46 aeneicollis. They first examined a 65 km latitudinal transect and found that 47 populations at the north and south edges had distinct mito-nuclear genotypes, with 48 intermediate populations showing signs of intermixing (Figure 1A). The authors then 49 focused on the region where intermixing occurred. They compared individuals whose 50 mitochondrial and nuclear genotypes “matched”—i.e., both came from either the 51 northern or southern population—to individuals with “mismatched” mitochondrial and 52 nuclear genotypes, where the two genomes came from different populations. They 53 examined how matched or mismatched genomes impacted key life-history traits, 54 including fecundity, larval development, and male mating frequency.  55  56 Rank et al. (2020) found that beetles with matched mito-nuclear genomes typically 57 outperformed genomically mismatched beetles, which moved slower, mated less, 58 and were less fecund (Figure 1B). Notably, these effects were amplified following 59 heat treatment. In addition, the direction of the mito-nuclear mixing was not 60 symmetrical; beetles with northern nuclear genomes and southern mtDNA suffered 61 the most. In sum, the authors’ results demonstrate that mito-nuclear interactions are 62 of great importance to life-history evolution and may play a large role in maintaining 63 population structure. 64  65 Mito-nuclear interactions have been largely overlooked in natural populations and 66 have the potential to play an important role in many evolutionary processes, from 67 responses to disease to speciation. This study provides a robust ecological 68 experimental framework to test the effects of mito-nuclear epistasis, which can 69 further the goal of understanding genotype-specific effects on traits that shape life 70 history evolution. 71  72  73  74 Figure Legend 75  76  77 Figure 1: (A) Visual representation of mito-nuclear genotypes across the sampling 78 locations. (B) Overview of main findings, whereby matched genotypes mostly 79 outperformed mismatched individuals.  80  81 References 82  83 Burton RS, Pereira RJ, Barreto FS. 2013. Cytonuclear genomic interactions and 84 hybrid breakdown. Annual Review of Ecology, Evolution, and Systematics 85 44:281-302. 86 Camus MF, Wolff JN, Sgrò CM, Dowling DK. 2017. Experimental support that natural 87 selection has shaped the latitudinal distribution of mitochondrial haplotypes in 88 Australian Drosophila melanogaster. Molecular Biology and Evolution 89 34:2600-2612. 90 Healy TM, Burton RS. 2020. Strong selective effects of mitochondrial DNA on the 91 nuclear genome. Proceedings of the National Acadamy of Sciences USA 92 117:6616-6621. 93 Immonen E, Collet M, Goenaga J, Arnqvist G. 2016. Direct and indirect genetic 94 effects of sex-specific mitonuclear epistasis on reproductive ageing. Heredity 95 116:338-347. 96 North SouthIntermixed"Mismatched"Matched MismatchedTraitA BLane N. 2005. Power, sex, suicide: mitochondria and the meaning of life. Oxford ; 97 New York: Oxford University Press. 98 Meiklejohn CD, Montooth KL, Rand DM. 2007. Positive and negative selection on 99 the mitochondrial genome. Trends in Genetics 23:259-263. 100 Mishmar D, Ruiz-Pesini E, Golik P, Macaulay V, Clark AG, Hosseini S, Brandon M, 101 Easley K, Chen E, Brown MD, et al. 2003. Natural selection shaped regional 102 mtDNA variation in humans. Proceedings of the National Academy of 103 Sciences USA 100:171-176. 104 Morales HE, Pavlova A, Amos N, Major R, Kilian A, Greening C, Sunnucks P. 2018. 105 Concordant divergence of mitogenomes and a mitonuclear gene cluster in 106 bird lineages inhabiting different climates. Nature Ecology Evolution 2:1258-107 1267. 108 Rand DM. 2001. The units of selection in mitochondrial DNA. Annual Review of 109 Ecology, Evolution, and Systematics 32:415-448. 110 Rank, NE, Mardulyn P, Heidl SJ, Roberts KT, Zavala NA, Smiley JT, Dahlhoff EP. 111 2020. Mitonuclear mismatch alters performance and reproductive success in 112 naturally‐introgressed populations of a montane leaf beetle. Evolution. 113 doi:10.1111/evo.13962 114 Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC. 2004. Effects of 115 purifying and adaptive selection on regional variation in human mtDNA. 116 Science 303:223-226.  117 Silva G, Lima FP, Martel P, Castilho R. 2014. Thermal adaptation and clinal 118 mitochondrial DNA variation of European anchovy. Proceedings of the Royal 119 Society of London (Series B) 281:20141093.  120 

Digest: Mito-nuclear interactions modulate life-history phenotypes in the wild

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Digest: Mito-nuclear interactions modulate life-history phenotypes in the wild

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