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Changes in selection intensity on the mitogenome of subterranean and fossorial rodents respective to aboveground species

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Abstract

Several rodent lineages independently acquired the ability to dig complex networks of tunnels where fossorial and subterranean species spend part or their whole life, respectively. Their underground lifestyles imposed harsh physiological demands, presumably triggering strong selective pressures on genes involved in energy metabolism like those coding for mitochondrial proteins. Moreover, underground lifestyles must have increased inbreeding and susceptibility to population bottlenecks as well as restricted migration, leading to small effective population size (Ne) that, in turn, must have reduced the effectiveness of selection. These stringent environmental conditions and small Ne might be still operating as antagonist factors of selection efficacy in these rodents. In this report, we tested, in a phylogenetic framework, how the intensity of selection on protein-coding mitochondrial genes (mt-genes) fluctuated along the evolution of fossorial and subterranean rodents respective to aboveground lineages. Our findings showed significant selection relaxation in most mt-genes of subterranean hystricomorphs (African mole-rats, tuco-tucos, and coruro), while only in three mt-genes of fossorial hystricomorphs (degus, red vizcacha rat, and fossorial spiny rats) selection efficacy was strongly reduced, probably due to demographic constraints. Conversely, selection intensification was found to have occurred in three mt-genes in fossorial sciuromorphs (ground squirrels, chipmunks, marmot, and allies). Our findings indicated that evolution of mitogenomes in fossorial and, mainly, in subterranean rodents was a complex output of a balance between intense ecological and physiological pressures, together with demographic constraints leading to genetic drift that, in turn, might have resulted in relaxed selection in hystricomorphs.

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References

  • Adkins RM, Gelke EL, Rowe D, Honeycutt RL (2001) Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Mol Biol Evol 18:777–791

    Article  PubMed  CAS  Google Scholar 

  • Álvarez A, Moyers RL, Arévalo, Verzi DH (2017) Diversification patterns and size evolution in caviomorph rodents. Biol J Linn Soc 121:907–922

    Article  Google Scholar 

  • Antolin MF, Van Horne B, Berger MD Jr, Holloway AK, Roach JL, Weeks RD, Jr (2001) Effective population size and genetic structure of a Piute ground squirrel (Spermophilus mollis) population. Can J Zool 79:26–34

    Article  Google Scholar 

  • Begall S, Burda H, Schleich CE (2007). Subterranean rodents. Springer, Berlin

    Book  Google Scholar 

  • Blanga-Kanfi S, Miranda H, Penn O, Pupko T, DeBry RW, Huchon D (2009) Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evol Biol 9:71

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83:1153–1181

    Article  PubMed  CAS  Google Scholar 

  • Carleton MD, Musser GG (2005) Order rodentia. In: Wilson DE, Reeder DM (eds) Mammal species of the world. The Johns Hopkins University Press, Baltimore, 745–752

    Google Scholar 

  • Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Charlesworth D (2010) Elements of evolutionary genetics. Roberts and Company Publishers, Greenwood Village

    Google Scholar 

  • Churakov G, Sadasivuni MK, Rosenbloom KR, Huchon D, Brosius J, Schmitz J (2010) Rodent evolution: back to the root. Mol Biol Evol 27:1315–1326

    Article  PubMed  CAS  Google Scholar 

  • Cutrera AP, Lacey EA, Bush C (2006) Intraspecific variation in effective population size in talar tuco-tucos (Ctenomys talarum): the role of demography. J Mammal 87:108–116

    Article  Google Scholar 

  • Davies KTJ, Bennett NC, Tsagkogeorga G, Rossiter SJ, Faulkes CG (2015) Family wide molecular adaptations to underground life in african mole-rats revealed by phylogenomic analysis. Mol Biol Evol 32:msv175

    Article  CAS  Google Scholar 

  • Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113

    Article  CAS  Google Scholar 

  • Eyre-Walker A, Keightley PD, Smith NGC, Gaffney D (2002) Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol 19:2142–2149

    Article  PubMed  CAS  Google Scholar 

  • Fabre P-H, Hautier L, Dimitrov D, Douzery EJP (2012) A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol Biol 12:88

    Article  PubMed  PubMed Central  Google Scholar 

  • Fabre P-H, Galewski T, Tilak M, Douzery EJP (2013) Diversification of South American spiny rats (Echimyidae): a multigene phylogenetic approach. Zool Scr 42:117–134

    Article  Google Scholar 

  • Fabre P-H, Upham NS, Emmons LH, Justy F, Leite YLR, Loss AC, Orlando L, Tilak M-K, Patterson BD, Douzery EJP (2016) Mitogenomic phylogeny, diversification, and biogeography of South American spiny rats. Mol Biol Evol 34:msw261

    Article  Google Scholar 

  • Fernández ME, Vassallo AI, Zárate M (2000) Functional morphology and palaeobiology of the pliocene rodent Actenomys (Caviomorpha: Octodontidae): the evolution to a subterranean mode of life. Biol J Linn Soc 71:71–90

    Article  Google Scholar 

  • Galewski T, Mauffrey J-F, Leite YLR, Patton JL, Douzery EJP (2005) Ecomorphological diversification among South American spiny rats (Rodentia; Echimyidae): a phylogenetic and chronological approach. Mol Phylogenet Evol 34:601–615

    Article  PubMed  CAS  Google Scholar 

  • Gallardo MH, Kohler N, Araneda C (1995) Bottleneck effects in local populations of fossorial Ctenomys (Rodentia, ctenomyidae) affected by vulcanism. Heredity 74:647–653

    Article  Google Scholar 

  • Garvin MR, Bielawski JP, Sazanov LA, Gharrett AJ (2015) Review and meta-analysis of natural selection in mitochondrial complex I in metazoans. J Zool Syst Evol Res 53:1–17

    Article  Google Scholar 

  • Ginot S, Hautier L, Marivaux L, Vianey-Liaud M (2016) Ecomorphological analysis of the astragalo-calcaneal complex in rodents and inferences of locomotor behaviours in extinct rodent species. Peer J 4:e2393

    Article  PubMed  Google Scholar 

  • Hampton M, Melvin RG, Kendall AH, Kirkpatrick BR, Peterson N, Andrews MT (2011) Deep sequencing the transcriptome reveals seasonal adaptive mechanisms in a hibernating mammal. PLoS ONE 6:e27021

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hildebrand M 1988. Analysis of vertebrate structure. 3rd edn. Wiley, New York

    Google Scholar 

  • Hittel DS, Storey KB (2002) Differential expression of mitochondria-encoded genes in a hibernating mammal. J Exp Biol 205:1625–1631

    PubMed  CAS  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  CAS  Google Scholar 

  • Lacey EA, Cutrera AP (2007) Behavior, demography, and immunogenetic variation: new insights from subterranean rodents. In: Subterranean rodents. Springer, Berlin Heidelberg, pp 341–355

    Chapter  Google Scholar 

  • Lacey EA, Patton JL, Cameron GN (eds) (2000) Life underground: the biology of subterranean rodents. The University of Chicago Press, Chicago

    Google Scholar 

  • Lagaria A, Youlatos D (2006) Anatomical correlates to scratch digging in the forelimb of European ground squirrels (Spermophilus citellus). J Mammal 87:563–570

    Article  Google Scholar 

  • Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2017) Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773

    PubMed  Google Scholar 

  • Lessa EP (2000) The evolution of subterranean rodents: a synthesis. In: Lacey EA, Patton JL, Cameron GN (eds) Life underground: the biology of subterranean rodents. The University of Chicago Press, Chicago, 390–420

    Google Scholar 

  • Lessa EP, Vassallo AI, Verzi DH, Mora MS (2008) Evolution of morphological adaptations for digging in living and extinct ctenomyid and octodontid rodents. Biol J Linn Soc 95:267–283

    Article  Google Scholar 

  • Lloyd RE, McGeehan JE (2013) Structural analysis of mitochondrial mutations reveals a role for bigenomic protein interactions in human disease. PLoS ONE 8:e69003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Loss AC, Leite YLR (2015) Distribuição geográfica e variação genética de Euryzygomatomys spinosus (Rodentia: Echimyidae). In: 8° Congresso Brasileiro de Mastozoologia. Sociedade Brasileira de Mastozoologia, João Pessoa, Rodentia, p 275

    Google Scholar 

  • Morgan CC, Verzi DH (2011) Carpal-metacarpal specializations for burrowing in South American octodontoid rodents. J Anat 219:167–175

    Article  PubMed  PubMed Central  Google Scholar 

  • Nabholz B, Ellegren H, Wolf JBW (2013) High levels of gene expression explain the strong evolutionary constraint of mitochondrial protein-coding genes. Mol Biol Evol 30:272–284

    Article  PubMed  CAS  Google Scholar 

  • Nevo E (1995) Mammalian evolution underground. The ecological-genetic-phenetic interfaces. Acta Theriol 3:9–31

    Article  Google Scholar 

  • Ojeda AA (2010) Phylogeography and genetic variation in the South American rodent Tympanoctomys barrerae (Rodentia: Octodontidae). J Mammal 91:302–313

    Article  Google Scholar 

  • Opazo JC, Bugueño MP, Carter MJ, Palma RE, Bozinovic F (2008) Phylogeography of the Subterranean Rodent Spalacopus cyanus (Caviomorpha, Octodontidae). J Mammal 89:837–844

    Article  Google Scholar 

  • Patterson BD, Upham NS (2014) A newly recognized family from the Horn of Africa, the Heterocephalidae (Rodentia: Ctenohystrica). Zool J Linn Soc 172:942–963

    Article  Google Scholar 

  • Patton JL, Pardiñas UFJ, D’Elía G (eds) (2015) Mammals of South America. The University of Chicago Press, Chicago

    Google Scholar 

  • Penney DF, Zimmerman EG (1976) Genic divergence and local population differentiation by random drift in the pocket gopher genus Geomys. Evolution 30:473–483

    Article  PubMed  Google Scholar 

  • Phifer-Rixey M, Bonhomme F, Boursot P, Churchill GA, Piálek J, Tucker PK, Nachman MW (2012) Adaptive evolution and effective population size in wild house mice. Mol Biol Evol 29:2949–2955

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF (1990) DNA “fingerprinting” reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proc Natl Acad Sci 87:2496–2500

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard M, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulte-Hostedde AI, Gibbs HL, Millar JS (2001) Microgeographic genetic structure in the yellow-pine chipmunk (Tamias amoenus). Mol Ecol 10:1625–1631

    Article  PubMed  CAS  Google Scholar 

  • Silva CC, da IH, Tomasco FG, Hoffman, Lessa EP (2009) Genes and ecology: accelerated rates of replacement substitutions in the cytochrome b gene of subterranean rodents. Open Evol J 3:17–30

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2759

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tavares WC, Abi-Rezik P, Seuánez HN (2018) Historical and ecological influence in the evolutionary diversification of external morphology of neotropical spiny rats (Echimyidae, Rodentia). J Zool Syst Evol Res 1–12

  • Tomasco IH, Lessa EP (2011) The evolution of mitochondrial genomes in subterranean caviomorph rodents: adaptation against a background of purifying selection. Mol Phylogenet Evol 61:64–70

    Article  PubMed  Google Scholar 

  • Tomasco IH, Lessa EP (2014) Two mitochondrial genes under episodic positive selection in subterranean octodontoid rodents. Gene 534:371–378

    Article  PubMed  CAS  Google Scholar 

  • Wallace DC (2005) A Mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wertheim JO, Murrell B, Smith MD, Kosakovsky Pond SL, Scheffler K (2015) RELAX: detecting relaxed selection in a phylogenetic framework. Mol Biol Evol 32:820–832

    Article  PubMed  CAS  Google Scholar 

  • Wlasiuk G, Garza JC, Lessa EP (2003) Genetic and geographic differentiation in the Rio Negro tuco-tuco (Ctenomys rionegrensis): inferring the roles of migration and drift from multiple genetic markers. Evolution 57:913–926

    Article  PubMed  Google Scholar 

  • Wu S, Wu W, Zhang F, Ye J, Ni X, Sun J, Edwards SV, Meng J, Organ CL (2012) Molecular and paleontological evidence for a post-cretaceous origin of rodents. PLoS ONE 7:e46445

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xia X (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  PubMed  CAS  Google Scholar 

  • Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. In: Salemi M, Vandamme A-M (eds) The phylogenetic handbook: a practical approach to DNA and protein phylogeny. Cambridge University Press, Cambridge, 615–630

    Chapter  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7

    Article  PubMed  CAS  Google Scholar 

  • Zelditch ML, Li J, Tran LAP, Swiderski DL. 2015. Relationships of diversity, disparity, and their evolutionary rates in squirrels (Sciuridae). Evolution 69: 1284–1300

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a postdoctoral fellowship to WCT provided by Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro and Coordenação de Aperfeiçoamento de Pessoal de Níıvel Superior—FAPERJ/CAPES (Grant E26/202.171/15).

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Correspondence to Hector N. Seuánez.

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Tavares, W.C., Seuánez, H.N. Changes in selection intensity on the mitogenome of subterranean and fossorial rodents respective to aboveground species. Mamm Genome 29, 353–363 (2018). https://doi.org/10.1007/s00335-018-9748-5

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