Advertisement

The selective constraints of ecological specialization in mustelidae on mitochondrial genomes

  • Qinguo Wei
  • Honghai ZhangEmail author
  • Xiaoyang Wu
  • Weilai Sha
Original Paper
  • 40 Downloads

Abstract

The locomotor preference may drive the evolution of animals in a certain way, and species living in different environments might own different energy requirement style. We hypothesized that the locomotor preference and habitat variation might impose different influence on mustelidae mitochondrial genomes (mtDNA). To test this, we sampled 22 species of mustelidae, encompassing natatorial, scansorial, fossorial, and non-specialists, to determine whether the variation in locomotor specialization influence the evolution of their mitochondrial genomes. The selective constraints analyses showed that the ratio of non-synonymous/synonymous substitutions (dN/dS) in mitochondrial protein-coding genes (PCGs) was significantly higher in non-specialist group than specialist groups (natatorial, scansorial, and fossorial), which suggested that the specialist groups’ mtDNA experienced much stronger purifying selection during evolution as they need much more energy in their daily life. When comparing dN/dS of each PCG among these four groups, six protein-coding genes (ND2-3, ND5, CoxIII, ATP6, Cytb) also showed different dN/dS ratios between non-specialist and specialist groups. We also found that the ATP8 gene was positively selected in the branch of Lutra lutra. Our study thus demonstrated that the selective constraints relevant to locomotor specialization play an essential role in the evolution of mustelidae mtDNA.

Keywords

Locomotor preference Mitochondrial genomes Mustelidae Selective constraints dN/dS 

Notes

Funding information

This work was financially supported by the Special Fund for Forest Scientific Research in the Public Welfare (201404420) and the National Natural Science Foundation of China (31672313, 31372220).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13364_2019_461_MOESM1_ESM.xlsx (11 kb)
ESM 1 (XLSX 11 kb)
13364_2019_461_MOESM2_ESM.xlsx (13 kb)
ESM 2 (XLSX 13 kb)

References

  1. Andrieux LO, Arenales DT (2014) Whole-genome identification of neutrally evolving pseudogenes using the evolutionary measure dN/dS. Methods Mol Biol 1167:75–85PubMedCrossRefPubMedCentralGoogle Scholar
  2. Balaban R, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120:483–495PubMedCrossRefPubMedCentralGoogle Scholar
  3. Beja PR (1996) An analysis of otter Lutra lutra predation on introduced american crayfish Procambarus clarkii in Iberian streams. J Appl Ecol 33:1156–1170CrossRefGoogle Scholar
  4. Björnerfeldt S, Webster M, Tvilà C (2006) Relaxation of selective constraint on dog mitochondrial DNA following domestication. Genome Res 16:990–994PubMedPubMedCentralCrossRefGoogle Scholar
  5. Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780PubMedPubMedCentralCrossRefGoogle Scholar
  6. Botton-Divet L, Cornette R, Houssaye A, Fabre AC, Herrel A (2017) Swimming and running: a study of the convergence in long bone morphology among semi-aquatic mustelids (Carnivora: Mustelidae). Biol J Linn Soc 121:38–49CrossRefGoogle Scholar
  7. Botton-Divet L, Houssaye A, Herrel A, Fabre AC, Cornette R (2018) Swimmers, diggers, climbers and more, a study of integration across the mustelids’ locomotor apparatus (Carnivora: Mustelidae). Evol Biol 45:182–195CrossRefGoogle Scholar
  8. Chong RA, Mueller RL (2013) Low metabolic rates in salamanders are correlated with weak selective constraints on mitochondrial genes. Evolution 67:894–899PubMedCrossRefPubMedCentralGoogle Scholar
  9. Das J (2010) The role of mitochondrial respiration in physiological and evolutionary adaptation. Bioessays 28:890–901CrossRefGoogle Scholar
  10. Edgar RC (2004) MUSCLE: multiple sequence alignment with improved accuracy and speed. In: Computational Systems Bioinformatics Conference.Google Scholar
  11. Fabre AC, Cornette R, Slater G, Argot C, Peigné S, Goswami A, Pouydebat E (2013) Getting a grip on the evolution of grasping in musteloid carnivorans: a three-dimensional analysis of forelimb shape. J Evol Biol 26:1521–1535PubMedCrossRefPubMedCentralGoogle Scholar
  12. Fabre AC, Cornette R, Goswami A, Peigné S (2015) Do constraints associated with the locomotor habitat drive the evolution of forelimb shape? A case study in musteloid carnivorans. J Anat 226:596–610PubMedPubMedCentralCrossRefGoogle Scholar
  13. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  14. Fonseca RRD, Johnson WE, O’Brien SJ, Ramos MJ, Antunes A (2008) The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics 9:119–119PubMedPubMedCentralCrossRefGoogle Scholar
  15. Galtier N, Nabholz B, Glémin S, Hurst GD (2010) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18:4541–4550CrossRefGoogle Scholar
  16. Holmes T (1980) Locomotor adaptations in the limb skeletons of North American mustelids. Humboldt State UniversityGoogle Scholar
  17. Hughes AL (2013) Accumulation of slightly deleterious mutations in the mitochondrial genome: a hallmark of animal domestication. Gene 515:28–33PubMedCrossRefPubMedCentralGoogle Scholar
  18. Iversen JA (1972) Basal energy metabolism of mustelids. J Comp Physiol 81:341–344CrossRefGoogle Scholar
  19. Kilbourne BM (2017) Selective regimes and functional anatomy in the mustelid forelimb: diversification toward specializations for climbing, digging, and swimming. Ecol Evol 7:8852–8863PubMedPubMedCentralCrossRefGoogle Scholar
  20. Koepfli KP, Deere KA, Slater GJ, Begg C, Begg K, Grassman L, Lucherini M, Veron G, Wayne RK (2008) Multigene phylogeny of the Mustelidae: resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biol 6:1–22CrossRefGoogle Scholar
  21. Kruuk H, Balharry E, Taylor PT (1994) Oxygen consumption of the Eurasian otter Lutra lutra in relation to water temperature. Physiol Zool 67:1174–1185CrossRefGoogle Scholar
  22. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874PubMedCrossRefGoogle Scholar
  23. Maceachern S, Mcewan J, Mcculloch A, Mather A, Savin K, Goddard M (2009) Molecular evolution of the Bovini tribe (Bovidae, Bovinae): is there evidence of rapid evolution or reduced selective constraint in domestic cattle? BMC Genomics 10:179–193PubMedPubMedCentralCrossRefGoogle Scholar
  24. Mcclune DW, Kostka B, Delahay RJ, Montgomery WI, Marks NJ, Scantlebury DM (2015) Winter is coming: seasonal variation in resting metabolic rate of the European badger (Meles meles). PLoS One 10:e0135920PubMedPubMedCentralCrossRefGoogle Scholar
  25. Michaux JR, Hardy OJ, Justy F, Fournier P, Kranz A, Cabria M, Davison A, Rosoux R, Libois R (2010) Conservation genetics and population history of the threatened European mink Mustela lutreola, with an emphasis on the west European population. Mol Ecol 14:2373–2388CrossRefGoogle Scholar
  26. Moray C, Lanfear R, Bromham L (2014) Domestication and the mitochondrial genome: comparing patterns and rates of molecular evolution in domesticated mammals and birds and their wild relatives. Genome Biol Evol 6:161–169PubMedPubMedCentralCrossRefGoogle Scholar
  27. Nieminen P, Rouvinen WK, Saarela S, Mustonen AM (2007) Fasting in the American marten (Martes americana): a physiological model of the adaptations of a lean-bodied animal. J Comp Physiol B 177:787–795PubMedCrossRefPubMedCentralGoogle Scholar
  28. Palozzi JM, Jeedigunta SP, Hurd TR (2018) Mitochondrial DNA purifying selection in mammals and invertebrates. J Mol Biol 430:4834–4848PubMedCrossRefPubMedCentralGoogle Scholar
  29. Penny D (1992) The comparative method in evolutionary biology. J Classif 9:169–172CrossRefGoogle Scholar
  30. Pfeiffer P, Culik BM (1998) Energy metabolism of underwater swimming in river-otters (Lutra lutra L.). J Comp Physiol B 168:143–148PubMedCrossRefPubMedCentralGoogle Scholar
  31. Preston J (2007) Otters: ecology, behaviour and conservation. Q Rev Bio 82:288–289CrossRefGoogle Scholar
  32. Proulx G, Aubry K, Birks J, Buskirk S, Fortin C, Frost H, Krohn W, Mayo L, Monakhov V, Payer D 2005. World distribution and status of the genus Martes in 2000Google Scholar
  33. Rose J, Moore A, Russell A, Butcher M (2014) Functional osteology of the forelimb digging apparatus of badgers. J Mammal 95:543–558CrossRefGoogle Scholar
  34. Sato JJ, Wolsan M, Minami S, Hosoda T, Sinaga MH, Hiyama K, Yamaguchi Y, Suzuki H (2009) Deciphering and dating the red panda’s ancestry and early adaptive radiation of Musteloidea. Mol Phylogenet Evol 53:907–922PubMedCrossRefPubMedCentralGoogle Scholar
  35. Sato JJ, Wolsan M, Prevosti FJ, D’elía G, Begg C, Begg K, Hosoda T, Campbell KL, Suzuki H (2012) Evolutionary and biogeographic history of weasel-like carnivorans (Musteloidea). Mol Phylogenet Evol 63:745–757PubMedCrossRefPubMedCentralGoogle Scholar
  36. Schutz H, Guralnick RP (2010) Postcranial element shape and function: assessing locomotor mode in extant and extinct mustelid carnivorans. Zool J Linn Soc-Lond 150:895–914CrossRefGoogle Scholar
  37. Shen YY, Shi P, Sun YB, Zhang YP (2009) Relaxation of selective constraints on avian mitochondrial DNA following the degeneration of flight ability. Genome Res 19:1760–1765PubMedPubMedCentralCrossRefGoogle Scholar
  38. Sperl W, Jesina P, Zeman J, Mayr JA, Demeirleir L, Vancoster R, Pícková A, Hansíková H, Houst’Ková Hkrejcík Z (2006) Deficiency of mitochondrial ATP synthase of nuclear genetic origin. Neuromuscul Disord 16:821–829PubMedCrossRefPubMedCentralGoogle Scholar
  39. Sun YB, Shen YY, Irwin DM, Zhang YP (2011) Evaluating the roles of energetic functional constraints on teleost mitochondrial-encoded protein evolution. Mol Biol Evol 28:39–44PubMedCrossRefPubMedCentralGoogle Scholar
  40. Sun SE, Li Q, Kong L, Yu H (2017) Limited locomotive ability relaxed selective constraints on molluscs mitochondrial genomes. Sci Rep 7:10628–10636PubMedPubMedCentralCrossRefGoogle Scholar
  41. Wallace DC (2007) Why do we still have a maternally inherited mitochondrial DNA? Insights from evolutionary medicine. Annu Rev Biochem 76:781–821PubMedCrossRefPubMedCentralGoogle Scholar
  42. Wang Z, Yonezawa T, Liu B, Ma T, Shen X, Su J, Guo S, Hasegawa M, Liu J (2011) Domestication relaxed selective constraints on the yak mitochondrial genome. Mol Biol Evol 28:1553–1556PubMedCrossRefPubMedCentralGoogle Scholar
  43. Wang Y, Shen Y, Feng C, Zhao K, Song Z, Zhang Y, Yang L, He S (2016) Mitogenomic perspectives on the origin of Tibetan loaches and their adaptation to high altitude. Sci Rep 6:29690–29700PubMedPubMedCentralCrossRefGoogle Scholar
  44. Williams TM (1983) Locomotion in the north American mink, a semi-aquatic mammal. II The effect of an elongate body on running energetics and gait patterns. J Exp Biol 103:283–295Google Scholar
  45. Xu S, Luo SJ, Sang H (2007) High altitude adaptation and phylogenetic analysis of Tibetan horse based on the mitochondrial genome. J Genet Genomics 34:720–729PubMedCrossRefGoogle Scholar
  46. Yang ZH (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591PubMedCrossRefPubMedCentralGoogle Scholar
  47. Yang ZH, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496–503PubMedCrossRefPubMedCentralGoogle Scholar
  48. Zhang S, Han J, Zhong D, Wang T (2013) Analysis of selective constraints on mitochondrial DNA, flight ability and physiological index on avian. IEEE Eng Med Biol 35:1498–1501Google Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2019

Authors and Affiliations

  1. 1.College of Life ScienceQufu Normal UniversityQufuChina

Personalised recommendations