Abstract
Mitochondrial DNA (mtDNA) encodes for proteins mainly involved in the oxidative phosphorylation process, and due to its molecular features, it is one of the most used molecular markers for phylogenetic and taxonomic purposes. Since mitochondria are the primary source of energy for aerobic organisms, it has been suggested that modifications of the mitochondrial genome’s features could be linked with major adaptive processes to particular environmental conditions. In this respect, Antarctic Collembola (springtails) may be considered an interesting model to study whether positive selective pressure has occurred, inducing significant changes in the mtDNA characteristics that have eventually led to cold adaptation. In this study, we describe the molecular features of the mitochondrial genome of Cryptopygus terranovus, a springtail species endemic to Victoria Land. Molecular data are also employed to support the new taxonomic placement of C. terranovus, and to establish if the conspecific lineages of Friesea antarctica, that lives in separated biogeographical regions of the Antarctic Continent, are indeed distinct species. Finally, all the mitochondrial genomes of springtails, so far sequenced, were applied for calculating the ratio (ω) of nonsynonymous versus synonymous nucleotide substitutions. This approach allowed us to investigate if Antarctic collembolans could have experienced Darwinian selective pressures compared to the non-Antarctic springtail species. Indeed, our data does indicate positive selection (ω > 1), suggesting that survival at extreme environmental conditions could be also related to mtDNA modifications.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ballard JWO, Kreitman M (1995) Is mitochondrial DNA a strictly neutral marker? Trends Ecol Evol 10:485–488. https://doi.org/10.1016/S0169-5347(00)89195-8
Beet CR, Hogg ID, Collins GE, Cowan DA, Wall DH, Adams BJ (2016) Genetic diversity among populations of Antarctic springtails (Collembola) within the Mackay Glacier ecotone. Genome 59:762–770. https://doi.org/10.1139/gen-2015-0194
Bennet KR, Hogg ID, Adams BJ, Hebert PDN (2016) High levels of intraspecific genetic divergence revealed for Antarctic springtails: evidence for small-scale isolation during Pleistocene glaciation. Biol J Linn Soc 119:166–178. https://doi.org/10.1111/bij.12796
Blier PU, Dufresne F, Burton RS (2001) Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet 17:400–406. https://doi.org/10.1016/S0168-9525(01)02338-1
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780. https://doi.org/10.1093/nar/27.8.1767
Brower AV (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patters of mitochondrial DNA evolution. Proc Natl Acad Sci USA 91:6491–6495. https://doi.org/10.1073/pnas.91.14.6491
Carapelli A, Comandi S, Convey P, Nardi F, Frati F (2008) The complete mitochondrial genome of the Antarctic springtail Cryptopygus antarcticus (Hexapoda: Collembola). BMC Genomics 9:315. https://doi.org/10.1186/1471-2164-9-315
Carapelli A, Convey P, Nardi F, Frati F (2014) The mitochondrial genome of the antarctic springtail Folsomotoma octooculata (Hexapoda; Collembola), and an update on the phylogeny of collembolan lineages based on mitogenomic data. Entomologia 2:190. https://doi.org/10.4081/entomologia.2014.190
Carapelli A, Leo C, Frati F (2017) High levels of genetic structuring in the Antarctic springtail Cryptopygus terranovus. Antarct Sci 29:311–323. https://doi.org/10.1017/S0954102016000730
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Clark MS, Thorne MAS, Purać J, Burns G, Hillyard G, Popović ZD, Grubor-Lajšić G, Worland RM (2009) Surviving the cold: molecular analyses of insect cryoprotective dehydration in the Arctic springtail Megaphorura arctica (Tullberg). BMC Genomics 10:328. https://doi.org/10.1186/1471-2164-10-328
Collins GE, Hogg ID (2016) Temperature-related activity of Gomphiocephalus hodgsoni (Collembola) mitochondrial DNA (COI) haplotypes in Taylor Valley, Antarctica. Polar Biol 39:379–389. https://doi.org/10.1007/s00300-015-1788-7
Comandi S, Carapelli A, Podsiadlowski L, Nardi F, Frati F (2009) The complete mitochondrial genome of Atelura formicaria (Hexapoda: Zygentoma) and the phylogenetic relationships of basal insects. Gene 439:25–34. https://doi.org/10.1016/j.gene.2009.02.020
Consuegra S, John E, Verspoor E, de Leaniz CG (2015) Patterns of natural selection acting on the mitochondrial genome of a locally adapted fish species. Genet Sel Evol 47:58. https://doi.org/10.1186/s12711-015-0138-0
Cook CE, Yue Q, Akam M (2005) Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Philos T R Soc Lond B Biol Sci 272:1295–1304. https://doi.org/10.1098/rspb.2004.3042
De Rijk P, Wuyts J, De Wachter R (2003) RnaViz2: an improved representation of RNA secondary structure. Bioinformatics 19:299–300. https://doi.org/10.1093/bioinformatics/19.2.299
Deepak J, Nidhin B, Anil Kumar KP, Pradeep PJ, Harikrishnan M (2016) A molecular approach towards the taxonomy of fresh water prawns Macrobrachium striatum and M. equidens (Decapoda, Palaemonidae) using mitochondrial markers. Mitochondr DNA Part A 27:2585–2593. https://doi.org/10.3109/19401736.2015.1041114
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxydase subunit I from diverse metazoan invertebrate. Mol Mar Biol Biotech 3:294–299
Frati F, Fanciulli PP, Carapelli A, Dallai R (1997) The Collembola of northern Victoria Land (Antarctica): distribution and ecological remarks. Pedobiologia 41:50–55
Garvin MR, Bielawski JP, Gharrett AJ (2011) Positive Darwinian selection in the piston that powers proton pumps in complex I of the mitochondria of Pacific salmon. PLoS ONE 6:e24127. https://doi.org/10.1371/journal.pone.0024127
Gillespie JJ, Johnston JS, Cannone JJ, Gutell RR (2006) Characteristics of the nuclear (18S, 5.8S, 28S and 5S) and mitochondrial (12S and 16S) rRNA genes of Apis mellifera (Insecta: Hymenoptera): structure, organization, and retrotransposable elements. Insect Mol Biol 15:657–686. https://doi.org/10.1111/j.1365-2583.2006.00689.x
Gnaiger E, Boushel R, Søndergaard H et al (2015) Mitochondrial coupling and capacity of oxidative phosphorylation in skeletal muscle of Inuit and Caucasians in the arctic winter. Scand J Med Sci Sports 25:126–134. https://doi.org/10.1111/sms.12612
Greenslade P (1995) Collembola from the Scotia Arc and Antarctic Peninsula including descriptions of two new species and notes on biogeography. Polskie Pismo Entomol 64:305–319
Greenslade P (2015) Synonymy of two monobasic Anurophorinae genera (Collembola: Isotomidae) from the Antarctic Continent. N Z Entomol 38:134–141. https://doi.org/10.1080/00779962.2015.1033810
Greenslade P (2018) An Antarctic biogeographical anomaly resolved: the true identity of a widespread species of Collembola. Polar Biol 41:969–981. https://doi.org/10.1007/s00300-018-2261-1
Hassanin A, Léger N, Deutsch J (2005) Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. Syst Biol 54:277–298. https://doi.org/10.1080/10635150590947843
Hassanin A, Ropiquet A, Couloux A, Cruaud C (2009) Evolution of the mitochondrial genome in mammals living at high altitude: new insight from a study of the tribe Caprini (Bovidae, Antilopinae). J Mol Evol 68:293–310. https://doi.org/10.1007/s00239-009-9208-7
Hawes TC, Torricelli G, Stevens MI (2010) Haplotype diversity in the Antarctic springtail Gressittacantha terranova at fine spatial scale—a Holocene twist to a Pliocene tale. Antarct Sci 22:766–773. https://doi.org/10.1017/S0954102010000490
Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773. https://doi.org/10.1093/molbev/msw260
Laslett D, Canbäck B (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24:172–175. https://doi.org/10.1093/bioinformatics/btm573
Lewis AR, Marchant DR, Ashworth AC et al (2008) Mid-Miocene cooling and the extinction of the tundra in continental Antarctica. PNAS 105:10676–10680. https://doi.org/10.1073/pnas.0802501105
Lozano-Fernandez J, Carton R, Tanner AR, Puttick MN, Blaxter M, Vinther J, Olesen J, Giribet G, Edgecombe GD, Pisani D (2016) A molecular palaeobiological exploration of arthropod terrestrialization. Philos Trans R Soc Lond B Biol Sci 371:20150133. https://doi.org/10.1098/rstb.2015.0133
Maddison DR, Maddison WP (2005) MacClade 4: analysis of phylogeny and character evolution, version 4.08a. Sinauer Associates, Sunderland, MA
Maunsell SC, Kitching RL, Greenslade P, Nakamura A, Burwell CJ (2013) Springtail (Collembola) assemblages along an elevational gradient in Australian subtropical rainforest. Aust J Entomol 52:114–212. https://doi.org/10.1111/aen.12012
McGaughran A, Stevens MI, Holland BR (2010) Biogeography of circum-Antarctic springtails. Mol Phylogenet Evol 57:48–58. https://doi.org/10.1016/j.ympev.2010.06.003
McGaughran A, Stevens MI, Hogg ID, Carapelli A (2011) Extreme glacial legacies: a synthesis of the Antarctic springtail phylogeographic record. Insects 2:62–82. https://doi.org/10.3390/insects2020062
Meiklejohn CD, Montooth KL, Rand DM (2007) Positive and negative selection on the mitochondrial genome. Trends Genet 23(6):259–263. https://doi.org/10.1016/j.tig.2007.03.008
Melo-Ferreira J, Vilela J, Fonseca MM, da Fonseca R, Boursot P, Alves PC (2014) The elusive nature of adaptive mitochondrial DNA evolution of an Arctic lineage prone to frequent introgression. Genome Biol Evol 6:886–896. https://doi.org/10.1093/gbe/evu059
Nardi F, Spinsanti G, Boore JL, Carapelli A, Dallai R, Frati F (2003) Hexapod origins: monophyletic or paraphyletic? Science 299:1887–1889. https://doi.org/10.1126/science.1078607
Podsiadlowski L, Carapelli A, Nardi F, Dallai R, Koch M, Frati Boore JL, F, (2006) The mitochondrial genomes of Campodea fragilis and Campodea lubbocki (Hexapoda: Diplura): High genetic divergence in a morphologically uniform taxon. Gene 381:49–61. https://doi.org/10.1016/j.gene.2006.06.009
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701. https://doi.org/10.1093/aesa/87.6.651
Simon C, Buckley T, Frati F, Stewart J, Beckenbach A (2006) Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Annu Rev Ecol Ecol S 37:545–579. https://doi.org/10.1146/annurev.ecolsys.37.091305.110018
Sinclair BJ, Vernon P, Klok CJ, Chown SL (2003) Insects at low temperatures: an ecological perspective. Trends Ecol Evol 18:257–262. https://doi.org/10.1016/S0169-5347(03)00014-4
Sinclair BJ, Stevens MI (2006) Terrestrial microarthropods of Victoria Land and Queen Maud Mountains, Antarctica: implications of climate change. Soil Biol Biochem 38:3158–3170. https://doi.org/10.1016/j.soilbio.2005.11.035
Stevens MI, Greenslade P, Hogg ID, Sunnucks P (2006) Examining Southern Hemisphere springtails: could any have survived glaciation of Antarctica? Mol Biol Evol 23:874–882. https://doi.org/10.1093/molbev/msj073
Stevens MI, D’Haese CA (2017) Morphologically tortured: taxonomic placement of an Antarctic springtail (Collembola: Isotomidae) misguided by morphology and ecology. Zool Scr 46:180–187. https://doi.org/10.1111/zsc.12204
Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (*and other methods., version 4. Sinauer Associates, Sunderland, MA
Talbot DA, Duchamp C, Rey B, Hanuise N, Rouanet JL, Sibille B, Brand MD (2004) Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins. J Phisiol 558:123–135. https://doi.org/10.1113/jphysiol.2004.063768
Taylor RW, Turnbull DM (2005) Mitochondrial DNA mutation in human disease. Nat Rev Genet 6:389–402. https://doi.org/10.1038/nrg1606
Torricelli G, Frati F, Convey P, Telford M, Carapelli A (2010a) Population structure of Friesea grisea (Collembola, Neanuridae) in the Antarctic Peninsula and Victoria Land: evidence for local genetic differentiation of pre-Pleistocene origin. Antarct Sci 22:757–765. https://doi.org/10.1017/S0954102010000775
Torricelli G, Carapelli A, Convey P, Nardi F, Boore JL, Frati F (2010b) High divergence across the whole mitochondrial genome in the "pan-Antarctic" springtail Friesea grisea: Evidence for cryptic species? Gene 449:30–40. https://doi.org/10.1016/j.gene.2009.09.006
Wallace DC (2010) Mitochondrial DNA in disease and aging. Environ Mol Mutagen 51:440–450. https://doi.org/10.1002/em.20586
Wang Z, Shi X, Sun L, Bai Y, Zhang D, Tang B (2017) Evolution of mitochondrial energy metabolism genes associated with hydrothermal vent adaption of alvinocaridid shrimps. Genes Genom 39:1367–1376. https://doi.org/10.1007/s13258-017-0600-1
Wernersson R, Pedersen AG (2003) RevTrans: constructing alignments of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31:3527–3539. https://doi.org/10.1093/nar/gkg609
Willem V (1902) Les collemboles recueillis par l’expédition antarctique belge. Ann Soc Entomol Belgium 45:260–262
Wise KAJ (1967) Collembola (springtails). Antarct Res S 10:123–148
Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524. https://doi.org/10.1046/j.0269-8463.2001.00547.x
Yang Z, Wong WSW, Nielsen R (2005) Bayes Empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118. https://doi.org/10.1093/molbev/msi097
Yang Z (2006) Computational molecular evolution. Oxford University Press, Oxford, May PHaRM
Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. https://doi.org/10.1093/molbev/msm088
Yang Z, Nielsen R (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19:908–917. https://doi.org/10.1093/oxfordjournals.molbev.a004148
Ying W, Qing-Song Z, Hui-Jie Q, Ai-Bing Z, Fang Y, Xu-Bo W, Chao-Dong Z, Yan-Zhou Z (2016) Formal nomenclature and description of cryptic species of the Encyrtus sasakii complex (Hymenoptera: Encyrtidae). Sci Rep-UK 6:34372. https://doi.org/10.1038/srep34372
Zhang B, Zhang YH, Wang X, Zhang HX, Lin Q (2017) The mitochondrial genome of a sea anemone Bolocera sp. exhibits novel genetic structures potentially involved in adaptation to the deep-sea environment. Ecol Evol 7:4951–4962. https://doi.org/10.1002/ece3.3067
Zhang F, Jantarit S, Nilsai A, Stevens MI, Ding Y, Satasook C (2018) Species delimitation in the morphologically conserved Coecobrya (Collembola: Entomobryidae): a case study integrating morphology and molecular traits to advance current taxonomy. Zool Scr 47:342–356. https://doi.org/10.1111/zsc.12279
Acknowledgements
This work was funded by: the Italian Program of Research in Antarctica (PNRA16_00234), and the Italian MIUR (PRIN). Partial support was also provided by the University of Siena. All Authors declare no conflict of interest and approved the performed research and the draught of the manuscript. We would like to kindly thank the anonymous Referee, Professor Mark Stevens and Professor Bettine van Vuuren for their important help in improving the present manuscript.
Author information
Authors and Affiliations
Contributions
A.C. collected the material, performed the molecular and bioinformatics analyses and drafted the manuscript; C.L. performed the experiments of the molecular and part of the bioinformatics analyses, and contributed to the drafting of the manuscript. P.P.F. and F.F. contributed to the draught of the manuscript.
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
300_2019_2466_MOESM1_ESM.pdf
Table S1. List of complete (or almost complete) springtail mtDNA available on GenBank and their accession numbers. On GenBank, the species Friesea antarctica is still identified as Friesea grisea; the accession numbers provided in the table are referred to specimens previously identified as F. grisea. AP = Antarctic Peninsula; VL = Victoria Land. Supplementary material 1 (PDF 15 kb)
300_2019_2466_MOESM2_ESM.pdf
Table S2: P-distance matrix among the cox1 sequences of the 13 springtails species included in all the analyses of the current study plusCryptopygus cisantarcticus. The divergence matrix was used to estimate the time of divergence among the Isotomidae and the two F. antarctica (AP and VL). Supplementary material 1 (PDF 14 kb)
Rights and permissions
About this article
Cite this article
Carapelli, A., Fanciulli, P., Frati, F. et al. Mitogenomic data to study the taxonomy of Antarctic springtail species (Hexapoda: Collembola) and their adaptation to extreme environments. Polar Biol 42, 715–732 (2019). https://doi.org/10.1007/s00300-019-02466-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-019-02466-8