Exploring Cold Hardiness within a Butterfly Clade: Supercooling Ability and Polyol Profiles in European Satyrinae
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
GA19-15031S
Grant Agency of the Czech Republic
TAČR SS01010526
Technology Agency of the Czech Republic
PubMed
35447811
PubMed Central
PMC9031891
DOI
10.3390/insects13040369
PII: insects13040369
Knihovny.cz E-zdroje
- Klíčová slova
- Lepidoptera: Nymphalidae, butterfly physiology, carbohydrate, cold hardiness, cryoprotectants, elevation, mountains, temperate zone, winter survival,
- Publikační typ
- časopisecké články MeSH
The cold hardiness of overwintering stages affects the distribution of temperate and cold-zone insects. Studies on Erebia, a species-rich cold-zone butterfly genus, detected unexpected diversity of cold hardiness traits. We expanded our investigation to eight Satyrinae species of seven genera. We assessed Autumn and Winter supercooling points (SCPs) and concentrations of putatively cryoprotective sugars and polyols via gas chromatography-mass spectrometry. Aphantopus hyperantus and Hipparchia semele survived freezing of body fluids; Coenonympha arcania, C. gardetta, and Melanargia galathea died prior to freezing; Maniola jurtina, Chazara briseis, and Minois dryas displayed a mixed response. SCP varied from -22 to -9 °C among species. Total sugar and polyol concentrations (TSPC) varied sixfold (2 to 12 μg × mg-1) and eightfold including the Erebia spp. results. SCP and TSPC did not correlate. Alpine Erebia spp. contained high trehalose, threitol, and erythritol; C. briseis and C. gardetta contained high ribitol and trehalose; lowland species contained high saccharose, maltose, fructose, and sorbitol. SCP, TSPC, and glycerol concentrations were affected by phylogeny. Species of mountains or steppes tend to be freeze-avoidant, overwinter as young larvae, and contain high concentrations of trehalose, while those of mesic environments tend to be freeze-tolerant, overwinter as later instars, and rely on compounds such as maltose, saccharose, and fructose.
Faculty of Science University of South Bohemia Branišovská 31 370 05 České Budějovice Czech Republic
Zobrazit více v PubMed
Sauer J., Domisch S., Nowak C., Haase P. Low mountain ranges: Summit traps for montane freshwater species under climate change. Biodivers. Conserv. 2011;20:3133–3146. doi: 10.1007/s10531-011-0140-y. DOI
McCain C.M., Garfinkel C.F. Climate change and elevational range shifts in insects. Curr. Opin. Insect Sci. 2021;47:111–118. PubMed
Sistri G., Menchetti M., Santini L., Pasquali L., Sapienti S., Cini A., Platania L., Balletto E., Barbero F., Bonelli S., et al. The isolated Erebia pandrose Apennine population is genetically unique and endangered by climate change. Insect Conserv. Divers. 2022;15:136–148. doi: 10.1111/icad.12538. DOI
Matter S.F., Doyle A., Illerbrun K., Wheeler J., Roland J. An assessment of direct and indirect effects of climate change for populations of the Rocky Mountain Apollo butterfly (Parnassius smintheus Doubleday) Insect Sci. 2011;18:385–392. doi: 10.1111/j.1744-7917.2011.01407.x. DOI
Abarca M., Larsen E.A., Ries L. Heatwaves and Novel Host Consumption Increase Overwinter Mortality of an Imperiled Wetland Butterfly. Front. Ecol. Evol. 2019;7:193. doi: 10.3389/fevo.2019.00193. DOI
Roland J., Filazzola A., Matter S.F. Spatial variation in early-winter snow cover determines local dynamics in a network of alpine butterfly populations. Ecography. 2020;44:334–343. doi: 10.1111/ecog.05407. DOI
Konvicka M., Kuras T., Liparova J., Slezak V., Horazna D., Klecka J., Kleckova I. Low winter precipitation, but not warm autumns and springs, threatens mountain butterflies in middle-high mountains. PeerJ. 2021;9:12021. doi: 10.7717/peerj.12021. PubMed DOI PMC
Klockmann M., Fischer K. Strong reduction in diapause survival under warm and humid overwintering conditions in a temperate-zone butterfly. Popul. Ecol. 2019;61:150–159. doi: 10.1002/1438-390X.1016. DOI
Kuras T., Benes J., Fric Z., Konvicka M. Dispersal patterns of endemic alpine butterflies with contrasting population structures: Erebia epiphron and E. sudetica. Popul. Ecol. 2003;45:115–123. doi: 10.1007/s10144-003-0144-x. DOI
Sonderegger P. Die Erebien der Schweiz (Lepidoptera: Satyrinae, Genus Erebia) Verlag Peter Sonderegger; Biel/Bienne, Switzerland: 2005. 712p
Schmitt T., Habel J.C., Rodder D., Louy D. Effects of recent and past climatic shifts on the genetic structure of the high mountain Yellow-spotted ringlet butterfly Erebia manto (Lepidoptera, Satyrinae): A conservation problem. Global Change Biol. 2014;20:2045–2061. doi: 10.1111/gcb.12462. PubMed DOI
Pena C., Witthauer H., Kleckova I., Fric Z., Wahlberg N. Adaptive radiations in butterflies: Evolutionary history of the genus Erebia (Nymphalidae: Satyrinae) Biol. J. Linn. Soc. 2015;116:449–467. doi: 10.1111/bij.12597. DOI
Ehl S., Dalstein V., Tull F., Gros P., Schmitt T. Specialized or opportunistic-how does the high mountain endemic butterfly Erebia nivalis survive in its extreme habitats? Insect Sci. 2018;25:161–171. PubMed
Vrba P., Konvicka M., Nedved O. Reverse altitudinal cline in cold hardiness among Erebia butterflies. CryoLetters. 2012;33:251–258. PubMed
Vrba P., Nedved O., Zahradnickova H., Konvicka M. More complex than expected: Cold hardiness and the concentration of cryoprotectants in overwintering larvae of five Erebia butterflies (Lepidoptera: Nymphalidae) Eur. J. Entomol. 2017;114:470–480. doi: 10.14411/eje.2017.060. DOI
Williams C.M., Nicolai A., Ferguson L.V., Bernards M.A., Hellmann J.J., Sinclair B.J. Cold hardiness and deacclimation of overwintering Papilio zelicaon pupae. Comp. Biochem. Physiol. A. 2014;178:51–58. doi: 10.1016/j.cbpa.2014.08.002. PubMed DOI
Chazot N., Condamine F.L., Dudas G., Pena C., Kodandaramaiah U., Matos-Maravi P., Aduse-Poku K., Elias M., Warren A.D., Lohman D.J., et al. Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies. Nat. Comm. 2021;12:5717. doi: 10.1038/s41467-021-25906-8. PubMed DOI PMC
Kleckova I., Konvicka M., Klecka J. Thermoregulation and microhabitat use in mountain butterflies of the genus Erebia: Importance of fine-scale habitat heterogeneity. J. Therm. Biol. 2014;41:50–58. doi: 10.1016/j.jtherbio.2014.02.002. PubMed DOI
Zachariassen K.E. Physiology of cold tolerance in insects. Physiol. Rev. 1985;65:799–832. doi: 10.1152/physrev.1985.65.4.799. PubMed DOI
Ramlov H., Bedford J., Leader J. Freezing tolerance of the New Zealand weta, Hemideina maori Hutton (Orthoptera, Stenopelmatidae) J. Therm. Biol. 1992;17:51–54. doi: 10.1016/0306-4565(92)90019-C. DOI
Sinclair B.J., Vernon P., Klok C.J., Chown S.L. Insects at low temperatures: An ecological perspective. Trends Ecol. Evol. 2003;18:257–262. doi: 10.1016/S0169-5347(03)00014-4. DOI
Sinclair B.J., Alvarado L.E.C., Ferguson L.V. An invitation to measure insect cold tolerance: Methods, approaches, and workflow. J. Therm. Biol. 2015;53:180–197. doi: 10.1016/j.jtherbio.2015.11.003. PubMed DOI
Nedved O. Modelling the relationship between cold injury and accumulated degree days in terrestrial arthropods. Cryo-Lett. 1998;19:267–274.
Vrba P., Nedved O., Konvicka M. Contrasting Supercooling Ability in Lowland and Mountain European Colias Butterflies. J. Entomol. Sci. 2014;49:63–69. doi: 10.18474/0749-8004-49.1.63. DOI
Somme L. Supercooling and winter survival in terrestrial arthropods. Comp. Biochem. Physiol. A. 1982;73:519–543. doi: 10.1016/0300-9629(82)90260-2. DOI
Ramlov H. Aspects of natural cold tolerance in ectothermic animals. Hum. Reprod. 2000;15:26–46. doi: 10.1093/humrep/15.suppl_5.26. PubMed DOI
Kostal V., Slachta M., Simek P. Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocotis apterus (Heteroptera: Insecta) Comp. Biochem. Phys. B. 2001;130:365–374. doi: 10.1016/S1096-4959(01)00441-9. PubMed DOI
Kadlec T., Vrba P., Kepka P., Schmitt T., Konvicka M. Tracking the decline of the once-common butterfly: Delayed oviposition, demography and population genetics in the hermit Chazara briseis. Anim. Conserv. 2010;13:172–183. doi: 10.1111/j.1469-1795.2009.00318.x. DOI
Suchackova Bartonova A., Konvicka M., Maresova J., Blahova D., Cip D., Skala P., Andres M., Hula V., Dolek M., Geyer A., et al. Extremely Endangered Butterflies of Scattered Central European Dry Grasslands Under Current Habitat Alteration. Insect Syst. Divers. 2021;5:6. doi: 10.1093/isd/ixab017. DOI
Kadlec T., Vrba P. A second generation of Coenonympha arcania (Linnaeus, 1761) in northern Bohemia, Czech Republic (Lepidoptera, Satyrinae) Atalanta. 2007;38:181–183.
Kodandaramaiah U., Wahlberg N. Phylogeny and biogeography of Coenonympha butterflies (Nymphalidae: Satyrinae)—patterns of colonization in the Holarctic. Syst. Entomol. 2009;34:315–323. doi: 10.1111/j.1365-3113.2008.00453.x. DOI
Wiemers M., Schweiger O., Harpke A., Settele J. Climatic niche characteristics of the butterflies in Europe (CLIMBER)—A new database for measuring the response of butterflies to climatic changes. Zitteliana. 2016;88:53.
Tropek R., Cizek O., Kadlec T., Klecka J. Habitat use of Hipparchia semele (Lepidoptera) in its artificial stronghold: Necessity of the resource-based habitat view in restoration of disturbed sites. Pol. J. Ecol. 2017;65:385–399.
Kalarus K., Nowicki P. How Do Landscape Structure, Management and Habitat Quality Drive the Colonization of Habitat Patches by the Dryad Butterfly (Lepidoptera: Satyrinae) in Fragmented Grassland? PLoS ONE. 2015;10:e0138557. doi: 10.1371/journal.pone.0138557. PubMed DOI PMC
Hanson A.A., Venette R.C. Thermocouple design for measuring temperatures of small insects. CryoLetters. 2013;34:261–266. PubMed
Brunnhofer V., Nedved O., Hodkova M. Methodical improvement for measuring of supercooling point in insects. Acta Entomol. Bohemoslov. 1991;88:349–350.
Kostal V., Zahradnickova H., Simek P., Zeleny J. Multiple component system of sugars and polyols in the overwintering spruce bark beetle, Ips typographus. J. Insect Physiol. 2007;53:580–586. doi: 10.1016/j.jinsphys.2007.02.009. PubMed DOI
Ter Braak C.J.F., Smilauer P. Canoco 5, Windows Release (5.00) 2013. [(accessed on 1 September 2019)]. Available online: http://www.canoco5.com/
Blomberg S.P., Garland T., Ives A.R. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution. 2003;57:717–745. doi: 10.1111/j.0014-3820.2003.tb00285.x. PubMed DOI
Revell L.J. Phytools: Phylogenetic tools for comparative biology (and other things) Methods Ecol. Evol. 2012;3:217–223. doi: 10.1111/j.2041-210X.2011.00169.x. DOI
Paradis E., Claude J., Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20:289–290. doi: 10.1093/bioinformatics/btg412. PubMed DOI
Legendre P., Galzin R., Harmelin-Vivien M.L. Relating behavior to habitat: Solutions to the fourth-corner problem. Ecology. 1997;78:547–562. doi: 10.2307/2266029. DOI
Pena C., Nylin S., Freitas A.V.L. Higher level phylogeny of Satyrinae butterflies (Lepidoptera: Nymphalidae) based on DNA sequence data. Mol. Phylogenet. Evol. 2006;40:29–49. doi: 10.1016/j.ympev.2006.02.007. PubMed DOI
Walters K.R., Jr., Pan Q., Serianni A.S., Duman J.G. Cryoprotectant Biosynthesis and the Selective Accumulation of Threitol in the Freeze-tolerant Alaskan Beetle, Upis ceramboides. J. Biol. Chem. 2009;284:16822–16831. doi: 10.1074/jbc.M109.013870. PubMed DOI PMC
Van der Merwe M., Chown S.L., Smith V.R. Thermal tolerance limits in six weevil species (Coleoptera, Curculionidae) from sub-Antarctic Marion Island. Polar Biol. 1997;18:331–336. doi: 10.1007/s003000050196. DOI
Vernon P., Vannier G. Freezing susceptibility and freezing tolerance in Palaearctic Cetoniidae (Coleoptera) Can. J. Zool. 2001;79:67–74. doi: 10.1139/z00-168. DOI
Ditrich T., Kostal V. Comparative analysis of overwintering physiology in nine species of semi-aquatic bugs (Heteroptera: Gerromorpha) Physiol. Entomol. 2011;36:261–270. doi: 10.1111/j.1365-3032.2011.00794.x. DOI
Strachan L.A., Tarnowski-Garner H.E., Marshall K.E., Sinclair B.J. The Evolution of Cold Tolerance in Drosophila Larvae. Physiol. Biochem. Zool. 2011;84:43–53. doi: 10.1086/657147. PubMed DOI
Andersen J.L., Manenti T., Sorensen J.G., MacMillan H.A., Loeschcke V., Overgaard J. How to assess Drosophila cold tolerance: Chill coma temperature and lower lethal temperature are the best predictors of cold distribution limits. Funct. Ecol. 2015;29:55–65. doi: 10.1111/1365-2435.12310. DOI
Dennis A.B., Dunning L.T., Sinclair B.J., Buckley T.R. Parallel molecular routes to cold adaptation in eight genera of New Zealand stick insects. Sci. Rep. 2015;5:13965. doi: 10.1038/srep13965. PubMed DOI PMC
Albre J., Gers C., Legal L. Molecular phylogeny of the Erebia tyndarus (Lepidoptera, Rhopalocera, Nymphalidae, Satyrinae) species group combining CoxII and ND5 mitochondrial genes: A case study of a recent radiation. Mol. Phylogenet. Evol. 2008;47:196–210. doi: 10.1016/j.ympev.2008.01.009. PubMed DOI
Pena C., Nylin S., Wahlberg N. The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): A challenge for phylogenetic methods. Zool. J. Linn. Soc. 2011;161:64–87. doi: 10.1111/j.1096-3642.2009.00627.x. DOI
Sinclair B.J., Addo-Bediako A., Chown S.L. Climatic variability and the evolution of insect freeze tolerance. Biol. Rev. 2003;78:181–195. doi: 10.1017/S1464793102006024. PubMed DOI
Zachariassen K.E. The role of polyols and nucleating agents in cold hardy beetles. J. Comp. Physiol. 1980;140:227–234. doi: 10.1007/BF00690407. DOI
Wallis deVries M.F., Baxter W., Van Vliet A.J.H. Beyond climate envelopes effects of weather on regional population trends in butterflies. Oecologia. 2011;167:559–571. doi: 10.1007/s00442-011-2007-z. PubMed DOI PMC
Oliver T.H., Marshall H.H., Morecroft M.D., Brereton T., Prudhomme C., Huntingford C. Interacting effects of climate change and habitat fragmentation on drought-sensitive butterflies. Nat. Clim. Change. 2015;5:941–945. doi: 10.1038/nclimate2746. DOI
Stuhldreher G., Hermann G., Fartmann T. Cold-adapted species in a warming world—An explorative study on the impact of high winter temperatures on a continental butterfly. Entomol. Exp. Appl. 2014;151:270–279. doi: 10.1111/eea.12193. DOI
Slamova I., Klecka J., Konvicka M. Diurnal Behavior and Habitat Preferences of Erebia aethiops, an Aberrant Lowland Species of a Mountain Butterfly Clade. J. Insect Behav. 2011;24:230–246. doi: 10.1007/s10905-010-9250-8. DOI
Kulfan J., Strbova E., Zach P. Effect of vegetation and management on occurrence of larvae and adults of generalist Maniola jurtina L. (Lepidoptera) in meadow habitats. Pol. J. Ecol. 2012;60:601–609.
Villemey A., Peterman W.E., Richard M., Ouin A., van Halder I., Stevens V.M., Baguette M., Roche P., Archaux F. Butterfly dispersal in farmland: A replicated landscape genetics study on the meadow brown butterfly (Maniola jurtina) Landsc. Ecol. 2016;31:1629–1641. doi: 10.1007/s10980-016-0348-z. DOI
Li N.G., Toxopeus J., Moos M., Sorensen J.G., Sinclair B.J. A comparison of low temperature biology of Pieris rapae from Ontario, Canada, and Yakutia, Far Eastern Russia. Comp. Biochem. Phys. A. 2020;242:1106492. doi: 10.1016/j.cbpa.2020.110649. PubMed DOI
Kock R.A., Orynbayev M., Robinson S., Zuther S., Singh N.J., Beauvais W., Morgan E.R., Kerimbayev A., Khomenko S., Martineau H.M., et al. Saigas on the brink: Multidisciplinary analysis of the factors influencing mass mortality events. Sci. Adv. 2018;4:aao231. doi: 10.1126/sciadv.aao2314. PubMed DOI PMC
Kleckova I., Klecka J. Facing the Heat: Thermoregulation and Behaviour of Lowland Species of a Cold-Dwelling Butterfly Genus, Erebia. PLoS ONE. 2016;11:e0150393. doi: 10.1371/journal.pone.0150393. PubMed DOI PMC
Pullin A.S., Bale J.S., Fontaine X.L.R. Physiological aspects of diapause and cold tolerance during overwintering in Pieris brassicae. Physiol. Entomol. 1991;16:447–456. doi: 10.1111/j.1365-3032.1991.tb00584.x. DOI
Lehmann P., Pruisscher P., Kostal V., Moos M., Simek P., Nylin S., Agren R., Varemo L., Wiklund C., Wheat C.W., et al. Metabolome dynamics of diapause in the butterfly Pieris napi: Distinguishing maintenance, termination and post-diapause phases. J. Exp. Biol. 2018;221:jeb169508. doi: 10.1242/jeb.169508. PubMed DOI
Pullin A.S., Bale J.S. Effects of low temperature on diapausing Aglais urticae and Inachis io (Lepidoptera, Nymphalidae)—overwintering physiology. J. Insect Physiol. 1989;35:283–290. doi: 10.1016/0022-1910(89)90076-0. DOI
Vrba P., Dolek M., Nedved O., Zahradnickova H., Cerrato C., Konvicka M. Overwintering of the boreal butterfly Colias palaeno in central Europe. CryoLetters. 2014;35:247–254. PubMed
Ahmadi B., Moharramipour S., Sinclair B.J. Overwintering biology of the carob moth Apomyelois ceratoniae (Lepidoptera: Pyralidae) Int. J. Pest Manag. 2016;62:69–74. doi: 10.1080/09670874.2015.1102984. DOI
Han E.N., Bauce E. Non-freeze survival of spruce budworm larvae, Choristoneura fumiferana, at subzero temperatures during diapause. Entomol. Exp. Appl. 1995;75:67–74. doi: 10.1111/j.1570-7458.1995.tb01911.x. DOI
Toxopeus J., Kostal V., Sinclair B.J. Evidence for non-colligative function of small cryoprotectants in a freeze-tolerant insect. Proc. R. Soc. B Biol. 2019;286:20190050. doi: 10.1098/rspb.2019.0050. PubMed DOI PMC
Vrba P., Nedved O., Zahradnickova H., Konvicka M. Temporal plasticity in cold hardiness and cryoprotectant contents in northern versus temperate Colias butterflies (Lepidoptera: Pieridae) CryoLetters. 2017;38:330–338. PubMed
Li J.W., Shi J., Xue Y., Mao H.B., Luo Y.Q. Major physiological adjustments in freezing-tolerant grey tiger longicorn beetle (Xylotrechus rusticus) during overwintering period. J. Forest. Res. 2014;25:653–659. doi: 10.1007/s11676-014-0504-8. DOI
Hasanvand H., Izadi H., Mohammadzadeh M. Overwintering Physiology and Cold Tolerance of the Sunn Pest, Eurygaster integriceps, an Emphasis on the Role of Cryoprotectants. Front. Physiol. 2020;11:321. doi: 10.3389/fphys.2020.00321. PubMed DOI PMC
Ishiguro S., Li Y.P., Nakana K., Tsumuki H., Goto M. Seasonal changes in glycerol content and cold hardiness in two ecotypes of the rice stem borer, Chilo suppressalis, exposed to the environment in the Shonai district, Japan. J. Insect Physiol. 2007;53:392–397. doi: 10.1016/j.jinsphys.2006.12.014. PubMed DOI
Park Y., Kim Y., Park G.W., Lee J.O., Lee K.W. Supercooling capacity along with up-regulation of glycerol content in an overwintering butterfly, Parnassius bremeri. J. Asia-Pac. Entomol. 2017;20:949–954. doi: 10.1016/j.aspen.2017.06.014. DOI
Mohammadzadeh M., Izadi H. Cold Acclimation of Trogoderma granarium Everts Is Tightly Linked to Regulation of Enzyme Activity, Energy Content, and Ion Concentration. Front. Physiol. 2018;9:1427. doi: 10.3389/fphys.2018.01427. PubMed DOI PMC
Kostal V., Nedved O., Simek P. Accumulation of high concentrations of myo-inositol in the overwintering ladybird beetle Ceratomegilla undecimnotata. Cryo-Lett. 1996;17:267–272.
Yoshida M., Abe J., Moiyama M., Kuwabara T. Carbohydrate levels among winter wheat cultivars varying in freezing tolerance and snow mold resistance during autumn and winter. Physiol. Plant. 1998;103:8–16. doi: 10.1034/j.1399-3054.1998.1030102.x. DOI
Kostal V., Stetina T., Poupardin R., Korbelova J., Bruce A.W. Conceptual framework of the ecophysiological phases of insect diapause development justified by transcriptomic profiling. Proc. Nat. Acad. Sci. USA. 2017;114:8532–8537. doi: 10.1073/pnas.1707281114. PubMed DOI PMC
Elbein A.D., Pan Y.T., Pastuszak I., Carroll D. New insights on trehalose: A multifunctional molecule. Glycobiology. 2003;13:17R–27R. doi: 10.1093/glycob/cwg047. PubMed DOI
Tamang A.M., Kalra B., Parkash R. Cold and desiccation stress induced changes in the accumulation and utilization of proline and trehalose in seasonal populations of Drosophila immigrans. Comp. Biochem. Physiol. A. 2017;203:304–313. doi: 10.1016/j.cbpa.2016.10.011. PubMed DOI
Guo N., Puhlev I., Brown D., Mansbridge J., Levine F. Trehalose expression confers desiccation tolerance on human cells. Nat. Biotechnol. 2000;18:168–171. doi: 10.1038/72616. PubMed DOI
Sinclair B.J. Water relations of the freeze-tolerant New Zealand alpine cockroach Celatoblatta quinquemaculata (Dictyoptera: Blattidae) J. Insect Physiol. 2000;46:869–876. doi: 10.1016/S0022-1910(99)00193-6. PubMed DOI
Clements R.S. The Polyol Pathway. Drugs. 1986;32:3–5. doi: 10.2165/00003495-198600322-00003. PubMed DOI
Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC
Lanfear R., Calcott B., Ho S.Y.W., Guindon S. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 2016;29:1695–1701. doi: 10.1093/molbev/mss020. PubMed DOI
Rambaut A., Drummond A.J., Xie D., Baele G., Suchard M.A. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018;67:901–904. doi: 10.1093/sysbio/syy032. PubMed DOI PMC