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Intraspecific genetic variation for anesthesia success in a New Zealand freshwater snail

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Abstract

Intraspecific genetic variation can drive phenotypic variation even across very closely related individuals. Here, we demonstrate that genetic differences between snails are a major contributor to wide variation in menthol anesthesia success in an important freshwater snail model system, Potamopyrgus antipodarum. Anesthesia is used to immobilize organisms for experiments and surgical procedures and to humanely mitigate pain. This is the first example of which we are aware of a role for genetic variation in anesthesia success in a mollusk. These findings highlight the fact that using only one strain or lineage for many experiments will not provide a full picture of phenotypic variation, demonstrate the importance of optimizing biomedically relevant techniques and protocols across a variety of genetic backgrounds, illuminate a potential mechanism underlying previously documented challenges in molluscan anesthesia, and set the stage for powerful and humane manipulative experiments in P. antipodarum.

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References

  • American Veterinary Medical Association (2020) The AMVA guidelines for the euthanasia of animals: 2020 Edition

  • Baier F, Hong N, Yang G, Pabis A, Miton CM, Barrozo A, Carr PD, Kamerlin SCL, Jackson CJ (2019) Cryptic genetic variation shapes the adaptive evolutionary potential of enzymes. eLife 8:e40789

    Article  PubMed  PubMed Central  Google Scholar 

  • Bankers L, Fields P, McElroy KE, Boore JL, Logsdon JM Jr, Neiman M (2017) Genomic evidence for population-specific responses to coevolving parasites in a New Zealand freshwater snail. Mol Ecol 26:3663–3675

    Article  CAS  PubMed  Google Scholar 

  • Butler-Struben HM, Brophy SM, Crook RJ (2018) In vivo recording of neural and behavioral correlates of anesthesia induction, reversal, and euthanasia in cephalopod molluscs. Front Physiol 9:109

    Article  PubMed  PubMed Central  Google Scholar 

  • Chesler E, Ritchie J, Kokayeff A, Lariviere WR, Wilson SG, Moghil JS (2003) Genotype-dependence of gabapentin and pregabalin sensitivity: the pharmacogenetic mediation of analgesia is specific to the type of pain being inhibited. Pain 106:325–335

    Article  CAS  PubMed  Google Scholar 

  • Cooper JE (2011) Anesthesia, analgesia, and euthanasia of invertebrates. ILAR J 52:196–204

    Article  CAS  PubMed  Google Scholar 

  • Crook RJ, Hanlon RT, Walters ET (2013) Squid have nociceptors that display widespread long-term sensitization and spontaneous activity after bodily injury. J Neurosci 33:10021–10026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Donne C, Neiman M, Woodell JD, Haase M, Verhaegen G (2020) A layover in Europe: reconstructing the invasion route of asexual lineages of a New Zealand snail to North America. Mol Ecol 29:3446–3465

    Article  PubMed  Google Scholar 

  • Faralli M, Lawson T (2020) Natural genetic variation in photosynthesis: an untapped resource to increase crop yield potential? Plant J 101:518–528

    Article  CAS  PubMed  Google Scholar 

  • Fiorito G, Affuso A, Basil J, Cole A, de Girolamo P, D’Angelo L, Dickel L, Gestal C, Grasso F, Kuba M, Mark F, Melillo D, Osorio D, Perkins K, Ponte G, Shashar N, Smith D, Smith J, Andrews PLR (2015) Guidelines for the care and welfare of cephalopods in research- a consensus based on an initiative by CephRes, FELASA, and the Boyd group. Lab Anim 49:1–90

    Article  PubMed  Google Scholar 

  • Gao J, Hu Z, Shi L, Li N, Ouyang Y, Shu S, Yao S, Chen X (2018) HCN channels contribute to the sensitivity of intravenous anesthetics in developmental mice. Oncotarget 9:12907–12917

    Article  PubMed  PubMed Central  Google Scholar 

  • Geiß C, Ruppert K, Askem C, Barroso C, Faber D, Ducrot V, Holbech H, Hutchinson TH, Kajankari P, Kinnberg KL, Lagadic L, Matthiessen P, Morris S, Neiman M, Penttinen O-P, Sanchez-Marin P, Tiegeler M, Weltje L, Oehlmann J (2017) Validation of the OECD reproduction test guideline with the New Zealand mudsnail Potamopyrgus antipodarum using trenbolone and prochloraz. Ecotoxicology 26:370–382

    Article  PubMed  Google Scholar 

  • Gibney ER (2020) Personalised nutrition - phenotypic and genetic variation in response to dietary intervention. Proc Nutrition Soc 79:236–245

    Article  CAS  Google Scholar 

  • Gilbertson CR, Wyatt JD (2016) Evaluation of euthanasia techniques for an invertebrate species, land snails (Succinea putris). J Am Assoc Lab Anim Sci 55:577–581

    PubMed  PubMed Central  Google Scholar 

  • Guan Z, Scott RL, Nash HA (2000) A new assay for the genetic study of general anesthesia in Drosophila melanogaster: use in analysis of mutations in the X-chromosomal 12E region. J Neurogenet 14:25–42

    Article  PubMed  Google Scholar 

  • Guenette SA, Lair S (2006) Anesthesia of the leopard frog, Rana pipiens: a comparative study between four different agents. J Herpetol Med Surg 16:38–44

    Article  Google Scholar 

  • Hawasli AH, Saifee O, Liu C, Nonet ML, Crowder CM (2004) Resistance of volatile anesthetics by mutations enhancing excitatory neurotransmitter release in Caenorhabditis elegans. Genetics 168:831–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jalinsky J, Logsdon JM Jr, Neiman M (2020) Male phenotypes in a female framework: evidence for degeneration in sperm produced by male snails from asexual lineages. J Evol Biol 33:1050–1059

    Article  Google Scholar 

  • Krois NR, Cherukuri A, Puttagunta N, Neiman M (2013) Higher rate of tissue regeneration in polyploid asexual vs. diploid sexual freshwater snails. Biol Lett 9:20130422

    Article  PubMed  PubMed Central  Google Scholar 

  • Larkin K, Tucci C, Neiman M (2016) Effects of polyploidy and reproductive mode on life history trait expression. Ecol Evol 6:765–778

    Article  PubMed  PubMed Central  Google Scholar 

  • Larsson J, Wahlström G (1998) The influence of age and administration rate on the brain sensitivity to propofol in rats. Acta Anaesthesiol Scand 42:987–994

    Article  CAS  PubMed  Google Scholar 

  • Lewbart GA, Mosley C (2011) Clinical anesthesia and analgesia in invertebrates. J Exot Pet Med 21:59–70

    Article  Google Scholar 

  • Mackay TFC, Huang W (2018) Charting the genotype–phenotype map: lessons from the Drosophila melanogaster Genetic Reference Panel. WIREs Dev Biol 7:e289

    Article  Google Scholar 

  • Magnuson R (2018) An exploration of alternative anesthesia in the difficult-to-anesthetize New Zealand freshwater snail Potamopyrgus antipodarum. Iowa Research Online

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • McCraw BM (1958) Relaxation of snails before fixation. Nature 181:575

    Article  Google Scholar 

  • Moghil JS, Smith SB, O’Reilly MK, Plourde G (2005) Influence of nociception and stress-induced antinociception on genetic variation in isoflurane anesthetic potency among mouse strains. Anesthesiology 103:751–758

    Article  Google Scholar 

  • Morgan PG, Sedensky MM (1994) Mutations conferring new patterns of sensitivity to volatile anesthetics in Caenorhabditis elegans. Anesthesiology 81:888–898

    Article  CAS  PubMed  Google Scholar 

  • Nash HA (2002) In vivo genetics of anaesthetic action. Br J Anaesth 89:143–155

    Article  CAS  PubMed  Google Scholar 

  • National Academies of Sciences, Engineering, and Medicine (2020) Next steps for functional genomics: proceedings of a workshop. The National Academies Press, Washington, DC. https://doi.org/10.17226/25780.

  • Neiman M, Paczesniak D, Soper DM, Baldwin AT, Hehman G (2011) Wide variation in ploidy level and genome size in a New Zealand freshwater snail with coexisting sexual and asexual lineages. Evolution 65:3203–3216

    Article  Google Scholar 

  • Niepoth N, Bendesky A (2020) How natural genetic variation shapes behavior. Annu Rev Genom Hum Genet 21:437–463

    Article  CAS  Google Scholar 

  • Paczesniak D, Jokela J, Larkin K, Neiman M (2013) Discordance between nuclear and mitochondrial genomes in sexual and asexual lineages of the freshwater snail Potamopyrgus antipodarum. Mol Ecol 22:4695–4710

    Article  PubMed  Google Scholar 

  • Poole T (1997) Happy animals make good science. Lab Anim 31:116–124

    Article  CAS  PubMed  Google Scholar 

  • Rogstad SH, Keane B, Beresh J (2002) Genetic variation across VNTR loci in central North American Taraxacum surveyed at different spatial scales. Plant Ecol 161:111–121

    Article  Google Scholar 

  • Roper CFE, Hochberg FG (1988) Behavior and systematics of cephalopods from Lizard Island, Australia, based on color and body patterns. Malacologia 29:153–193

    Google Scholar 

  • Scientific Panel on Animal Health and Welfare (AHAW) (2005) Opinion of the scientific panel on animal health and welfare (AHAW) on a request from the commission related to the ‘Aspects of the biology and welfare of animals used for experimental and other scientific purposes.’ EFSA J 3:1–136

    Google Scholar 

  • Seltzer Z (2014) Nothing in pain makes sense except in the light of genetics. Pain 2014:841–842

    Article  Google Scholar 

  • Sharbrough J, Luse M, Boore JL, Logsdon JM Jr, Neiman M (2018) Radical amino acid mutations persist longer in the absence of sex. Evolution 72:808–824

    Article  CAS  PubMed  Google Scholar 

  • Steele LM, Morgan PG, Sedensky MM (2007) Genetics and the mechanisms of action of inhaled anesthetics. Curr Pharmacogenom 5:125–141

    Article  CAS  Google Scholar 

  • Takou M, Wieters B, Kopriva S, Coupland G, Linstädter A, De Meaux J (2019) Linking genes with ecological strategies in Arabidopsis thaliana. J Exp Biol 70:1141–1151

    CAS  Google Scholar 

  • Trimmer C, Keller A, Murphy NR, Snyder LL, Willer JR, Nagai MH, Katsanis N, Vosshall LB, Matsunami H, Mainland JD (2019) Genetic variation across the human olfactory receptor repertoire alters odor perception. Proc Natl Acad Sci USA 116:9475–9480

    Article  CAS  PubMed  Google Scholar 

  • Verhaegen G, McElroy K, Bankers L, Neiman M, Haase M (2018) Adaptive phenotypic plasticity in a clonal invader. Ecol Evol 8:4465–4483

    Article  PubMed  PubMed Central  Google Scholar 

  • Wells MJ (1978) Octopus: physiology and behavior of an advanced invertebrate. Chapman and Hall, London

    Book  Google Scholar 

  • Zachar N, Neiman M (2013) Profound effects of population density on fitness-related traits in an invasive freshwater snail. PLoS ONE 8:e80067

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We gratefully acknowledge Molly Gallagher, Sydney Stork, Benjamin Ripperger, and Alexander Kern for snail care. John Logsdon contributed to snail collections. David (“Davey”) Neiman contributed his Excel expertise to data analysis. Several anonymous reviewers of an earlier version of the manuscript provided valuable feedback. The University of Iowa Department of Biology Honors program, the Iowa Center for Undergraduate Research, and Rick and Linda Maxson logistically and financially supported several undergraduate researchers involved in the project. The SNP genotyping described here was also supported by National Science Foundation-MCB 1122176, National Science Foundation-DEB 1731657, and National Science Foundation-DEB 1601242.

Funding

The study was funded by NSF-MCB 1122176, NSF-DEB 1731657, NSF-DEB 1601242.

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Author notes

  1. Qiudong Song and Richard Magnuson are co-first authors and contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, University of Iowa, Iowa City, IA, USA

    Qiudong Song, Richard Magnuson, Joseph Jalinsky, Marissa Roseman & Maurine Neiman

  2. Department of Gender, Women’s, and Sexuality Studies, University of Iowa, Iowa City, IA, USA

    Maurine Neiman

Authors
  1. Qiudong Song
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  2. Richard Magnuson
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  3. Joseph Jalinsky
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  4. Marissa Roseman
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  5. Maurine Neiman
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Contributions

MN, RM, and QS designed the study. RM and QS collected the snail phenotype data. JJ and MR generated the SNP data. MN analyzed the phenotype data and JJ analyzed the SNP data. MN, RM, and QS wrote the manuscript, and JJ and MR provided editorial revisions. All authors approved the final manuscript.

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Correspondence to Maurine Neiman.

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Song, Q., Magnuson, R., Jalinsky, J. et al. Intraspecific genetic variation for anesthesia success in a New Zealand freshwater snail. Genetica 149, 47–54 (2021). https://doi.org/10.1007/s10709-020-00110-6

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  • DOI: https://doi.org/10.1007/s10709-020-00110-6

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