Analysis across diverse fish species highlights no conserved transcriptome signature for proactive behaviour.

Sonia Rey, Xingkun Jin, Børge Damsgård, Marie-Laure Bégout, Simon Mackenzie
Author Information
  1. Sonia Rey: Institute of Aquaculture, University of Stirling, Stirlingshire, FK9 4LA, UK.
  2. Xingkun Jin: Institute of Aquaculture, University of Stirling, Stirlingshire, FK9 4LA, UK.
  3. Børge Damsgård: Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway, 9037, Tromsø, Norway.
  4. Marie-Laure Bégout: Ifremer, Place Gaby Coll, 17137 L'Houmeau, La Rochelle, France.
  5. Simon Mackenzie: Institute of Aquaculture, University of Stirling, Stirlingshire, FK9 4LA, UK. simon.mackenzie@stir.ac.uk. ORCID

Abstract

BACKGROUND: Consistent individual differences in behaviour, known as animal personalities, have been demonstrated within and across species. In fish, studies applying an animal personality approach have been used to resolve variation in physiological and molecular data suggesting a linkage, genotype-phenotype, between behaviour and transcriptome regulation. In this study, using three fish species (zebrafish; Danio rerio, Atlantic salmon; Salmo salar and European sea bass; Dicentrarchus labrax), we firstly address whether personality-specific mRNA transcript abundances are transferrable across distantly-related fish species and secondly whether a proactive transcriptome signature is conserved across all three species.
RESULTS: Previous zebrafish transcriptome data was used as a foundation to produce a curated list of mRNA transcripts related to animal personality across all three species. mRNA transcript copy numbers for selected gene targets show that differential mRNA transcript abundance in the brain appears to be partially conserved across species relative to personality type. Secondly, we performed RNA-Seq using whole brains from S. salar and D. labrax scoring positively for both behavioural and molecular assays for proactive behaviour. We further enriched this dataset by incorporating a zebrafish brain transcriptome dataset specific to the proactive phenotype. Our results indicate that cross-species molecular signatures related to proactive behaviour are functionally conserved where shared functional pathways suggest that evolutionary convergence may be more important than individual mRNAs.
CONCLUSIONS: Our data supports the proposition that highly polygenic clusters of genes, with small additive effects, likely support the underpinning molecular variation related to the animal personalities in the fish used in this study. The polygenic nature of the proactive brain transcriptome across all three species questions the existence of specific molecular signatures for proactive behaviour, at least at the granularity of specific regulatory gene modules, level of genes, gene networks and molecular functions.

Keywords

References

  1. Mol Ecol. 2010 Mar;19 Suppl 1:176-96 [PMID: 20331779]
  2. Bioinformatics. 2009 Apr 15;25(8):1091-3 [PMID: 19237447]
  3. Chin Med J (Engl). 2002 Nov;115(11):1701-5 [PMID: 12609092]
  4. Evolution. 2017 Aug;71(8):1999-2009 [PMID: 28542920]
  5. Mol Ecol. 2013 Dec;22(24):6100-15 [PMID: 24118534]
  6. Psychol Bull. 2001 Jan;127(1):45-86 [PMID: 11271756]
  7. R Soc Open Sci. 2019 Mar 13;6(3):181859 [PMID: 31032038]
  8. Nat Ecol Evol. 2018 Jun;2(6):944-955 [PMID: 29434349]
  9. Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):E1801-10 [PMID: 22691501]
  10. Trends Ecol Evol. 2004 Jul;19(7):372-8 [PMID: 16701288]
  11. Front Neurosci. 2017 Jul 24;11:383 [PMID: 28790881]
  12. Trends Ecol Evol. 2008 Jan;23(1):26-32 [PMID: 18022278]
  13. Behav Processes. 2010 Oct;85(2):198-203 [PMID: 20674703]
  14. Mol Biol Evol. 2015 Mar;32(3):690-703 [PMID: 25492498]
  15. Nat Rev Genet. 2015 Aug;16(8):441-58 [PMID: 26149713]
  16. BMC Evol Biol. 2017 Jul 6;17(1):162 [PMID: 28683774]
  17. BMC Genomics. 2015 Nov 18;16:977 [PMID: 26581708]
  18. PLoS One. 2013 Apr 16;8(4):e62037 [PMID: 23614007]
  19. Genome Res. 2016 Aug;26(8):1134-44 [PMID: 27252236]
  20. Biol Rev Camb Philos Soc. 2007 May;82(2):291-318 [PMID: 17437562]
  21. Neurosci Biobehav Rev. 1999 Nov;23(7):925-35 [PMID: 10580307]
  22. Nat Rev Genet. 2009 Aug;10(8):565-77 [PMID: 19584810]
  23. Mol Biol Evol. 2017 Jul 1;34(7):1812-1819 [PMID: 28387841]
  24. BMC Bioinformatics. 2011 Aug 04;12:323 [PMID: 21816040]
  25. Trends Ecol Evol. 1994 Nov;9(11):442-6 [PMID: 21236920]
  26. Trends Ecol Evol. 2013 Nov;28(11):651-8 [PMID: 23756106]
  27. J Exp Biol. 2017 Apr 15;220(Pt 8):1524-1532 [PMID: 28167808]
  28. Trends Ecol Evol. 2015 Dec;30(12):709-711 [PMID: 26522730]
  29. Trends Ecol Evol. 2010 Feb;25(2):81-9 [PMID: 19748700]
  30. BMC Genomics. 2014 Oct 17;15:905 [PMID: 25326170]
  31. Front Physiol. 2015 Apr 09;6:111 [PMID: 25914648]
  32. J Fish Biol. 2010 May;76(7):1576-91 [PMID: 20557617]
  33. PLoS One. 2009;4(4):e5314 [PMID: 19390591]
  34. Adv Exp Med Biol. 2014;781:149-68 [PMID: 24277299]
  35. Sci Rep. 2017 Jul 3;7(1):4545 [PMID: 28674437]
  36. Trends Ecol Evol. 2015 Jan;30(1):50-60 [PMID: 25498413]
  37. Nat Protoc. 2013 Aug;8(8):1494-512 [PMID: 23845962]
  38. Horm Behav. 2008 Sep;54(4):534-8 [PMID: 18632100]
  39. Biotechnol Lett. 2018 Feb;40(2):227-236 [PMID: 29124515]
  40. Anim Behav. 2014 Jun 1;92:263-270 [PMID: 24954950]
  41. Evolution. 2013 Feb;67(2):305-14 [PMID: 23356605]
  42. Philos Trans R Soc Lond B Biol Sci. 2010 Dec 27;365(1560):4001-12 [PMID: 21078652]

Grants

  1. KBBE-2010-4 Contract nº 265957/Seventh Framework Programme

MeSH Term

Animals
Bass
RNA, Messenger
RNA-Seq
Salmo salar
Transcriptome
Zebrafish

Chemicals

RNA, Messenger

Word Cloud

Created with Highcharts 10.0.0speciesbehaviouracrossproactivemoleculartranscriptomefishanimalpersonalitythreemRNAconservedusedvariationdatazebrafishtranscriptrelatedgenebrainspecificindividualpersonalitiesstudyusingsalarlabraxwhethersignaturedatasetsignaturespolygenicgenesBACKGROUND:Consistentdifferencesknowndemonstratedwithinstudiesapplyingapproachresolvephysiologicalsuggestinglinkagegenotype-phenotyperegulationDaniorerioAtlanticsalmonSalmoEuropeanseabassDicentrarchusfirstlyaddresspersonality-specificabundancestransferrabledistantly-relatedsecondlyRESULTS:PreviousfoundationproducecuratedlisttranscriptscopynumbersselectedtargetsshowdifferentialabundanceappearspartiallyrelativetypeSecondlyperformedRNA-SeqwholebrainsSDscoringpositivelybehaviouralassaysenrichedincorporatingphenotyperesultsindicatecross-speciesfunctionallysharedfunctionalpathwayssuggestevolutionaryconvergencemayimportantmRNAsCONCLUSIONS:supportspropositionhighlyclusterssmalladditiveeffectslikelysupportunderpinningnaturequestionsexistenceleastgranularityregulatorymoduleslevelnetworksfunctionsAnalysisdiversehighlightsAnimalConvergentevolutionFishPhenotypeProactiveRNAsequencing

Similar Articles

Cited By