Modelling the ballistic-to-diffusive transition in nematode motility reveals variation in exploratory behaviour across species.


Journal

Journal of the Royal Society, Interface
ISSN: 1742-5662
Titre abrégé: J R Soc Interface
Pays: England
ID NLM: 101217269

Informations de publication

Date de publication:
30 08 2019
Historique:
entrez: 29 8 2019
pubmed: 29 8 2019
medline: 18 7 2020
Statut: ppublish

Résumé

A quantitative understanding of organism-level behaviour requires predictive models that can capture the richness of behavioural phenotypes, yet are simple enough to connect with underlying mechanistic processes. Here, we investigate the motile behaviour of nematodes at the level of their translational motion on surfaces driven by undulatory propulsion. We broadly sample the nematode behavioural repertoire by measuring motile trajectories of the canonical laboratory strain Caenorhabditis elegans N2 as well as wild strains and distant species. We focus on trajectory dynamics over time scales spanning the transition from ballistic (straight) to diffusive (random) movement and find that salient features of the motility statistics are captured by a random walk model with independent dynamics in the speed, bearing and reversal events. We show that the model parameters vary among species in a correlated, low-dimensional manner suggestive of a common mode of behavioural control and a trade-off between exploration and exploitation. The distribution of phenotypes along this primary mode of variation reveals that not only the mean but also the variance varies considerably across strains, suggesting that these nematode lineages employ contrasting 'bet-hedging' strategies for foraging.

Identifiants

pubmed: 31455164
doi: 10.1098/rsif.2019.0174
pmc: PMC6731512
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

20190174

Références

J Neurosci. 1999 Nov 1;19(21):9557-69
pubmed: 10531458
J Theor Biol. 1975 Apr;50(2):477-96
pubmed: 1094203
Adv Parasitol. 1975;13:71-122
pubmed: 1169872
J Neurosci. 2002 Jul 1;22(13):5727-33
pubmed: 12097525
Neuron. 2002 Dec 19;36(6):1091-102
pubmed: 12495624
J Exp Biol. 1964 Mar;41:135-54
pubmed: 14161604
Eur Biophys J. 2004 Dec;33(8):691-3
pubmed: 15257424
Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3184-91
pubmed: 15689400
Biophys J. 2005 Aug;89(2):912-31
pubmed: 15951372
Nature. 2007 Jan 25;445(7126):406-9
pubmed: 17251974
Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8582-9
pubmed: 17494755
WormBook. 2006 Jan 25;:1-8
pubmed: 18050465
PLoS Comput Biol. 2008 Apr 25;4(4):e1000028
pubmed: 18389066
Handb Exp Pharmacol. 2009;(191):423-43
pubmed: 19089339
J Biol. 2008 Dec 15;7(10):37
pubmed: 19090979
Genome. 2009 Jan;52(1):1-7
pubmed: 19132066
J Neurosci. 2009 Apr 29;29(17):5370-80
pubmed: 19403805
PLoS One. 2010 Nov 16;5(11):e13914
pubmed: 21103370
Trends Ecol Evol. 1989 Feb;4(2):41-4
pubmed: 21227310
Cell. 2011 Nov 11;147(4):922-33
pubmed: 22078887
Science. 2012 Jun 1;336(6085):1157-60
pubmed: 22539553
Curr Opin Neurobiol. 2012 Aug;22(4):580-91
pubmed: 22699037
Proc Natl Acad Sci U S A. 2013 Jan 8;110(2):791-6
pubmed: 23267063
PLoS One. 2013;8(3):e59865
pubmed: 23555813
Phys Rev E Stat Nonlin Soft Matter Phys. 2013 Apr;87(4):042136
pubmed: 23679400
Nat Methods. 2013 Jun;10(6):483-90
pubmed: 23866325
Proc Natl Acad Sci U S A. 2013 Aug 20;110(34):14018-23
pubmed: 23898201
Cell. 2013 Aug 29;154(5):1023-1035
pubmed: 23972393
Curr Biol. 2013 Oct 7;23(19):R862-4
pubmed: 24112976
PLoS One. 2013 Nov 05;8(11):e78535
pubmed: 24223821
J R Soc Interface. 2014 Jan 15;11(92):20131092
pubmed: 24430127
Proc Natl Acad Sci U S A. 2014 Mar 18;111(11):3949-54
pubmed: 24594603
Curr Opin Neurobiol. 2014 Apr;25:99-106
pubmed: 24709607
Elife. 2014 Dec 09;3:null
pubmed: 25490069
Genetics. 2015 Jun;200(2):387-407
pubmed: 26088431
Cell. 2015 Oct 22;163(3):656-69
pubmed: 26478179
Proc Natl Acad Sci U S A. 2016 Feb 23;113(8):E1082-8
pubmed: 26711989
Proc Natl Acad Sci U S A. 2016 Feb 23;113(8):E1074-81
pubmed: 26712014
Elife. 2016 Jan 29;5:null
pubmed: 26824391
Bioscience. 2014 Jun 1;64(6):476-486
pubmed: 26955070
Elife. 2016 Sep 20;5:
pubmed: 27644113
J Cell Biol. 1988 Feb;106(2):303-9
pubmed: 3339093
J Neurosci. 1985 Apr;5(4):956-64
pubmed: 3981252
Genetics. 1974 May;77(1):71-94
pubmed: 4366476
Nature. 1972 Oct 27;239(5374):500-4
pubmed: 4563019
Biophys J. 1970 Oct;10(10):980-93
pubmed: 5531614
Genetics. 1978 Oct;90(2):243-56
pubmed: 730048
Science. 1997 Aug 8;277(5327):834-6
pubmed: 9242616
Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8420-7
pubmed: 9671692

Auteurs

Stephen J Helms (SJ)

AMOLF Institute, Amsterdam, The Netherlands.

W Mathijs Rozemuller (WM)

AMOLF Institute, Amsterdam, The Netherlands.

Antonio Carlos Costa (AC)

Department of Physics and Astronomy, Vrije Universiteit, Amsterdam, The Netherlands.

Leon Avery (L)

Department of Physiology and Biophysics, Virginia Commonwealth University, Richmond, VA, USA.

Greg J Stephens (GJ)

Department of Physics and Astronomy, Vrije Universiteit, Amsterdam, The Netherlands.
Okinawa Institute of Science and Technology, Onna-son, Okinawa, Japan.

Thomas S Shimizu (TS)

AMOLF Institute, Amsterdam, The Netherlands.

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