Dr Robbie Rae

School of Biological and Environmental Sciences

Image of Dr Robbie Rae

Faculty: Faculty of Science

School: School of Biological and Environmental Sciences

Email address: R.G.Rae@ljmu.ac.uk

Telephone: 0151 231 2486

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Reader in Ecological Genetics

Parasites and hosts have been embroiled in a co-evolutionary arms race for millions of years. To study this relationship I use parasitic nematodes and gastropods (slugs and snails). Specifically, I research the slug parasitic nematode Phasmarhabditis hermaphrodita. It has been developed as a biological control agent to kill slugs and snails in farms and gardens for 25 years. We have recently isolated 20 wild strains of different Phasmarhabditis species and have investigated their behaviour, pathogenicity to slugs as well as there tolerance to abiotic factors. We have also begun sequencing the genomes of our Phasmarhabditis species. Our main aim is to make a better biological control agent for slugs. To do this I have received funding from BASF Agricultural Specialities, the Royal Horticultural Society and the Wellcome Trust. More information can be found at my blog phasmarhabditis@wordpress.com

In general, my research can be split into 3 areas:

1. Investigating natural variation in pathogenicity of wild strains of Phasmarhabditis and the associated microbiome.
2. Examining how snails defend themselves from Phasmarhabditis nematodes and the role of the gastropod shell.
3. Studying the effect of Phasmarhabditis nematodes on slug and snail behaviour.

I’ve been lucky enough to be awarded funding to fund several PhD students who worked on various nematodes. Dr. Sandra Edmunds graduated in 2019 and worked on investigating whether entomopathogenic nematodes can be used to kill mosquitos. Dr. James Cutler examined natural variation in pathogenicity and behaviour of slug parasitic nematodes. James was funded by BASF Agricultural Specialities (who make P. hermaphrodita) and was an excellent student but sadly passed away in 2022. Dr. Kerry McDonald Howard worked on the effect of soil on the survival and infection of P. hermaphrodita (co-funded by the Royal Horticultural Society). Laura Sheehy delved into the genomics of our collection of P. hermaphrodita as well looking at the microbiome of not just these nematodes but in slugs too (funded by BASF Agricultural Specialities).

At JMU I am module leader for the final year Research Project (6201NATSCI) as well as Applications of Genetics in Health and Disease (6203NATSCi). I also teach on a range of undergraduate courses including Genes and Genomes, Genetics and Evolution and Health and Disease.

Degrees

2007, University of Aberdeen, United Kingdom, PhD Plant and Soil Science
2003, University of Aberdeen, United Kingdom, MSc Environmental Science
2002, University of Aberdeen, United Kingdom, BSc (Hons ) Forest Management

Certifications

Higher Education Authority, Fellow of the Higher Education Authority

Academic appointments

Reader in Ecological Genetics, Liverpool John Moores University, 2020 - present
Lecturer in Ecological Genetics, Liverpool John Moores University, 2013 - 2020
Postdoctoral research fellow, Max Planck Institute for Developmental Biology (MPG), 2007 - 2013

Highlighted publications

Rae R, Sheehy L, McDonald-Howard K. 2023. Thirty years of slug control using the parasitic nematode Phasmarhabditis hermaphrodita and beyond Pest Management Science, DOI Author Url Publisher Url Public Url

Sheehy L, MacDonald-Howard K, Williams CD, Weedall GD, Jones H, Rae R. 2023. A parasitic nematode induces dysbiosis in susceptible but not resistant gastropod hosts MicrobiologyOpen, 12 DOI Author Url Publisher Url Public Url

Sheehy L, Cutler J, Weedall GD, Rae R. 2022. Microbiome analysis of malacopathogenic nematodes suggests no evidence of a single bacterial symbiont responsible for gastropod mortality Frontiers in Immunology, DOI Author Url Publisher Url Public Url

Falkingham PL, Rae R. 2021. 3D morphology of nematode encapsulation in snail shells, revealed by micro-CT imaging Scientific Reports, 11 DOI Author Url Publisher Url Public Url

Howe DK, Ha AD, Colton A, De Ley IT, Rae RG, Ross J, Wilson M, Nermut J, Zhao Z, Mc Donnell RJ, Denver DR. 2020. Phylogenetic evidence for the invasion of a commercialized European Phasmarhabditis hermaphrodita lineage into North America and New Zealand PLoS One, 15 DOI Author Url Publisher Url Public Url

Rae R, Cutler J. 2020. Pathogenicity of wild and commercial Phasmarhabditis hermaphrodita exposed to the pestiferous slug Deroceras invadens Journal of Invertebrate Pathology, 174 DOI Author Url Publisher Url Public Url

Knot I, Zouganelis GD, Weedall GD, Wich SA, Rae R. 2020. DNA barcoding of nematodes using the MinION Frontiers in Ecology and Evolution, DOI Author Url Publisher Url Public Url

Morris A, Green M, Martin H, Crossland K, Swaney WT, Williamson SM, Rae R. 2018. A nematode that can manipulate the behaviour of slugs Behavioural Processes, DOI Author Url Publisher Url Public Url

Rae R. 2017. The gastropod shell has been co-opted to kill parasitic nematodes Scientific Reports, 7 DOI Author Url Publisher Url Public Url

Journal article

Rae R, Sheehy L, McDonald-Howard K. 2023. Thirty years of slug control using the parasitic nematode Phasmarhabditis hermaphrodita and beyond Pest Management Science, DOI Author Url Publisher Url Public Url

Sheehy L, MacDonald-Howard K, Williams CD, Weedall GD, Jones H, Rae R. 2023. A parasitic nematode induces dysbiosis in susceptible but not resistant gastropod hosts MicrobiologyOpen, 12 DOI Author Url Publisher Url Public Url

Rae R. 2023. Avoidance and attraction behaviour of slugs exposed to parasitic nematodes Journal of Invertebrate Pathology, DOI Author Url Publisher Url Public Url

Andrus PS, Rae R, Wade CM. 2022. Nematodes and trematodes associated with terrestrial gastropods in Nottingham, England Journal of Helminthology, 96 :1-13 DOI Author Url Publisher Url Public Url

Massart S, Adams I, Al Rwahnih M, Baeyen S, Bilodeau GJ, Blouin AG, Boonham N, Candresse T, Chandellier A, De Jonghe K, Fox A, Gaafar YZA, Gentit P, Haegeman A, Ho W, Hurtado-Gonzales O, Jonkers W, Kreuze J, Kutjnak D, Landa BB, Liu M, Maclot F, Malapi-Wight M, Maree HJ, Martoni F, Mehle N, Minafra A, Mollov D, Moreira AG, Nakhla M, Petter F, Piper AM, Ponchart JP, Rae R, Remenant B, Rivera Y, Rodoni B, Botermans M, Roenhorst JW, Rollin J, Saldarelli P, Santala J, Souza-Richards R, Spadaro D, Studholme DJ, Sultmanis S, van der Vlugt R, Tamisier L, Trontin C, Vazquez-Iglesias I, Vicente CSL, van de Vossenberg BTLH, Westenberg M, Wetzel T, Ziebell H, Lebas BSM. 2022. Guidelines for the reliable use of high throughput sequencing technologies to detect plant pathogens and pests Peer Community Journal, 2 DOI Publisher Url Public Url

Lebas B, Adams I, Al Rwahnih M, Baeyen S, Bilodeau G, Blouin AG, Boonham N, Candresse T, Chandelier A, De Jonghe K, Fox A, Gaafar YZA, Gentit P, Haegeman A, Ho W, Hurtado-Gonzales O, Jonkers W, Kreuze J, Kutjnak D, Landa B, Liu M, Maclot F, Malapi-Wight M, Maree HJ, Martoni F, Mehle N, Minafra A, Mollov D, Moreira A, Nakhla M, Petter F, Piper AM, Ponchart J, Rae R, Remenant B, Rivera Y, Rodoni B, Roenhorst J, Rollin J, Saldarelli P, Santala J, Souza-Richards R, Spadaro D, Studholme DJ, Sultmanis S, van der Vlugt R, Tamisier L, Trontin C, Vazquez-Iglesias I, Vicente CSL, Vossenberg BTLH, Wetzel T, Ziebell H, Massart S. 2022. Facilitating the adoption of high-throughput sequencing technologies as a plant pest diagnostic test in laboratories: A step-by-step description EPPO Bulletin, 52 :394-418 DOI Publisher Url

Sheehy L, Cutler J, Weedall GD, Rae R. 2022. Microbiome analysis of malacopathogenic nematodes suggests no evidence of a single bacterial symbiont responsible for gastropod mortality Frontiers in Immunology, DOI Author Url Publisher Url Public Url

Keyte M, Grannell A, Sheehy L, Shepherd J, Rae R. 2022. Phasmarhabditis californica in Germany Nematology: international journal of fundamental and applied nematological research, :1-6 DOI Publisher Url Public Url

McDonald-Howard K, Williams CD, Jones H, Rae R. 2022. A method of culturing and breeding slugs through several generations Journal of Molluscan Studies, 88 DOI Author Url Publisher Url Public Url

Cutler J, Rae R. 2021. The malacopathogenic nematode Phasmarhabditis californica does not affect the survival of earthworms (Lumbricus terrestris and Eisenia fetida) or insects (Galleria mellonella and Tenebrio molitor) Biocontrol Science and Technology, DOI Author Url Publisher Url Public Url

Grannell A, Cutler J, Rae R. 2021. Size-susceptibility of Cornu aspersum exposed to the malacopathogenic nematodes Phasmarhabditis hermaphrodita and P. californica Biocontrol Science and Technology, 31 :1149-1160 DOI Author Url Publisher Url Public Url

Rae R, Cutler J. 2021. Natural variation in host finding behaviour of gastropod parasitic nematodes (Phasmarhabditis spp.) exposed to host associated cues Journal of Helminthology, 95 DOI Author Url Publisher Url Public Url

Falkingham PL, Rae R. 2021. 3D morphology of nematode encapsulation in snail shells, revealed by micro-CT imaging Scientific Reports, 11 DOI Author Url Publisher Url Public Url

Howe DK, Ha AD, Colton A, De Ley IT, Rae RG, Ross J, Wilson M, Nermut J, Zhao Z, Mc Donnell RJ, Denver DR. 2020. Phylogenetic evidence for the invasion of a commercialized European Phasmarhabditis hermaphrodita lineage into North America and New Zealand PLoS One, 15 DOI Author Url Publisher Url Public Url

Rae R, Cutler J. 2020. Pathogenicity of wild and commercial Phasmarhabditis hermaphrodita exposed to the pestiferous slug Deroceras invadens Journal of Invertebrate Pathology, 174 DOI Author Url Publisher Url Public Url

Barua A, McDonald-Howard K, McDonnell R, Rae R, Williams CD. 2020. Toxicity of essential oils to slug parasitic and entomopathogenic nematodes Journal of Pest Science, 93 :1411-1419 DOI Author Url Publisher Url Public Url

Knot I, Zouganelis GD, Weedall GD, Wich SA, Rae R. 2020. DNA barcoding of nematodes using the MinION Frontiers in Ecology and Evolution, DOI Author Url Publisher Url Public Url

Edmunds S, Wilding C, Rae R. 2020. Pathogenicity and environmental tolerance of commercial and UK native entomopathogenic nematodes (Steinernema and Heterorhabditis spp.) to the larvae of mosquitos (Aedes aegypti and Ochlerotatus detritus). International Journal of Pest Management, 67 :232-240 DOI Author Url Publisher Url Public Url

Cutler J, Williamson SM, Rae R. 2019. The effect of sertraline, haloperidol and apomorphine on the behavioural manipulation of slugs (Deroceras invadens) by the nematode Phasmarhabditis hermaphrodita Behavioural Processes, DOI Author Url Publisher Url Public Url

Rae RG. 2019. My favourite nematode – Phasmarhabditis hermaphrodita Nematology, 21 DOI Author Url Publisher Url Public Url

Rae RG, Andrus P. 2018. Natural variation in chemoattraction in the gastropod parasitic nematodes Phasmarhabditis hermaphrodita, P. neopapillosa and P. californica exposed to slug mucus Nematology, DOI Author Url Publisher Url Public Url

Andrus P, Ingle O, Coleman T, Rae R. 2018. Gastropod parasitic nematodes (Phasmarhabditis sp.) are attracted to hyaluronic acid in snail mucus by cGMP signalling Journal of Helminthology, DOI Author Url Publisher Url Public Url

Edmunds C, Post RJ, Wilding CS, Rae R. 2018. A survey investigating the diversity and distribution of entomopathogenic nematodes in the UK and the first confirmed UK record of Steinernema carpocapsae Nematology, 20 :851-858 DOI Author Url Publisher Url Public Url

Rae RG, Andrus P. 2018. Development of Phasmarhabditis hermaphrodita (and members of the Phasmarhabditis genus) as new genetic model nematodes to study the genetic basis of parasitism Journal of Helminthology, DOI Author Url Publisher Url Public Url

Morris A, Green M, Martin H, Crossland K, Swaney WT, Williamson SM, Rae R. 2018. A nematode that can manipulate the behaviour of slugs Behavioural Processes, DOI Author Url Publisher Url Public Url

Rae RG. 2017. Shell encapsulation of parasitic nematodes by Arianta arbustorum (Linnaeus, 1758) in the laboratory and in field collections Journal of Molluscan Studies, DOI Author Url Publisher Url Public Url

Edmunds C, Wilding CS, Rae R. 2017. Susceptibility of Chironomus plumosus larvae (Diptera: Chironomidae) to entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae): potential for control European Journal of Entomology, 114 :526-532 DOI Author Url Publisher Url Public Url

Rae R. 2017. The gastropod shell has been co-opted to kill parasitic nematodes Scientific Reports, 7 DOI Author Url Publisher Url Public Url

Cutler J, Hughes K, Rae R. 2017. Susceptibility of cockroaches (Gromphadorhina portentosa, Nauphoeta cinerea and Blaptica dubia) exposed to entomopathogenic nematodes Biocontrol Science and Technology, 27 :556-564 DOI Author Url Publisher Url Public Url

Rae RG. 2017. Phasmarhabditis hermaphrodita – a new model to study the genetic evolution of parasitism Nematology, 19 DOI Author Url Publisher Url Public Url

Carnaghi M, Rae R, Tandingan De Ley I, Johnston E, Kindermann G, Mc Donnell R, O'Hanlon A, Reich I, Sheahan J, Williams CD, Gormally MJ. 2017. Nematode associates and susceptibility of a protected slug (Geomalacus maculosus) to four biocontrol nematodes Biocontrol Science and Technology, DOI Author Url Publisher Url Public Url

Williams A, Rae R. 2016. Cepaea nemoralis (Linnaeus, 1758) uses its shell as a defence mechanism to trap and kill parasitic nematodes Journal of Molluscan Studies, 1-2 DOI Author Url Publisher Url Public Url

Wynne R, Morris A, Rae R. 2016. Behavioural avoidance by slugs and snails of the parasitic nematode Phasmarhabditis hermaphrodita BIOCONTROL SCIENCE AND TECHNOLOGY, 26 :1129-1138 DOI Author Url Publisher Url Public Url

Sinha A, Rae R. 2016. Genome-Wide RNAi Screens in C. elegans to Identify Genes Influencing Lifespan and Innate Immunity. Methods in molecular biology (Clifton, N.J.), 1470 :171-182 DOI Author Url Publisher Url

Whitaker G, Rae R. 2015. The gastropod parasitic nematode Phasmarhabditis hermaphrodita does not affect non-target freshwater snails Lymnaea stagnalis, Bithynia tentaculata and Planorbarius corneus NEMATOLOGY, 17 :679-683 DOI Author Url Publisher Url Public Url

Williams AJ, Rae R. 2015. Susceptibility of the Giant African snail (Achatina fulica) exposed to the gastropod parasitic nematode Phasmarhabditis hermaphrodita JOURNAL OF INVERTEBRATE PATHOLOGY, 127 :122-126 DOI Author Url Publisher Url Public Url

Sinha A, Rae R. 2014. A Functional Genomic Screen for Evolutionarily Conserved Genes Required for Lifespan and Immunity in Germline-Deficient C. elegans PLOS ONE, 9 DOI Author Url Publisher Url

Rae R, Witte H, Rödelsperger C, Sommer RJ. 2012. The importance of being regular: Caenorhabditis elegans and Pristionchus pacificus defecation mutants are hypersusceptible to bacterial pathogens. Int J Parasitol, 42 :747-753 DOI Author Url Publisher Url

Sinha A, Rae R, Iatsenko I, Sommer RJ. 2012. System wide analysis of the evolution of innate immunity in the nematode model species Caenorhabditis elegans and Pristionchus pacificus. PLoS One, 7 :e44255 DOI Author Url Publisher Url

Rae R, Sinha A, Sommer RJ. 2012. Genome-wide analysis of germline signaling genes regulating longevity and innate immunity in the nematode Pristionchus pacificus. PLoS Pathog, 8 :e1002864 DOI Author Url Publisher Url

Rae R, Sommer RJ. 2011. Bugs don't make worms kill Journal of Experimental Biology, 214 :1053 DOI Author Url Publisher Url

Rae R, Iatsenko I, Witte H, Sommer RJ. 2010. A subset of naturally isolated Bacillus strains show extreme virulence to the free-living nematodes Caenorhabditis elegans and Pristionchus pacificus. Environ Microbiol, 12 :3007-3021 DOI Author Url Publisher Url

Rae RG, Tourna M, Wilson MJ. 2010. The slug parasitic nematode Phasmarhabditis hermaphrodita associates with complex and variable bacterial assemblages that do not affect its virulence. J Invertebr Pathol, 104 :222-226 DOI Author Url Publisher Url

Weller AM, Mayer WE, Rae R, Sommer RJ. 2010. Quantitative assessment of the nematode fauna present on Geotrupes dung beetles reveals species-rich communities with a heterogeneous distribution. J Parasitol, 96 :525-531 DOI Author Url Publisher Url

Rae RG, Robertson JF, Wilson MJ. 2009. Optimization of biological (Phasmarhabditis hermaphrodita) and chemical (iron phosphate and metaldehyde) slug control Crop Protection, 28 :765-773 DOI Author Url Publisher Url

MacMillan K, Haukeland S, Rae R, Young I, Crawford J, Hapca S, Wilson M. 2009. Dispersal patterns and behaviour of the nematode Phasmarhabditis hermaphrodita in mineral soils and organic media Soil Biology and Biochemistry, 41 :1483-1490 DOI Author Url Publisher Url

Rae RG, Robertson JF, Wilson MJ. 2009. Chemoattraction and host preference of the gastropod parasitic nematode Phasmarhabditis hermaphrodita. J Parasitol, 95 :517-526 DOI Author Url Publisher Url

Rae R, Schlager B, Sommer RJ. 2008. Assessment of the olfactory response to chemicals or bacteria in pristionchus nematodes. CSH Protoc, 2008 :pdb.prot5064 DOI Author Url Publisher Url

Rae R, Schlager B, Sommer RJ. 2008. Isolation of pristionchus nematodes from beetles. CSH Protoc, 2008 :pdb.prot5063 DOI Author Url Publisher Url

Rae R, Schlager B, Sommer RJ. 2008. Pristionchus pacificus: A Genetic Model System for the Study of Evolutionary Developmental Biology and the Evolution of Complex Life-History Traits. CSH Protoc, 2008 :pdb.emo102 DOI Author Url Publisher Url

Rae R, Riebesell M, Dinkelacker I, Wang Q, Herrmann M, Weller AM, Dieterich C, Sommer RJ. 2008. Isolation of naturally associated bacteria of necromenic Pristionchus nematodes and fitness consequences. J Exp Biol, 211 :1927-1936 DOI Author Url Publisher Url

Rae RG, Robertson JF, Wilson MJ. 2008. Susceptibility and immune response of Deroceras reticulatum, Milax gagates and Limax pseudoflavus exposed to the slug parasitic nematode Phasmarhabditis hermaphrodita Journal of Invertebrate Pathology, 97 :61-69 DOI Author Url Publisher Url

Rae R, Verdun C, Grewal PS, Robertson JF, Wilson MJ. 2007. Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita--progress and prospects. Pest Manag Sci, 63 :1153-1164 DOI Author Url Publisher Url

Hapca S, Crawford J, Rae R, Wilson M, Young I. 2007. Movement of the parasitic nematode Phasmarhabditis hermaphrodita in the presence of mucus from the host slug Deroceras reticulatum Biological Control, 41 :223-229 DOI Publisher Url

Wilson M, Robertson J, Rae R. 2006. The chemotactic response of Phasmarhabditis hermaphrodita (Nematoda: Rhabditida) to cues of Deroceras reticulatum (Mollusca: Gastropoda) Nematology, 8 :197-200 DOI Publisher Url

Rae RG, Robertson J, Wilson MJ. 2005. Susceptibility of indigenous UK earthworms and an invasive pest flatworm to the slug parasitic nematodePhasmarhabditis hermaphrodita Biocontrol Science and Technology, 15 :623-626 DOI Publisher Url

Rae R, Cowlishaw R, Andrus P. An investigation into nematodes encapsulated in shells of wild, farmed and museum specimens of Cornu aspersum and Helix pomatia Journal of Conchology, 43 :1-8

Chapters

Rae RG. 2015. Phasmarhabditis hermaphrodita as a control agent for slugs Nematode Pathogenesis of Insects and Other Pests Ecology and Applied Technologies for Sustainable Plant and Crop Protection Springer 9783319182650 DOI Publisher Url

Rae RG. 2015. Bacterial interactions of Pristionchus pacificus Pristionchus Pacificus A Nematode Model for Comparative and Evolutionary Biology Brill Academic Publishers 9789004260290

Sinha A, Rae R. 2015. Bacterial interactions and the innate immune system Nematology Monographs and Perspectives 11 :385-407 9789004260290

Editorial boards:

Frontiers in Worm Science, Associate Editor. 2023

Nematology. 2022

External PGR examinations performed:

University of Surrey, PhD, Transcriptomics data-driven metabolic modelling of nematodes for biocontrol of agricultural, domestic, and veterinary pests. 2023

Queens University Belfast, PhD, Behaviour of entomopathogenic nematodes. 2019

Research Grants Awarded:

BASF Agricultural Specialities, Another survey of European slugs for nematodes (Research Assistant position), Grant value (£): 12,000, Duration of research project: 3 months. 2021

BASF Agricultural Specialities, A survey of European slugs for pathogenic nematodes (Research Assistant position)., Grant value (£): 19,930.00, Duration of research project: 4 months. 2020

The Royal Horticultural Society and LJMU, Investigation into the efficacy of the slug biological control agent Phasmarhabditis hermaphrodita, Grant value (£): £68706, Duration of research project: 3 years. 2018

BASF Agricultural Specialities and LJMU, Investigation into natural genetic variation in virulence in slug parasitic nematodes, Grant value (£): £68706, Duration of research project: 3 years. 2018

Wellcome Trust, Biomedical undergraduate summer studentship, Grant value (£): 1600, Duration of research project: 8 weeks. 2015

Wellcome Trust, Investigation into a potential nematode biocontrol agent for Biomphalaria glabrata the intermediate snail host for the blood parasite Schistosoma mansoni, Grant value (£): 1600, Duration of research project: 2 months. 2014

BASF Agricultural Specialities, Genomic analysis of the parasitic nematode Phasmarhabditis hermaphrodita (and other wild Phasmarhabditis species) – a biological control agent of slugs, Grant value (£): 120559.

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