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Red squirrels in the British Isles are infected with leprosy bacilli

Charlotte Avanzi, Jorge del-Pozo, Andrej Benjak, Karen Stevenson, Victor R. Simpson, Philippe Busso, Joyce McLuckie, Chloé Loiseau, Colin Lawton, Janne Schoening, Darren J. Shaw, Jérémie Piton, Lucio Vera-Cabrera, Jesùs S. Velarde-Felix, Fergal McDermott, Stephen V. Gordon, Stewart T. Cole [email protected], and Anna L. Meredith [email protected]
Science
11 Nov 2016
Vol 354, Issue 6313
pp. 744-747
DOI: 10.1126/science.aah3783
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British squirrels infected with leprosy

With the exception of armadillos in the Americas, leprosy infections are considered almost exclusively restricted to humans. Avanzi et al. examined warty growths on the faces and extremities of red squirrels in the British Isles and found that two species of leprosy-causing organisms were to blame (see the Perspective by Stinear and Brosch). Mycobacterium leprae in the southern population of Brownsea Island squirrels originated from a medieval human strain. M. lepromatosis was found in red squirrels from elsewhere in the United Kingdom and Ireland. Human leprosy is proving hard to eradicate, despite available drugs. Perhaps other wildlife species are also reservoirs for this stubborn disease.
Science, this issue p. 744; see also p. 702

Abstract

Leprosy, caused by infection with Mycobacterium leprae or the recently discovered Mycobacterium lepromatosis, was once endemic in humans in the British Isles. Red squirrels in Great Britain (Sciurus vulgaris) have increasingly been observed with leprosy-like lesions on the head and limbs. Using genomics, histopathology, and serology, we found M. lepromatosis in squirrels from England, Ireland, and Scotland, and M. leprae in squirrels from Brownsea Island, England. Infection was detected in overtly diseased and seemingly healthy animals. Phylogenetic comparisons of British and Irish M. lepromatosis with two Mexican strains from humans show that they diverged from a common ancestor around 27,000 years ago, whereas the M. leprae strain is closest to one that circulated in Medieval England. Red squirrels are thus a reservoir for leprosy in the British Isles.

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Supplementary Material

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Materials and Methods
Figs. S1 to S5
Tables S1 to S14
References (31–51)

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Information & Authors

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Published In

Science
Volume 354 | Issue 6313
11 November 2016

Copyright

Copyright © 2016, American Association for the Advancement of Science.

Submission history

Received: 21 June 2016
Accepted: 27 September 2016
Published in print: 11 November 2016

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Acknowledgments

We thank E. Sheehy, E. Goldstein, M. Flaherty, A. Zintl, the National Trust, Forestry Commission Scotland, and Saving Scotland’s Red Squirrels for samples, help, and advice. We thank the Genomic Technologies Facility at the University of Lausanne for Illumina sequencing and technical support. Raw sequence read files have been deposited in the Sequence Read Archive of the National Center for Biotechnology Information under accession numbers SRR3672737 to SRR3672758 (NCBI BioProject PRJNA325727), SRR3674396 to SRR3674450 (NCBI BioProject PRJNA325827), SRR3674451 to SRR3674453 (NCBI BioProject PRJNA325856), and SRR3673933; representative TLR1 sequences have been deposited in GenBank under accession numbers KX388139, KX388140, and KX388141. Phylogenetic trees and SNP alignments have been deposited at Treebase under Study Accession URL http://purl.org/phylo/treebase/phylows/study/TB2:S19692. Supported by the Fondation Raoul Follereau and Swiss National Science Foundation grant IZRJZ3_164174 (S.T.C.), the Scottish Government Rural and Environment Science and Analytical Services Division (K.S.), and the Thomas O’Hanlon Memorial Award in Veterinary Medicine (F.McD.).

Authors

Affiliations

Charlotte Avanzi*
Global Health Institute, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
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Jorge del-Pozo*
Royal (Dick) School of Veterinary Studies and Roslin Institute, University of Edinburgh, Easter Bush Campus, Roslin, Scotland, UK.
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Andrej Benjak*
Global Health Institute, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
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Karen Stevenson
Moredun Research Institute, Pentlands Science Park, Bush Loan, Edinburgh, Scotland, UK.
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Victor R. Simpson
Wildlife Veterinary Investigation Centre, Chacewater, Cornwall, UK.
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Philippe Busso
Global Health Institute, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
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Joyce McLuckie
Moredun Research Institute, Pentlands Science Park, Bush Loan, Edinburgh, Scotland, UK.
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Chloé Loiseau
Global Health Institute, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
Present address: Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, 4002 Basel, Switzerland.
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Colin Lawton
School of Natural Sciences, Ryan Institute, National University of Ireland, Galway, Ireland.
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Janne Schoening
UCD School of Veterinary Medicine, University College Dublin, Belfield, Dublin, Ireland.
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Darren J. Shaw
Royal (Dick) School of Veterinary Studies and Roslin Institute, University of Edinburgh, Easter Bush Campus, Roslin, Scotland, UK.
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Jérémie Piton
Global Health Institute, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
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Lucio Vera-Cabrera
Laboratorio Interdisciplinario de Investigación Dermatológica, Servicio de Dermatología, Hospital Universitario, Monterrey, N.L., Mexico.
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Jesùs S. Velarde-Felix
Laboratorio Interdisciplinario de Investigación Dermatológica, Servicio de Dermatología, Hospital Universitario, Monterrey, N.L., Mexico.
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Fergal McDermott
UCD School of Veterinary Medicine, University College Dublin, Belfield, Dublin, Ireland.
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Stephen V. Gordon
UCD School of Veterinary Medicine, University College Dublin, Belfield, Dublin, Ireland.
UCD School of Medicine, University College Dublin, Belfield, Dublin, Ireland.
UCD School of Biomolecular and Biomedical Science, University College Dublin, Belfield, Dublin, Ireland.
UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Belfield, Dublin, Ireland.
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Stewart T. Cole‡ [email protected]
Global Health Institute, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
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Anna L. Meredith‡ [email protected]
Royal (Dick) School of Veterinary Studies and Roslin Institute, University of Edinburgh, Easter Bush Campus, Roslin, Scotland, UK.
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Notes

*
These authors contributed equally to this work.
‡Corresponding author: Email: [email protected] (S.T.C.); [email protected] (A.L.M.)

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