Science - USA (2022-04-29)

individuals with a sophisticated division of
labor ( 20 ). As a result, their wanting sys-
tem integrates both the social and the indi-
vidual levels.
A neuroscience of pleasure has revealed that
several common principles of the neural encod-
ing of stimuli with positive hedonic value are
shared among mammals ( 1 ). The presence of
a dopamine wanting system in the honey bee
brain suggests that a precursor to mammalian
wanting systems may have evolved very early,
that is, 220 million years ago, dating back
to the oldest currently known Hymenoptera
fossils ( 32 ).

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ACKNOWLEDGMENTS
We thank three anonymous reviewers for useful comments and
suggestions on a previous version of the manuscript.Funding:
This research was supported by the National Natural Science
Foundation of China (31772684) and China Agriculture Research
System of MOF and MARA (CARS-44). Support was also provided
by the CNRS, the University Paul Sabatier of Toulouse, the Institut
Universitaire de France, and the Fujian Agriculture and Forestry
University.Author contributions:J.H., Z.Z., W.F., and Y.Z.

performed the experiments relating aminergic signaling with

foraging and dance activity and also contributed to the analysis

of these data, together with Z.L., H.N., Y.L., S.Z., and S.S., who

supervised data collection. A.A., A.R., M.P., and M.G.d.B.S. performed

the experiments relating individual aminergic signaling and

individual appetitive responses and learning and also contributed

to data analysis, together with M.G., who supervised data

collection. S.S. and M.G. conceived of the project and supervised

the research work. Resources and funding were provided by

S.S. and M.G. M.G. wrote the original draft of the manuscript. All

authors discussed the data and contributed to the revision and

editing of the manuscript.Competing interests:The authors

declare no competing interests.Data and materials availability:

Data are available in Figshare ( 33 ).

SUPPLEMENTARY MATERIALS

science.org/doi/10.1126/science.abn9920

Materials and Methods

Figs. S1 to S5

References ( 34 – 44 )

MDAR Reproducibility Checklist

6 January 2022; accepted 4 March 2022

10.1126/science.abn9920

EPIDEMIOLOGY

Rabies shows how scale of transmission can enable

acute infections to persist at low prevalence

Rebecca Mancy^1 , Malavika Rajeev^2 , Ahmed Lugelo3,4, Kirstyn Brunker^1 , Sarah Cleaveland^1 ,

Elaine A. Ferguson^1 , Karen Hotopp^1 , Rudovick Kazwala^3 , Matthias Magoto^5 , Kristyna Rysava^6 ,

Daniel T. Haydon^1 , Katie Hampson^1 *

How acute pathogens persist and what curtails their epidemic growth in the absence of acquired immunity

remains unknown. Canine rabies is a fatal zoonosis that circulates endemically at low prevalence among

domestic dogs in low- and middle-income countries. We traced rabies transmission in a population of

50,000 dogs in Tanzania from 2002 to 2016 and applied individual-based models to these spatially

resolved data to investigate the mechanisms modulating transmission and the scale over which they

operate. Although rabies prevalence never exceeded 0.15%, the best-fitting models demonstrated

appreciable depletion of susceptible animals that occurred at local scales because of clusters of deaths and

dogs already incubating infection. Individual variation in rabid dog behavior facilitated virus dispersal and

cocirculation of virus lineages, enabling metapopulation persistence. These mechanisms have important

implications for prediction and control of pathogens that circulate in spatially structured populations.

U

nderstanding the processes that regu-

late endemic disease dynamics remains

a long-standing challenge in epidemio-

logy ( 1 , 2 ), and the mechanisms that

enable long-term persistence at low pre-

valence remain largely unexplored ( 3 ). This

is particularly true for canine rabies, a fatal

zoonotic virus for which naturally acquired

immunity has not been demonstrated. The

basic reproductive number R 0 of rabies, which

is defined as the expected number of sec-

ondary cases produced by a typical infectious

individual in a fully susceptible population

( 4 ), is low (between 1.1 and 2) and is relatively

insensitive to dog density ( 5 ), making the dis-

ease amenable to elimination through dog vac-

cination ( 6 ). Yet dog-mediated rabies remains

endemic across Africa and Asia, where it kills

tens of thousands of people every year ( 7 ), and

its persistent circulation at such low preva-

lence in largely unvaccinated populations is

an enduring enigma.

Rabies is, however, a usually tractable sys-

tem for understanding how population-level

patterns of infection emerge from pathogen

transmission at the individual level. Rabies is

transmitted through bites, which can often be

observed, and the clinical signs are readily

identifiable, with infected animals typically

dying within 1 week of disease onset (Fig. 1E).

Capitalizing on these distinctive characteris-

tics, we conducted exhaustive contact tracing

to generate spatially resolved data on rabies

infection and transmission in Serengeti district,

Northern Tanzania, between January 2002

and December 2015. Serengeti district adjoins

other populated districts to the north and west

and Serengeti National Park to the southeast

(Fig. 1A). We previously showed that domestic

dogs maintain rabies in this part of Tanzania,

with infrequent spillover to wildlife and spill-

back to domestic dogs ( 8 ). In Serengeti dis-

trict’s population of around 50,000 dogs (and

250,000 people), we traced 3612 rabies infec-

tions (comprising 3081 cases in dogs, 75 in

cats, 145 in wildlife, and 311 in livestock) (Fig. 1),

along with 6684 potential transmission events

to other animals and 1462 people bitten by

rabid animals, of whom 44 died from rabies.

Most identified cases could be statistically

512 29 APRIL 2022•VOL 376 ISSUE 6592 science.orgSCIENCE

(^1) Institute of Biodiversity, Animal Health and Comparative
Medicine, University of Glasgow, Glasgow, UK.^2 Department of
Ecology and Evolutionary Biology, Princeton University,
Princeton, NJ, USA.^3 Department of Veterinary Medicine and
Public Health, Sokoine University of Agriculture, Morogoro,
Tanzania.^4 Ifakara Health Institute, Dar es Salaam, Tanzania.
(^5) Serengeti District Veterinary Office, Mugumu, Tanzania. (^6) The
Zeeman Institute for Systems Biology and Infectious Disease
Epidemiology Research, University of Warwick, Warwick, UK.
*Corresponding author. Email: [email protected]
RESEARCH | REPORTS