Self-Medication in Animals Jacobus C

Self-medication in animals Jacobus C. de Roode, Thierry Lefèvre, Mark D. Hunter Science, April 12, 2013 A.k.a zoopharmacognosy

• Self-medication in animals typically evokes images of chimpanzees seeking out medicinal herbs to treat their diseases

• Belief that self-medication is associated with high cognitive abilities (learning...)

• Many animals can use medication through innate rather than learned responses. Animal pharmacists: moths, ants, fruit ﬁles...

• Antiparasite self-medication Medication

• Typical view: chewing non-nutritive substances such as plant piths or leaves.

• Increased ingestion of particular chemicals that are already in their diets PERSPECTIVES

ECOLOGY

Animal self-medication against parasites is more widespread than previously thought, with Self-Medication in Animals profound implications for host-parasite biology. Jacobus C. de Roode,1 * Thierry Lefèvre,2 Mark D. Hunter3

he concept of antiparasite self-med- Therapeutic and prophylactic medica- their eggs in high-ethanol food when they ication in animals typically evokes tion can be further divided depending on detect the presence of parasitoid wasps (8 );

images of chimpanzees seeking out the target of medication (see the figure). this reduces infection risk in their offspring DE O

T O medicinal herbs to treat their diseases (1 , Much work has focused on cases in which (transgenerational prophylaxis). Wood ants R

2). These images stem partly from the belief animals medicate themselves, including incorporate antimicrobial resin from coni- DE 1 C.

that animals can medicate themselves only baboons and woolly bear caterpillars ( , fer trees into their nests, preventing micro- BUS 4 6 5 O

when they have high cognitive abilities that , ), but animals may medicate their off- bial growth in the colony ( ) (social prophy- AC J / Y

allow them to observe, learn, and make con- spring or other genetic kin instead. Fruit laxis). Parasite-infected monarch butterﬂ ies L F R

3 E

scious decisions ( ). However, any concept ﬂ ies have been shown to preferentially lay can protect their offspring against high lev- T

of self-medication based solely on learning BUT is inadequate. Many animals can use med- H ARC

Types of animal medication N

ication through innate rather than learned O M responses. The growing list of animal phar- Behavior displayed by: ; macists includes moths (4 ), ants (5 ), and Healthy individual Diseased individual ARRAS

6 D fruit ﬂ ies ( ). The fact that these animals Prophylactic self-medication Therapeutic self-medication O G

self-medicate has profound implications for HU T/

Chewthe ecology and and swallow evolution ofplant animal hosts N A on April 17, 2013 D

and their parasites. O materials with antiparasitic O

2 W Janzen ( ) was the ﬁ rst to describe cases ; in which diseased vertebrates appeared to CK Plant toxins

properties TO S

select secondary plant compounds with anti- ER P

U ingestion to kill S

parasitic activity. Consequently, self-medi- / S

Self L cation has often been deﬁ ned as the antipar- A

M parasites I asitic use of secondary plant chemicals or N A S L

other non-nutritive substances by herbivores A M I www.sciencemag.org (1 ). However, boundaries between nutrients, N A / medicines, and toxins are permeable and are Y T FL T often deﬁ ned only by the ingested dose of Ethiopian baboon Papio anubis Woolly Bear Caterpillar Grammia incorrupta I RU F

7 ; a chemical ( ). Thus, whereas traditional R E n Transgenerational therapeutic medication G o N i

examples of animal medication involve ani- I

Transgenerational prophylaxis (offspring) (offspring) S

at EL mals eating speciﬁ c plants only when dis- c i A

1 d CH e

eased ( ), recent examples include animals I increasing the ingestion of particular chemi- M f m Downloaded from AR/ L L o

4 I

cals that are already in their diets ( ). t e ERP g Animals may use chemicals to relieve T ar CA symptoms that are not caused by parasitic T AR BE diseases, but we restrict our discussion to Y L L

self-medication as a defense against para- O O W

sites. Such defenses can come in two gen- ;

Fruit fly Drosophila melanogaster S N

eral forms (see the ﬁ gure). In therapeutic O M

medication, diseased individuals alter their Kin M Social prophylaxis (other relatives) CO

behavior to medicate in response to para- A DI site infection (4 ). In contrast, prophylaxis is E M I K used by infected and uninfected individuals I W / E

alike to prevent parasite infection, often in F UF

response to high parasite risk (5 ). O T G I B

1 E Department of Biology, Emory University, 1510 Clifton H 2 T Road, Atlanta, GA 30322, USA. Maladies Infectieuses et N Vecteurs: Écologie, Génétique, Évolution et Contrôle (UM1- O UM2-CNRS 5290-IRD 224), Institut de Recherche pour le BABO : S

Développement, 911 Avenue Agropolis, BP 64501, Mont- T

3 Wood ant Formica paralugubris Monarch butterfly Danaus plexippus DI

pellier 34394, France. Department of Ecology and Evo- E CR lutionary Biology, University of Michigan, 2053 Natural O Sciences Building, 830 North University, Ann Arbor, MI T HO

48109–1048, USA. E-mail: [email protected] Types of animal medication. P

150 12 APRIL 2013 VOL 340 SCIENCE www.sciencemag.org Published by AAAS PERSPECTIVES

ECOLOGY

images of chimpanzees seeking out the target of medication (see the figure). this reduces infection risk in their offspring DE O

T O medicinal herbs to treat their diseases (1 , Much work has focused on cases in which (transgenerational prophylaxis). Wood ants R

2). These images stem partly from the belief animals medicate themselves, including incorporate antimicrobial resin from coni- DE 1 C.

that animals can medicate themselves only baboons and woolly bear caterpillars ( , fer trees into their nests, preventing micro- BUS 4 6 5 O

when they have high cognitive abilities that , ), but animals may medicate their off- bial growth in the colony ( ) (social prophy- AC J / Y

allow them to observe, learn, and make con- spring or other genetic kin instead. Fruit laxis). Parasite-infected monarch butterﬂ ies L F R

3 E

scious decisions ( ). However, any concept ﬂ ies have been shown to preferentially lay can protect their offspring against high lev- T

of self-medication based solely on learning BUT is inadequate. Many animals can use med- H ARC

Types of animal medication N

6 D fruit ﬂ ies ( ). The fact that these animals Prophylactic self-medication Therapeutic self-medication O G

self-medicate has profound implications for HU T/

the ecology and evolution of animal hosts N A on April 17, 2013 D

and their parasites. O O

2 W Janzen ( ) was the ﬁ rst to describe cases ; in which diseased vertebrates appeared to CK TO S

select secondary plant compounds with anti- ER P U S

parasitic activity. Consequently, self-medi- / S

Self L cation has often been deﬁ ned as the antipar- A M I asitic use of secondary plant chemicals or N A S L

7 ; a chemical ( ). Thus, whereas traditional R E n Transgenerational therapeutic medication G o N i

examples of animal medication involve ani- I

Transgenerational prophylaxis (offspring) (offspring) S

at EL mals eating speciﬁ c plants only when dis- c i A

1 d CH e

eased ( ), recent examples include animals I increasing the ingestion of particular chemi- M f m Downloaded from AR/ L L o

4 I

cals that are already in their diets ( ). t e ERP g LayAnimals down may eggs use chemicals in high- to relieve T ar CA symptoms that are not caused by parasitic T ethanol food in the presence AR BE diseases, but we restrict our discussion to Y L L

self-medicationof parasitoid as a defense wasps against para- O O W

sites. Such defenses can come in two gen- ;

Fruit fly Drosophila melanogaster S N

eral forms (see the ﬁ gure). In therapeutic O M

medication, diseased individuals alter their Kin M Social prophylaxis (other relatives) CO

behavior to medicate in response to para- A DI site infection (4 ). In contrast, prophylaxis is E M I K used by infected and uninfected individuals I W / E

alike to prevent parasite infection, often in F UF

Incorporateresponse to high parasiteantimicrobial risk (5 ). O T G I B

resin1 from conifer trees into E Department of Biology, Emory University, 1510 Clifton H 2 T Road, Atlanta, GA 30322, USA. Maladies Infectieuses et N Vecteurs: Écologie,their Gén étiquenests, Évolution et Contrôle (UM1- O UM2-CNRS 5290-IRD 224), Institut de Recherche pour le BABO : S

Développement, 911 Avenue Agropolis, BP 64501, Mont- T

3 Wood ant Formica paralugubris Monarch butterfly Danaus plexippus DI

pellier 34394, France. Department of Ecology and Evo- E CR lutionary Biology, University of Michigan, 2053 Natural O Sciences Building, 830 North University, Ann Arbor, MI T HO 48109–1048, USA. E-mail: [email protected] Types of animal medication. Parasite-infectedP butterﬂies 150 12 APRIL 2013 VOL 340 SCIENCE www.sciencemag.org protect their offspring against Published by AAAS parasites by laying their eggs on antiparasitic milkweed Medication and consequences on host-parasite interaction

• What is the impact of the medication on the parasite transmission and virulence evolution? Preliminary evidence for some effects...

• Effects of medication on the evolution of the immune systems: medication provides an alternative to immune responses. • In honeybees: medication behaviors (e.g. antimicrobial resin into their nests) but lack of several genes associated with the immune system, which are present in other insects. Implications for human food production and health

• Human interference with ability of agricultural organisms to self-medicate. • For example, beekeepers select bees with reduced resin deposition, which is thought to be linked with increases in parasitism and disease in honeybees.

• As self-medicating animals, humans derive many of their medicines from natural products, such as plants. Studies of animal medication may lead to the discovery of new drugs for human health.