HAL Id: hal-02410979https://hal.archives-ouvertes.fr/hal-02410979

Submitted on 21 Sep 2020

HAL is a multi-disciplinary open accessarchive for the deposit and dissemination of sci-entific research documents, whether they are pub-lished or not. The documents may come fromteaching and research institutions in France orabroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, estdestinée au dépôt et à la diffusion de documentsscientifiques de niveau recherche, publiés ou non,émanant des établissements d’enseignement et derecherche français ou étrangers, des laboratoirespublics ou privés.

Distributed under a Creative Commons Attribution| 4.0 International License

Evolutionary perspectives on human infectious diseases:Challenges, advances, and promisesPierre Echaubard, James Rudge, Thierry Lefèvre

To cite this version:Pierre Echaubard, James Rudge, Thierry Lefèvre. Evolutionary perspectives on human infectiousdiseases: Challenges, advances, and promises. Evolutionary Applications, Blackwell, 2018, 11 (4),pp.383-393. �10.1111/eva.12586�. �hal-02410979�

Evolutionary Applications. 2018;11:383–393.  | 383wileyonlinelibrary.com/journal/eva

DOI: 10.1111/eva.12586

E D I T O R I A L

Evolutionary perspectives on human infectious diseases: Challenges, advances, and promises

1  | INTRODUC TION

Modern biomedicine has contributed remarkably to the reduction of infectious diseases worldwide, including the eradication of smallpox and the control of common childhood diseases (e.g., polio, measles, rubella) that once claimed millions of lives and caused suffering of tens of millions. This has been made possible through improved di-agnostics, surveillance, therapeutics, vaccines, and an associated health system infrastructure. These achievements can be largely credited to advances in biomedical sciences and their application in the 20th century.

The spectacular advances in the biomedical sciences were in turn a consequence of the emergence and widespread acceptance of the biomedical paradigm, in which the discovery of microbes and establishment of ‘germ theory’ had played a central role. By the 1960s, a sense began to prevail that infectious diseases had been conquered, or were at least conquerable in the case of malaria, den-gue, and other vector- borne diseases (VBD) that appeared to be “in retreat.”

Yet, by the 1980s, with the appearance of the HIV/AIDS pan-demic and followed by new antimicrobial- resistant strains of bacterial pathogens, confidence began to erode. Major setbacks also increasingly became apparent in the efforts to control VBDs particularly with the resurgence of malaria and dengue worldwide (WHO, 2016). An increasing number of historically localized or otherwise geographically confined VBDs began to spread and even jump continents, with the arrival of West Nile virus and Zika virus in the Americas being the most prominent of many examples. Such pathogens, identified decades ago in their native habitat and hosts as part of natural history studies, were long considered to be of relatively little public health concern or apparent impact (Lederberg, Shope, & Oaks, 1992; Packard, 2007).

Human population growth and anthropogenic environmental changes, accelerating with an unprecedented intensity and scale particularly since the mid- 1900s, are increasingly recognized as underlying much of the emerging infectious diseases (EID) prob-lem (Myers & Patz, 2009; Myers et al., 2013; Whitmee et al., 2015). These disease emergence drivers emblematic of the era of modern

development can be seen as consequences of modern medical and hygiene interventions introduced a century earlier. Together, they radically modified (and continue to alter) landscapes and ecosys-tems worldwide producing what has become a continual state of social, ecological, and evolutionary imbalance (McNeill, 1976). Among the environmental changes, global climate change has be-come widely accepted among experts as a significant contributor to these imbalances that will increasingly influence infectious dis-eases transmission, yet in ways that are difficult to predict (Altizer, Ostfeld, Johnson, Kutz, & Harvell, 2013; Lafferty, 2009; McMichael & Wilcox, 2009).

The complexity of factors and processes underlying infectious diseases and their transmission go well beyond the scope and an-alytic resolution of biomedicine (and conventional biomedical training), requiring a complementary framing approach capable of acknowledging and assessing cross- scale influences, context dependency, and the constant ‘arms race’ between co- evolving organisms (Van Valen, 1973). Evolutionary biology provides these scientific foundations to help refine our understanding of not only the meaning of health and disease (Stearns & Koella, 2008) from the standpoint of adaptation (or maladaptation), but also improve our understanding of the mechanisms underlying infectious disease transmission dynamics within social- ecological systems (Horwitz & Wilcox, 2005; Wilcox & Echaubard, 2016), context- dependent virulence and more effective treatment and control strategies (Echaubard, Sripa, Mallory, & Wilcox, 2016; Nesse, 2008; Restif, 2009). As such, evolutionary biology as a framing approach and methodological toolkit is a needed component of integrated dis-ease control and prevention (Allegranzi et al., 2017) and sustainable health development aligning with the recently adopted sustain-able development goals (SDGs), as part of the 2030 Agenda for Sustainable Development (Carroll et al., 2014).

This special issue is an attempt to present an up- to- date appraisal of the challenges, current advances, and promising research avenues where evolutionary principles and their ecological corollaries can be applied in research as a basis for human infectious disease in-terventions. Accordingly, the contributions published in this special issue together present an illustration of the diverse benefits of com-bining biomedical and public health perspectives with evolutionary

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.© 2018 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

384  |     EDITORIAL

causation in the context of infectious diseases for major infectious agents (Table 1).

2  | THEMES OF THE SPECIAL ISSUE

A main challenge of mainstreaming evolution into medicine and public health lies in the often very pragmatic and urgent nature of these fields (e.g., outbreak mitigation; Nesse & Stearns, 2008) and the relatively time- consuming nature of framing questions, interven-tions, and policies following evolutionary principles, which imply a long- term preventive vision rather than a short- term curative do-main of action. However, policy- oriented research and intervention informed by evolutionary biology have the potential to not only ef-fectively mitigate urgent crises but also anticipate, minimize, and respond to the evolution of unwanted epidemiological traits (e.g., antimicrobial resistance). Accordingly, the articles compiled for this special issue present a selected panel of evolutionary applications for infectious disease control, together providing relevant avenues for future research and sustainable disease prevention strategies.

The articles published in this special issue are organized based on their underlying evolutionary innovation and public health implica-tions and not necessarily on the disease study systems the authors are using to address their research questions. A range of disease systems, from macroparasites to microparasites (sensu Anderson & May, 1981), are examined through modeling, experimental and observational research designs as well as describing novel framing approaches.

As an opening paper, Kosoy and Kosoy (2017) explore the mul-tiple dimensions and related complexity of host–pathogens interac-tions revealed by the novel genetic and genomic data, along with extensive environmental parameters being acquired using newly de-veloped computational tools. They highlight the need for flexibility in studying natural systems of zoonotic pathogens with respect to how we choose perspectives within a continuum between unrestricted diversity of related parameters and well- defined roles played by in-fectious agents, potential and actual animal hosts, and environmen-tal variables. They proposed a model of investigation that requires a dynamic shift of perspectives along the simplicity–complexity (‘sim-plexity’) dimension emphasizing the difficulty to accommodate dual representations of both the subjective nature of investigations of zoonotic pathogens and much more objectively derived information, for example, coded in the genetic structure of DNA or in observing the morphology or behavior of bacteria. This also speaks directly to the issue of “problem framing” alluded to in this introduction where tools and perceptions emerging from biomedical sciences do not necessarily accommodate evolutionary- based predictions or public health implications.

Arguably the most widespread recognition of the importance of evolutionary biology for public health and medicine is in the con-text of the emergence of resistance to antimicrobials and insecti-cides. Sternberg and Thomas (2017) explore the overlaps between understanding and managing insecticide resistance in agriculture

and in public health with the aim to identify best practices in resis-tance mitigation strategies in the context of vector- borne disease interventions. They argue that the success of insecticide resistance management strategies is strongly dependent on the biological spe-cifics of each system and that the biological, operational, and reg-ulatory differences between agriculture and public health limit the wholesale transfer of knowledge and practices from one system to the other. Nonetheless, the authors argue that there are some valuable insights from agriculture that could assist in advancing the existing Global Plan for Insecticide Resistance Management (IRM). Accordingly, the authors suggest that for IRM strategies to succeed in public health, there needs to be a shift away from choosing vector control tools or strategies based on direct cost, toward factoring in the benefit of preserving susceptibility.

Focusing on Malaria, Huijben and Paaijmans (2017) analyze the evolutionary consequences of the way antimalarial drugs and insecticide- based interventions are currently implemented, which is leading to resistance and may ultimately lead to control failure. The authors describe how evolutionary principles can be applied to extend the lifespan of current and novel interventions highlighting in particular how understanding fitness costs arising from express-ing, utilizing, and maintaining molecular or metabolic pathways of resistance will be essential to mitigate resistance evolution. They continue arguing that similar to insecticide resistance management strategies, large heterogeneity in drug exposure can be created in space (host mosaic) or time (drug rotation) or by deploying different compounds simultaneously (mixed treatment) and that better resis-tance management is achieved if drugs can be combined that select for alternative allelic versions of the target locus.

Glunt et al. (2017) further discuss the challenges of insecti-cide resistance in the context of malaria, with a specific focus on pyrethroids impregnated long- lasting insecticidal bed nets (LLINs) and their efficacy in preventing malaria. About 1 billion LLINs, a major vector control tool, have been distributed in Africa in the last 10 years. During the same period of time resistance to pyrethroids in malaria mosquito vectors has increased significantly. Using a trans-mission model, the authors show that when LLIN- related lethal and sublethal effects were accrued over mosquito lifetimes, they greatly reduced the impact of resistance on malaria transmission potential under conditions of high net coverage. However if coverage falls, the epidemiological impact is far more pronounced. Similarly, if the in-tensity of resistance intensifies, the loss of malaria control increases nonlinearly. The authors argue that their findings help explain why insecticide resistance has not yet led to wide- scale failure of LLINs, as high distribution coverage is generally in place in most African endemic countries, but reinforce the call for alternative control tools and informed resistance management strategies.

While parasites can evolve classical resistance mechanisms (e.g., efflux pumps), it is also possible that changes in life- history traits could help parasites evade the effects of treatment. Birget, Greischar, Reece, and Mideo (2017) investigate how the life history of malaria parasites is governed by an intrinsic resource allocation problem where specialized stages are required for transmission, but

     |  385EDITORIAL

TABLE 1 

Sum

mar

y of

pub

lic h

ealth

dat

a, re

gula

r dia

gnos

tic a

nd tr

eatm

ent,

mai

n co

ntro

l str

ateg

y as

wel

l as

chal

leng

es fo

r con

trol

of t

he d

isea

se in

vest

igat

ed in

this

spe

cial

issu

e

Dis

ease

Publ

ic h

ealth

situ

atio

nD

iagn

ostic

& tr

eatm

ent

Cont

rol s

trat

egy

Chal

leng

es fo

r con

trol

Mal

aria

a•

212

mill

ion

new

cas

es o

f mal

aria

wor

ldw

ide

in

2015

• Th

e W

HO

Afr

ican

Reg

ion

acco

unte

d fo

r mos

t gl

obal

cas

es o

f mal

aria

(90%

), fo

llow

ed b

y th

e So

uth-

East

Asi

a (S

EA) R

egio

n (7

%) a

nd th

e Ea

ster

n M

edite

rran

ean

Regi

on (2

%).

• In

201

5, th

ere

wer

e an

est

imat

ed 4

29 0

00

mal

aria

dea

ths

wor

ldw

ide

(Afr

ica

92%

, SEA

Re

gion

6%

, Med

iterr

anea

n Re

gion

2%

).•

Betw

een

2010

and

201

5, m

alar

ia in

cide

nce

rate

s fe

ll by

21%

glo

bally

and

in th

e A

fric

an R

egio

n.

Dur

ing

this

sam

e pe

riod,

mal

aria

mor

talit

y ra

tes

fell

by a

n es

timat

ed 2

9% g

loba

lly a

nd b

y 31

% in

th

e A

fric

an R

egio

n.•

Sinc

e 20

10, t

he m

alar

ia m

orta

lity

rate

dec

lined

by

58%

in th

e W

este

rn P

acifi

c Re

gion

, by

46%

in

the

SEA

Reg

ion,

by

37%

in th

e Re

gion

of t

he

Am

eric

as, a

nd b

y 6%

in th

e Ea

ster

n M

edite

rran

ean

Regi

on. I

n 20

15, t

he E

urop

ean

Regi

on w

as m

alar

ia fr

ee•

In 2

015,

mal

aria

kill

ed a

n es

timat

ed 3

03,0

00

unde

r-fiv

es g

loba

lly, i

nclu

ding

292

,000

in th

e A

fric

an R

egio

n. B

etw

een

2010

and

201

5, th

e m

alar

ia m

orta

lity

rate

am

ong

child

ren

unde

r 5

fell

by a

n es

timat

ed 3

5%. N

ever

thel

ess,

mal

aria

re

mai

ns a

maj

or k

iller

of u

nder

-fiv

es, c

laim

ing

the

life

of 1

chi

ld e

very

2 m

in.

• W

HO

reco

mm

ends

dia

gnos

tic te

stin

g fo

r all

peop

le w

ith s

uspe

cted

mal

aria

be

fore

trea

tmen

t is

adm

inis

tere

d.•

Rapi

d di

agno

stic

test

ing

(RD

Ts),

intr

oduc

ed w

idel

y ov

er th

e pa

st

deca

de, h

as m

ade

it ea

sier

to s

wift

ly

dist

ingu

ish

betw

een

mal

aria

l and

no

nmal

aria

l fev

ers,

ena

blin

g tim

ely

and

appr

opria

te tr

eatm

ent.

• In

201

5, a

ppro

xim

atel

y ha

lf (5

1%) o

f ch

ildre

n w

ith a

feve

r who

sou

ght c

are

at a

pub

lic h

ealth

faci

lity

in 2

2 A

fric

an

coun

trie

s re

ceiv

ed a

mal

aria

di

agno

stic

test

com

pare

d to

29%

in

2010

.•

Art

emis

inin

-bas

ed c

ombi

natio

n th

erap

ies

(AC

Ts) a

re h

ighl

y ef

fect

ive

agai

nst P

. fal

cipa

rum

, the

mos

t pr

eval

ent a

nd le

thal

mal

aria

par

asite

af

fect

ing

hum

ans.

• G

loba

lly, t

he n

umbe

r of A

CT

trea

tmen

t cou

rses

pro

cure

d fr

om

man

ufac

ture

rs in

crea

sed

from

187

m

illio

n in

201

0 to

a p

eak

of 3

93

mill

ion

in 2

013,

but

sub

sequ

ently

fell

to 3

11 m

illio

n in

201

5.

• Ve

ctor

con

trol

is th

e m

ain

way

to

prev

ent a

nd re

duce

mal

aria

tr

ansm

issi

on.

• Tw

o fo

rms

of v

ecto

r con

trol

are

ef

fect

ive

in a

wid

e ra

nge

of

circ

umst

ance

s: in

sect

icid

e-tr

eate

d m

osqu

ito n

ets

(ITN

s) a

nd in

door

re

sidu

al s

pray

ing

(IRS)

.•

Ove

r the

last

5 y

ears

, the

use

of

trea

ted

nets

in th

e re

gion

has

in

crea

sed

sign

ifica

ntly

: in

2015

, an

estim

ated

53%

of t

he p

opul

atio

n at

ris

k sl

ept u

nder

a tr

eate

d ne

t co

mpa

red

to 3

0% in

201

0.•

In 2

015,

106

mill

ion

peop

le g

loba

lly

wer

e pr

otec

ted

by IR

S, in

clud

ing

49

mill

ion

peop

le in

Afr

ica.

The

pr

opor

tion

of th

e po

pula

tion

at ri

sk

of m

alar

ia p

rote

cted

by

IRS

decl

ined

fr

om a

pea

k of

5.7

% g

loba

lly in

201

0 to

3.1

% in

201

5.

• A

rtem

isin

in re

sist

ance

mos

tly

in th

e M

ekon

g su

breg

ion,

at

Thai

land

–Mya

nmar

and

Th

aila

nd–C

ambo

dia

bord

ers.

• M

osqu

ito re

sist

ance

to

inse

ctic

ides

• C

ompo

sitio

n of

Ano

phel

es

spec

ies

com

plex

es h

ave

impo

rtan

t im

plic

atio

ns fo

r co

ntro

l str

ateg

ies

• Tr

ansb

ound

ary

labo

r mig

ratio

n•

Inte

nsiv

e ag

ricul

tura

l cro

ppin

g sy

stem

s, s

uch

as fr

uit o

rcha

rds,

in

crea

se th

e lik

elih

ood

of

inse

ctic

ide

resi

stan

ce

deve

lopm

ent i

n m

alar

ia

mos

quito

es

(Con

tinue

s)

386  |     EDITORIAL

Dis

ease

Publ

ic h

ealth

situ

atio

nD

iagn

ostic

& tr

eatm

ent

Cont

rol s

trat

egy

Chal

leng

es fo

r con

trol

Den

gueb

• O

ne re

cent

est

imat

e in

dica

tes

390

mill

ion

deng

ue in

fect

ions

per

yea

r (95

% c

redi

ble

inte

rval

28

4–52

8 m

illio

n), o

f whi

ch 9

6 m

illio

n (6

7–13

6 m

illio

n) m

anife

st c

linic

ally

• Th

e pr

eval

ence

of d

engu

e is

est

imat

ed a

t 3.9

bi

llion

peo

ple,

in 1

28 c

ount

ries,

at r

isk

of

infe

ctio

n w

ith d

engu

e vi

ruse

s•

The

num

ber o

f cas

es re

port

ed in

crea

sed

from

2.

2 m

illio

n in

201

0 to

3.2

mill

ion

in 2

015.

• Be

fore

197

0, o

nly

9 co

untr

ies

had

expe

rienc

ed

seve

re d

engu

e ep

idem

ics.

The

dis

ease

is n

ow

ende

mic

in m

ore

than

100

cou

ntrie

s in

the

WH

O

regi

ons

of A

fric

a, th

e A

mer

icas

, the

Eas

tern

M

edite

rran

ean,

SEA

, and

the

Wes

tern

Pac

ific.

• C

ases

acr

oss

the

Am

eric

as, S

outh

-Eas

t Asi

a, a

nd

Wes

tern

Pac

ific

exce

eded

1.2

mill

ion

in 2

008

and

over

3.2

mill

ion

in 2

015.

Rec

ently

, the

nu

mbe

r of r

epor

ted

case

s ha

s co

ntin

ued

to

incr

ease

. In

2015

, 2.3

5 m

illio

n ca

ses

of d

engu

e w

ere

repo

rted

in th

e A

mer

icas

alo

ne, o

f whi

ch

10,2

00 c

ases

wer

e di

agno

sed

as s

ever

e de

ngue

ca

usin

g 11

81 d

eath

s.•

An

estim

ated

500

,000

peo

ple

with

sev

ere

deng

ue re

quire

hos

pita

lizat

ion

each

yea

r, an

d ab

out 2

.5%

of t

hose

aff

ecte

d di

e.

• D

engu

e fe

ver i

s a

seve

re, f

lu-li

ke

illne

ss th

at a

ffec

ts in

fant

s, y

oung

ch

ildre

n, a

nd a

dults

• D

engu

e sh

ould

be

susp

ecte

d w

hen

a hi

gh fe

ver i

s ac

com

pani

ed b

y se

vere

he

adac

he, p

ain

behi

nd th

e ey

es,

mus

cle

and

join

t pai

ns, n

ause

a,

vom

iting

, sw

olle

n gl

ands

or r

ash.

• Se

vere

den

gue

is a

pot

entia

lly d

eadl

y co

mpl

icat

ion

due

to p

lasm

a le

akin

g,

fluid

acc

umul

atio

n, s

ever

e bl

eedi

ng, o

r or

gan

impa

irmen

t.•

Ther

e is

no

spec

ific

trea

tmen

t for

de

ngue

feve

r. M

aint

enan

ce o

f the

pa

tient

’s bo

dy fl

uid

volu

me

is c

ritic

al

to s

ever

e de

ngue

car

e.•

In la

te 2

015

and

early

201

6, th

e fir

st

deng

ue v

acci

ne, D

engv

axia

(CYD

-TD

V) b

y Sa

nofi

Past

eur,

was

re

gist

ered

in s

ever

al c

ount

ries

for u

se

in in

divi

dual

s 9–

45 y

ears

of a

ge li

ving

in

end

emic

are

as.

• W

HO

reco

mm

ends

that

cou

ntrie

s sh

ould

con

side

r int

rodu

ctio

n of

the

deng

ue v

acci

ne C

YD-T

DV

onl

y in

ge

ogra

phic

al s

ettin

gs w

here

ep

idem

iolo

gica

l dat

a in

dica

te a

hig

h bu

rden

of d

isea

se.

At p

rese

nt, t

he m

ain

met

hod

to c

ontr

ol

or p

reve

nt th

e tr

ansm

issi

on o

f de

ngue

viru

s is

to c

omba

t vec

tor

mos

quito

es th

roug

h:•

Prev

entin

g m

osqu

itoes

from

ac

cess

ing

egg-

layi

ng h

abita

ts b

y en

viro

nmen

tal m

anag

emen

t and

m

odifi

catio

n•

Dis

posi

ng o

f sol

id w

aste

and

co

verin

g, e

mpt

ying

, and

cle

anin

g of

do

mes

tic w

ater

sto

rage

con

tain

ers

on a

wee

kly

basi

s •

App

lyin

g ap

prop

riate

inse

ctic

ides

to

wat

er s

tora

ge o

utdo

or c

onta

iner

s an

d en

viro

nmen

tal m

anag

emen

t•

Usi

ng o

f per

sona

l hou

seho

ld

prot

ectio

n su

ch a

s w

indo

w s

cree

ns,

long

-sle

eved

clo

thes

, ins

ectic

ide-

trea

ted

mat

eria

ls, c

oils

, and

va

poriz

ers;

• Im

prov

ing

com

mun

ity p

artic

ipat

ion

and

mob

iliza

tion

for s

usta

ined

ve

ctor

con

trol

• In

crea

sing

pop

ulat

ion

mov

emen

t, gl

obal

izat

ion

of

trad

e an

d ur

bani

zatio

n w

ithou

t ad

equa

te m

easu

res

to p

reve

nt

vect

or b

reed

ing

• Ru

bber

pla

ntat

ions

exp

ansi

on•

Mos

quito

vec

tor a

nd p

atho

gen

adap

tatio

n

(Con

tinue

s)

TABLE 1 

(Con

tinue

d)

     |  387EDITORIAL

Dis

ease

Publ

ic h

ealth

situ

atio

nD

iagn

ostic

& tr

eatm

ent

Cont

rol s

trat

egy

Chal

leng

es fo

r con

trol

Influ

enza

(z

oono

tic)

• H

uman

s ca

n be

infe

cted

with

avi

an, s

win

e, a

nd

othe

r zoo

notic

influ

enza

viru

ses,

suc

h as

avi

an

influ

enza

viru

s su

btyp

es A

(H5N

1), A

(H7N

9), a

nd

A(H

9N2)

and

sw

ine

influ

enza

viru

s su

btyp

es

A(H

1N1)

, A(H

1N2)

, and

A(H

3N2)

.•

The

maj

ority

of h

uman

cas

es o

f inf

luen

za A

(H

5N1)

and

A(H

7N9)

viru

s in

fect

ion

have

bee

n as

soci

ated

with

dire

ct o

r ind

irect

con

tact

with

in

fect

ed li

ve o

r dea

d po

ultr

y. C

ontr

ollin

g th

e di

seas

e in

the

anim

al s

ourc

e is

crit

ical

to

decr

ease

risk

to h

uman

s.•

Aqu

atic

bird

s ar

e th

e pr

imar

y na

tura

l res

ervo

ir fo

r mos

t sub

type

s of

influ

enza

A v

iruse

s. M

ost

caus

e as

ympt

omat

ic o

r mild

infe

ctio

n in

bird

s,

whe

re th

e ra

nge

of s

ympt

oms

depe

nds

on th

e vi

rus

prop

ertie

s.•

Viru

ses

that

cau

se s

ever

e di

seas

e in

pou

ltry

and

resu

lt in

hig

h de

ath

rate

s ar

e ca

lled

high

ly

path

ogen

ic a

vian

influ

enza

(HPA

I). V

iruse

s th

at

caus

e m

ild d

isea

se in

pou

ltry

are

calle

d lo

w-p

atho

geni

c av

ian

influ

enza

(LPA

I).

• Av

ian,

sw

ine,

and

oth

er z

oono

tic

influ

enza

viru

s in

fect

ions

in h

uman

s m

ay c

ause

dis

ease

rang

ing

from

mild

up

per r

espi

rato

ry tr

act i

nfec

tion

(feve

r and

cou

gh),

early

spu

tum

pr

oduc

tion,

and

rapi

d pr

ogre

ssio

n to

se

vere

pne

umon

ia, s

epsi

s w

ith s

hock

, ac

ute

resp

irato

ry d

istr

ess

synd

rom

e an

d ev

en d

eath

.•

Labo

rato

ry te

sts

are

requ

ired

to

diag

nose

hum

an in

fect

ion

with

zo

onot

ic in

fluen

za.

• Ra

pid

influ

enza

dia

gnos

tic te

sts

(RID

Ts) h

ave

low

er s

ensi

tivity

co

mpa

red

to P

CR

and

thei

r rel

iabi

lity

depe

nds

larg

ely

on th

e co

nditi

ons

unde

r whi

ch th

ey a

re u

sed.

• Ev

iden

ce s

ugge

sts

that

som

e an

tivira

l dr

ugs,

not

ably

neu

ram

inid

ase

inhi

bito

r (os

elta

miv

ir, z

anam

ivir)

, can

re

duce

the

dura

tion

of v

iral r

eplic

atio

n an

d im

prov

e pr

ospe

cts

of s

urvi

val;

how

ever

, ong

oing

clin

ical

stu

dies

are

ne

eded

.•

In s

uspe

cted

and

con

firm

ed c

ases

, ne

uram

inid

ase

inhi

bito

rs s

houl

d be

pr

escr

ibed

as

soon

as

poss

ible

to

max

imiz

e th

erap

eutic

ben

efits

.

• In

fluen

za v

iruse

s, w

ith th

e va

st

sile

nt re

serv

oir i

n aq

uatic

bird

s, a

re

impo

ssib

le to

era

dica

te.

• To

min

imiz

e pu

blic

hea

lth ri

sk,

qual

ity s

urve

illan

ce in

bot

h an

imal

an

d hu

man

pop

ulat

ions

, tho

roug

h in

vest

igat

ion

of e

very

hum

an

infe

ctio

n an

d ris

k-ba

sed

pand

emic

pl

anni

ng a

re e

ssen

tial.

• A

part

from

ant

ivira

l tre

atm

ent,

the

publ

ic h

ealth

man

agem

ent

incl

udes

per

sona

l pro

tect

ive

mea

sure

s lik

e re

gula

r han

d w

ashi

ng,

good

resp

irato

ry h

ygie

ne a

nd e

arly

se

lf-is

olat

ion

of th

ose

feel

ing

unw

ell,

feve

rish

and

havi

ng o

ther

sy

mpt

oms

of in

fluen

za.

• Pr

e-ex

posu

re o

r pos

texp

osur

e pr

ophy

laxi

s w

ith a

ntiv

irals

is

poss

ible

but

dep

ends

on

seve

ral

fact

ors,

for e

xam

ple,

indi

vidu

al

fact

ors,

type

of e

xpos

ure,

and

risk

as

soci

ated

with

the

expo

sure

.

• In

tern

atio

nal m

ovem

ent o

f st

rain

s•

Gen

etic

reas

sort

men

ts•

Emer

genc

e of

ose

ltam

ivir

resi

stan

ce h

as b

een

repo

rted

.•

Mos

t rec

ent A

(H5)

and

A

(H7N

9) v

iruse

s ar

e re

sist

-an

t to

adam

anta

ne a

ntiv

iral

drug

s (e

.g.,

aman

tadi

ne a

nd

riman

tadi

ne) a

nd a

re th

eref

ore

not r

ecom

men

ded

for

mon

othe

rapy

.

(Con

tinue

s)

TABLE 1 

(Con

tinue

d)

388  |     EDITORIAL

Dis

ease

Publ

ic h

ealth

situ

atio

nD

iagn

ostic

& tr

eatm

ent

Cont

rol s

trat

egy

Chal

leng

es fo

r con

trol

Cha

gas

dise

asec

• C

haga

s di

seas

e, a

lso

know

n as

Am

eric

an

tryp

anos

omia

sis,

is a

pot

entia

lly li

fe-t

hrea

teni

ng

illne

ss c

ause

d by

the

prot

ozoa

n pa

ra-

site

Try

pano

som

a cr

uzi (

T. c

ruzi)

.•

Abo

ut 6

mill

ion

to 7

mill

ion

peop

le w

orld

wid

e ar

e es

timat

ed to

be

infe

cted

with

Try

pans

osom

a cr

uzi.

• C

haga

s di

seas

e is

foun

d m

ainl

y in

end

emic

are

as

of 2

1 La

tin A

mer

ican

cou

ntrie

s, w

here

it is

m

ostly

vec

tor-

born

e tr

ansm

itted

to h

uman

s by

co

ntac

t with

fece

s or

urin

e of

tria

tom

ine

bugs

• C

haga

s di

seas

e oc

curs

prin

cipa

lly in

the

cont

inen

tal p

art o

f Lat

in A

mer

ica

and

not i

n th

e C

arib

bean

isle

s. In

the

past

dec

ades

, how

ever

, it

has

been

incr

easi

ngly

det

ecte

d in

the

Uni

ted

Stat

es o

f Am

eric

a, C

anad

a, a

nd m

any

Euro

pean

an

d so

me

Wes

tern

Pac

ific

coun

trie

s. T

his

is d

ue

mai

nly

to p

opul

atio

n m

obili

ty b

etw

een

Latin

A

mer

ica

and

the

rest

of t

he w

orld

.

• C

haga

s di

seas

e ca

n be

trea

ted

with

be

nzni

dazo

le a

nd a

lso

nifu

rtim

ox.

• Bo

th m

edic

ines

are

alm

ost 1

00%

ef

fect

ive

in c

urin

g th

e di

seas

e if

give

n so

on a

fter

infe

ctio

n at

the

onse

t of

the

acut

e ph

ase

incl

udin

g th

e ca

ses

of

cong

enita

l tra

nsm

issi

on. T

he e

ffic

acy

of b

oth

dim

inis

hes,

how

ever

, the

lo

nger

a p

erso

n ha

s be

en in

fect

ed.

• Th

e po

tent

ial b

enef

its o

f med

icat

ion

in p

reve

ntin

g or

del

ayin

g th

e de

velo

pmen

t of C

haga

s di

seas

e sh

ould

be

wei

ghed

aga

inst

the

long

du

ratio

n of

trea

tmen

t (up

to 2

mon

ths)

an

d po

ssib

le a

dver

se re

actio

ns

(occ

urrin

g in

up

to 4

0% o

f tre

ated

pa

tient

s).

• Th

e co

st o

f tre

atm

ent f

or C

haga

s di

seas

e re

mai

ns s

ubst

antia

l. In

C

olom

bia

alon

e, th

e an

nual

cos

t of

med

ical

car

e fo

r all

patie

nts

with

the

dise

ase

was

est

imat

ed to

be

abou

t US

267

mill

ion

in 2

008.

Spr

ayin

g in

sect

icid

e to

con

trol

vec

tors

wou

ld

cost

nea

rly U

S 5

mill

ion

annu

ally

—le

ss

than

2%

of t

he m

edic

al c

are

cost

.•

Ther

e is

no

vacc

ine

for C

haga

s di

seas

e.

• Ve

ctor

con

trol

is th

e m

ost e

ffec

tive

met

hod

of p

reve

ntio

n in

Lat

in

Am

eric

a. B

lood

scr

eeni

ng is

ne

cess

ary

to p

reve

nt in

fect

ion

thro

ugh

tran

sfus

ion

and

orga

n tr

ansp

lant

atio

n.•

The

cont

rol t

arge

ts a

re e

limin

atio

n of

the

tran

smis

sion

and

ear

ly

heal

thca

re a

cces

s fo

r the

infe

cted

an

d ill

pop

ultio

n.•

Dep

endi

ng o

n th

e ge

ogra

phic

al

area

, WH

O re

com

men

ds th

e fo

llow

ing

appr

oach

es to

pre

vent

ion

and

cont

rol:

o S

pray

ing

of h

ouse

s an

d su

rrou

ndin

g ar

eas

with

resi

dual

in

sect

icid

eso

Hou

se im

prov

emen

ts a

nd h

ouse

cl

eanl

ines

s to

pre

vent

vec

tor

infe

stat

ion;

o B

edne

ts

• Ps

ycho

-soc

ial c

halle

nges

suc

h as

stig

ma

rela

ted

to p

over

ty

and

emot

iona

l fea

rs o

f bei

ng

judg

ed le

adin

g to

low

repo

rtin

g an

d sc

reen

ing

• In

crea

sing

inse

ctic

ide

resi

stan

ce o

f Tria

tom

ine

vect

ors

and

rapi

d re

colo

nisa

-tio

n of

hou

seho

lds

by v

ecto

rs

afte

r spr

ayin

g•

Dia

gnos

is

(Con

tinue

s)

TABLE 1 

(Con

tinue

d)

     |  389EDITORIAL

Dis

ease

Publ

ic h

ealth

situ

atio

nD

iagn

ostic

& tr

eatm

ent

Cont

rol s

trat

egy

Chal

leng

es fo

r con

trol

Schi

stos

omia

sisd

• Sc

hist

osom

iasi

s is

an

acut

e an

d ch

roni

c pa

rasi

tic

dise

ase

caus

ed b

y bl

ood

fluke

s (tr

emat

ode

wor

ms)

of t

he g

enus

Sch

istos

oma.

• Es

timat

es s

how

that

at l

east

206

.4 m

illio

n pe

ople

re

quire

d pr

even

tive

trea

tmen

t in

2016

.•

Schi

stos

omia

sis

tran

smis

sion

has

bee

n re

port

ed

from

78

coun

trie

s. H

owev

er, p

reve

ntiv

e ch

emot

hera

py fo

r sch

isto

som

iasi

s, w

here

peo

ple

and

com

mun

ities

are

targ

eted

for l

arge

-sca

le

trea

tmen

t, is

onl

y re

quire

d in

52

ende

mic

co

untr

ies

with

mod

erat

e-to

-hig

h tr

ansm

issi

on.

• Sc

hist

osom

iasi

s is

pre

vale

nt in

trop

ical

and

su

btro

pica

l are

as, e

spec

ially

in p

oor c

omm

uniti

es

with

out a

cces

s to

saf

e dr

inki

ng w

ater

and

ad

equa

te s

anita

tion.

It is

est

imat

ed th

at a

t lea

st

91.4

% o

f tho

se re

quiri

ng tr

eatm

ent f

or

schi

stos

omia

sis

live

in A

fric

a.•

Ther

e ar

e 2

maj

or fo

rms

of s

chis

toso

mia

sis—

in-

test

inal

and

uro

geni

tal—

caus

ed b

y 5

mai

n sp

ecie

s of

blo

od fl

uke.

• Sc

hist

osom

iasi

s m

ostly

aff

ects

poo

r and

rura

l co

mm

uniti

es, p

artic

ular

ly a

gric

ultu

ral a

nd fi

shin

g po

pula

tions

. Wom

en d

oing

dom

estic

cho

res

in

infe

sted

wat

er, s

uch

as w

ashi

ng c

loth

es, a

re a

lso

at ri

sk a

nd c

an d

evel

op fe

mal

e ge

nita

l sc

hist

osom

iasi

s.

• Sc

hist

osom

iasi

s is

dia

gnos

ed th

roug

h th

e de

tect

ion

of p

aras

ite e

ggs

in s

tool

or

urin

e sp

ecim

ens.

Ant

ibod

ies

and/

or

antig

ens

dete

cted

in b

lood

or u

rine

sam

ples

are

als

o in

dica

tions

of

infe

ctio

n.•

For u

roge

nita

l sch

isto

som

iasi

s, a

fil

trat

ion

tech

niqu

e us

ing

nylo

n, p

aper

, or

pol

ycar

bona

te fi

lters

is th

e st

anda

rd d

iagn

ostic

tech

niqu

e.

Chi

ldre

n w

ith S

. hae

mat

obiu

m a

lmos

t al

way

s ha

ve m

icro

scop

ic b

lood

in th

eir

urin

e, w

hich

can

be

dete

cted

by

chem

ical

reag

ent s

trip

s.•

The

eggs

of i

ntes

tinal

sch

isto

som

iasi

s ca

n be

det

ecte

d in

feca

l spe

cim

ens

thro

ugh

a te

chni

que

usin

g m

ethy

lene

bl

ue-s

tain

ed c

ello

phan

e so

aked

in

glyc

erin

or g

lass

slid

es, k

now

n as

the

Kat

o-K

atz

tech

niqu

e.

• Th

e co

ntro

l of s

chis

toso

mia

sis

is

base

d on

larg

e-sc

ale

trea

tmen

t of

at-r

isk

popu

latio

n gr

oups

, acc

ess

to

safe

wat

er, i

mpr

oved

san

itatio

n,

hygi

ene

educ

atio

n, a

nd s

nail

cont

rol.

• Th

e W

HO

str

ateg

y fo

r sch

isto

so-

mia

sis

cont

rol f

ocus

es o

n re

duci

ng

dise

ase

thro

ugh

perio

dic,

targ

eted

tr

eatm

ent w

ith p

razi

quan

tel t

hrou

gh

the

larg

e-sc

ale

trea

tmen

t (pr

even

-tiv

e ch

emot

hera

py) o

f aff

ecte

d po

pula

tions

.•

It in

volv

es re

gula

r tre

atm

ent o

f all

at-r

isk

grou

ps. I

n a

few

cou

ntrie

s,

whe

re th

ere

is lo

w tr

ansm

issi

on, t

he

inte

rrup

tion

of th

e tr

ansm

issi

on o

f th

e di

seas

e sh

ould

be

aim

ed fo

r.

• En

viro

nmen

tal d

egra

datio

n•

Dam

s an

d la

rge-

scal

e irr

igat

ion

proj

ect t

hat c

ontr

ibut

e to

sna

il in

term

edia

te h

ost p

rolif

erat

ion

• A

nim

al re

serv

oirs

• Po

tent

ial f

or p

razi

quan

tel

resi

stan

ce

a WH

O (2

016)

.b Bh

att e

t al.

(201

3); B

rady

et a

l. (2

012)

.c Ta

rleto

n, R

eith

inge

r, U

rbin

a, K

itron

, and

Gür

tler (

2007

).d W

orld

Hea

lth O

rgan

izat

ion

& U

NIC

EF (2

004)

.

TABLE 1 

(Con

tinue

d)

390  |     EDITORIAL

producing these stages comes at the cost of producing fewer of the forms required for within- host survival. The underlying rationale is that drug treatment, by design, alters the probability of within- host survival and so should alter the costs and benefits of investing in transmission. The authors use a within- host model of malaria infec-tion to predict optimal patterns of investment in transmission in the face of different drug treatment regimens and determine the extent to which alternative patterns of investment can buffer the fitness loss due to drugs. This work emphasizes that in addition to classical resistance mechanisms, drug treatment generates selection for al-tered parasite life history. It also suggests that understanding how any shifts in life history will alter the efficacy of drugs, as well as any limitations on such shifts, is important for evaluating and predicting the consequences of drug treatment.

While evolutionary principles can help design more sustain-able insecticide and antimicrobial resistance mitigation strategies, evaluating the risk of emergence and transmission of vector- borne diseases also requires knowledge of the genetic and environmental contributions to pathogen transmission traits. In their perspective article, Lefevre et al. (2017) discuss how the associations between malaria parasites transmission traits and their related trade- offs and constraints could have important implications for understanding the evolution of parasite transmission and how so doing could inform disease control. For instance, they argue, frontline vector- borne disease prevention tools such as insecticide- treated bednets and in-door residual spraying rely on reducing mosquito contact rates with human hosts and reducing vector survival. Reduced vector survival has the benefits of decreasing mosquito abundance, the number of bites a mosquito can take over the course of its lifetime, and the probability that mosquitoes survive past the parasite’s development time. These effects likely shape the selective environment for para-sites within the vector. However, whether parasites can respond to interventions by evolving shorter EIPs or other heritable extended phenotypes that lengthen mosquito survival or change vector be-havior merit further investigation.

As in the case of malaria described by Lefevre et al. (2017), life- history trait evolution theory and its attributes can help better un-derstand the adaptive potential of triatomines—the vector of Chagas disease. The review by Flores- Ferrer, Marcou, Waleckx, Dumonteil, and Gourbière (2017) suggests that current knowledge of the deter-minants of high diversity and low virulence of the Trypanosoma cruzi parasite remains too limiting to design evolution- proof strategies, while such attributes may be part of the future of Chagas disease control after the 2020 WHO’s target of regional elimination of intra-domiciliary transmission has been reached. The authors argue that the eco- epidemiological relationships that build- up the selective pressures at work have been assiduously studied over the last cen-tury, so that, combined with concepts and modeling inspired from life- history evolution, a good evolutionary understanding could be rapidly gained. Although more specific information will surely be needed, the authors suggest that an effective research strategy would be to integrate data into the conceptual and theoretical frame-work of evolutionary ecology and life- history evolution to provide

the quantitative backgrounds necessary to understand and possibly anticipate adaptive responses to public health interventions.

Public health interventions targeting helminth diseases often rely on mass drug administration to reduce human morbidity and mortality. Considering the frequency of such interventions and the strength of the selective pressure they impose, the emergence and spread of drug resistance is a concern. In the case of schistosomiasis, although hotspots of reduced efficacy of the drug praziquantel have been reported, resistance is not widespread. However, parasite pop-ulations often exhibit considerable genetic variability in their natural tolerance, or acquired resistance, to drugs which, as Viana, Faust, Haydon, Webster, and Lamberton (2017) emphasize, is related to the fitness costs associated with such resistance compared to suscepti-ble lines. Using Bayesian state- space models (SSMs) fitted to data from an in vivo laboratory system, the authors tested the hypothesis that the spread of resistant Schistosoma mansoni may be limited by life- history costs not present in susceptible counterparts. S. man­soni parasites from a praziquantel- susceptible (S), a praziquantel- resistant (R) or a mixed line of originally resistant and susceptible parasites (RS) were exposed to a range of praziquantel doses. Results showed that parasite adult worm survival and fecundity in the mu-rine host decreased across all lines, including R, with increasing drug pressure. The authors also observed trade- offs between adult sur-vival and fecundity in all untreated lines, and these remained strong in S with praziquantel pressure. In contrast, trade- offs between adult survival and fecundity were lost under praziquantel pressure in R. Additionally the authors showed that life- history traits within the molluscan intermediate host were complex, but trade- offs were demonstrated between parasite establishment and cercarial output. These results have theoretical and applied implications and appli-cations for future schistosomiasis control programs and for other host–parasite treatment programs in general.

Complementing the work by Viana et al., 2017; Borlase, Webster, and Rudge (2017) present the case example of haematobium group Schistosoma spp. hybrids in West Africa, a system involving multiple interacting parasites and multiple definitive hosts, in a region where zoonotic reservoirs of schistosomiasis were not previously consid-ered to be of importance. The authors consider how existing math-ematical model frameworks for schistosome transmission could be expanded and adapted to zoonotic hybrid systems, exploring how such model frameworks can utilize molecular and epidemiological data, as well as the complexities and challenges this presents. The authors also highlight the opportunities and value such mathematical models could bring to this and a similar multihost, multiparasite sys-tems, including informing priorities for data collection, diagnostics and laboratory studies and exploring the impact that hybridizations may have on control measures, as well the impact that evolutionary pressures including control measures may have on driving the emer-gence and spread of parasite hybrids.

Evolutionary- based mathematical modeling is also increasingly used to enhance both understanding and design of integrated inter-vention in the context of microparasites such as Dengue. Lourenço et al. (2017) review and analyze the biological and epidemiological

     |  391EDITORIAL

background of dengue, together with the major achievements of computational approaches including highlighting critical knowl-edge gaps and research underachievements that call for an urgent renewed focus. The authors argue that possible advancements based on new processing strategies, including real- time computa-tional analysis of genetic data, phylodynamic modeling frameworks, within- host model frameworks and GPU accelerated computing al-ready implemented for other pathogens, are already at reach of the Dengue research community. These new approaches are expected to make a significant contribution to our understanding of the evo-lutionary ecology and immunology of the dengue virus and support the design of novel integrated control strategies adaptable to other microparasite systems such as avian influenza affecting domestic animals and humans alike.

Influenza pandemics represent a significant threat to global public health. Four major pandemics have been recorded since the 1900s, occurring in 1918, 1957, 1968, and 2009 when influenza A vi-ruses with genes from animal sources adapted to the human popula-tion, a process known as antigenic shift. The H1N1/2009 pandemic virus emerged from swine that contained gene segments ultimately derived from previously circulating human and avian viruses, high-lighting a key role of segmental reassortment of genes from multiple hosts for host adaption and pandemic emergence. In this context, Joseph, Vijaykrishna, Smith, and Su (2017) used a relaxed molec-ular clock model to test whether the European avian- like swine (EA- swine) influenza virus originated through the introduction of a single avian ancestor as an entire genome, followed by an analysis of host- specific selection pressures among different gene segments. The results indicate independent introduction of gene segments via transmission of avian viruses into swine followed by reassort-ment events that occurred at least 1–4 years prior to the EA- swine outbreak. All EA- swine gene segments exhibited greater selection pressure than avian viruses, reflecting both adaptive pressures and relaxed selective constraints that are associated with host switching. Key amino acid mutations in the viral surface proteins (H1 and N1) that play a role in adaptation to new hosts were also observed sug-gesting adaptive changes in viral genomes following the transmis-sion of avian influenza viruses to swine and the early establishment of the EA- swine lineage.

Complementing the work by Joseph et al., 2017; Grear, Hall, Dusek, and Ip (2017) investigated mechanisms of intercontinental highly pathogenic avian influenza virus (HPAIV) spread through wild bird reservoirs possibly related to the North America outbreak in 2014. This introduction resulted in several reassortment events with North American (NA) lineage low- pathogenic avian influenza viruses and the reassortant EA/NA H5N2 that went on to cause one of the largest HPAIV poultry outbreaks in North America. In their research article, the authors used a time- rooted phylodynamic model that explicitly incorporated viral population dynamics with evolutionary dynamics to estimate the basic reproductive number (R0) and viral migration among host types in domestic and wild birds, as well as between the EA H5N8 and EA/NA H5N2 in wild birds. While the authors did not find evidence to support the hypothesis

that transmission of novel HPAIVs in wild birds was restricted by mechanisms associated with highly pathogenic phenotypes or that the HPAIV poultry outbreak was self- sustaining and required viral input from wild birds, the model estimates of the transmission pa-rameters suggested that the HPAIV outbreak met or exceeded the thresholdforpersistenceinwildbirds(R0>1)andpoultry(R0≈1).Overall, the results of this work suggest that this novel HPAIV and reassortments did not encounter any transmission barriers sufficient to prevent persistence when introduced to wild or domestic birds and highlight the relevance of phylodynamic methods to test hy-potheses about geographical spread of AIVs in wild birds, multiyear evolutionary processes of AIVs in reservoir hosts and relative fitness of highly pathogenic versus low- pathogenic AIVs in wild birds for more integrated surveillance systems.

3  | CLOSING REMARKS: E VOLUTION, ADAPTIVE MANAGEMENT, AND SUSTAINABLE HE ALTH DE VELOPMENT

While disease control and prevention have achieved great successes, the paradigm within which it has been developed, including our un-derstanding of host–parasite relationships, infection, and disease, as well as best management practices, arguably is not enough. A major shortcoming is that the solutions it provides, often grounded in the curative domain, are not lasting. Evolutionary thinking applied to medical and public health problems promises to substitute the short- sighted use of drugs with sustainable solutions: If we cannot eradicate infections by frontal assault, we may be able to keep them at bay durably provided we can understand the fundamental nature of host–parasite relationships.

The evolutionary perspective asks ultimate questions, which are about why mechanisms or epidemiological phenotypes are the way they are (i.e., how has this mechanism given a selective advantage? what is the evolutionary history of this mechanism?). Most medical research and perspectives focus on proximal questions, questions about the mechanisms themselves (i.e., how does the mechanism work, what is the ontogeny of the mechanisms?). The distinction be-tween proximate (mechanistic) and ultimate (evolutionary) explana-tions was emphasized and formalized several decades ago but remain unfamiliar to the medical sciences and public health domain despite its epistemological importance (Nesse, 2013). Both types of expla-nations are necessary, neither substitutes for the other, and they in-form each other (Nesse, 2013; Nesse & Stearns, 2008). Incorporating evolutionary thinking in infectious disease research helps improving our understanding of diseases transmission dynamics, infection pat-terns, and disease manifestation trends by superimposing a context- dependent, systems dynamics prism that appreciates that organisms and their interactions are in constant flux (Levin, 1998). Accordingly, evolutionary biology can help identify new relevant questions such as the ones addressed in this special issue, and doing so, can help inform more integrated disease control interventions as well as more adaptive health management strategies.

392  |     EDITORIAL

Adaptive health management, standing on strong evolutionary foundations, has the potential to address two fundamental errors underpinning most current public health interventions targeting in-fectious diseases. The first error is often the implicit assumption that pathogens or parasite responses to human intervention and/or that human–parasite/pathogens interactions are linear, predictable, and controllable. The second error is the assumption that pathogens and parasites can be treated independently of the social- ecological sys-tem within which they evolve (Horwitz & Wilcox, 2005). By explicitly avoiding these errors, evolutionary- based adaptive health manage-ment could help strengthen the representation of the operational concept of resilience in public health and restore the health systems capacity to buffer infectious and noninfectious challenges, learn, and develop—as a framework for understanding how to sustain and enhance adaptive capacity in a complex world of rapid transforma-tions (Folke et al., 2002).

ACKNOWLEDG EMENTS

The authors wish to thank Serge Morand and Bruce A. Wilcox for their comments and suggestions on earlier drafts.

Pierre Echaubard1,2

James W. Rudge3,4

Thierry Lefevre5,6

1Global Health Asia Institute, Faculty of Public Health Mahidol University, Bangkok, Thailand

2Department of Biology, Laurentian University, Sudbury, ON, Canada3Department of Global Health and Development, London School of

Hygiene and Tropical Medicine, London, UK4Faculty of Public Health, Mahidol University, Bangkok, Thailand

5Institut de Recherche en Sciences de la Santé (IRSS), Bobo Dioulasso, Burkina Faso

6MIVEGEC, IRD, CNRS, University. Montpellier, Montpellier, France

R E FE R E N C E S

Allegranzi, B., Kilpatrick, C., Storr, J., Kelley, E., Park, B. J., & Donaldson, L. (2017). Global infection prevention and control priorities 2018–22: A call for action. The Lancet Global Health, 5, e1178–e1180. https://doi.org/10.1016/S2214-109X(17)30427-8

Altizer, S., Ostfeld, R. S., Johnson, P. T. J., Kutz, S., & Harvell, C. D. (2013). Climate change and infectious diseases: from evidence to a predic-tive framework. Science, 341, 514–519. https://doi.org/10.1126/science.1239401

Anderson, R. M., & May, R. M. (1981). The population dynamics of micro-parasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 291, 451–524. https://doi.org/10.1098/rstb.1981.0005

Bhatt, S., Gething, P. W., Brady, O. J., Messina, J. P., Farlow, A. W., Moyes, C. L., … Hay, S. I. (2013). The global distribution and burden of den-gue. Nature, 496, 504–507.

Birget, P. L. G., Greischar, M. A., Reece, S. E., & Mideo, N. (2017). Altered life history strategies protect malaria parasites against drugs. Evolutionary Application, 11, 442–455. https://doi.org/10.1111/eva.12516

Borlase, A., Webster, J. P., & Rudge, J. W. (2017). Opportunities and chal-lenges for modelling epidemiological and evolutionary dynamics in a

multihost, multiparasite system: Zoonotic hybrid schistosomiasis in West Africa. Evolutionary Application, 11, 501–515. https://doi.org/ 10.1111/eva.12529

Brady, O. J., Gething, P. W., Bhatt, S., Messina, J. P., Brownstein, J. S., Hoen, A. G., … Hay, S. I. (2012). Refining the global spatial limits of dengue virus transmission by evidence- based consensus. PLoS Neglected Tropical Diseases, 6, e1760.

Carroll, S. P., Jørgensen, P. S., Kinnison, M. T., Bergstrom, C. T., Denison, R. F., Gluckman, P., … Tabashnik, B. E. (2014). Applying evolutionary biology to address global challenges. Science, 346, 1245993. https://doi.org/10.1126/science.1245993

Echaubard, P., Sripa, B., Mallory, F. F., & Wilcox, B. A. (2016). The role of evolutionary biology in research and control of liver flukes in Southeast Asia. Infection, Genetics and Evolution, 43, 381–397. https://doi.org/10.1016/j.meegid.2016.05.019

Flores-Ferrer, A., Marcou, O., Waleckx, E., Dumonteil, E., & Gourbière, S. (2017). Evolutionary ecology of Chagas disease; what do we know and what do we need?. Evolutionary Application, 11, 470–487. https://doi.org/10.1111/eva.12582

Folke, C., Carpenter, S., Elmqvist, T., Gunderson, L., Holling, C. S., & Walker, B. (2002). Resilience and sustainable development: Building adaptive capacity in a world of transformations. AMBIO Journal of the Human Environment, 31, 437–440. https://doi.org/10.1579/0044-7447-31.5.437

Glunt, K. D., Coetzee, M., Huijben, S., Koffi, A. A., Lynch, P. A., N’Guessan, R., … Thomas, M. B. (2017). Empirical and theoret-ical investigation into the potential impacts of insecticide re-sistance on the effectiveness of insecticide- treated bed nets. Evolutionary Application, 11, 431–441. https://doi.org/10.1111/ eva.12574

Grear, D. A., Hall, J. S., Dusek, R. J., & Ip, H. S. (2017). Inferring epide-miologic dynamics from viral evolution: 2014–2015 Eurasian/North American highly pathogenic avian influenza viruses exceed transmis-sion threshold, R0 = 1, in wild birds and poultry in North America. Evolutionary Application, 11, 547–557. https://doi.org/10.1111/eva.12 576

Horwitz, P., & Wilcox, B. A. (2005). Parasites, ecosystems and sustain-ability: An ecological and complex systems perspective. International Journal for Parasitology, 35, 725–732. https://doi.org/10.1016/j.ijpara.2005.03.002

Huijben, S., & Paaijmans, K. P. (2017). Putting evolution in elimination: Winning our ongoing battle with evolving malaria mosquitoes and parasites. Evolutionary Application, 11, 415–430. https://doi.org/ 10.1111/eva.12530

Joseph, U., Vijaykrishna, D., Smith, G. J. D., & Su, Y. C. F. (2017). Adaptive evolution during the establishment of European avian- like H1N1 influenza A virus in swine. Evolutionary Applications, 11, 534–546. https://doi.org/10.1111/eva.12536n/a–n/a.

Kosoy, M., & Kosoy, R. (2017). Complexity and biosemiotics in evolution-ary ecology of zoonotic infectious agents. Evolutionary Applications, 11, 394–403. https://doi.org/10.1111/eva.12503

Lafferty, K. D. (2009). The ecology of climate change and infec-tious diseases. Ecology, 90, 888–900. https://doi.org/10.1890/ 08-0079.1

Lederberg, J., Shope, R. E., & Oaks, S. C. (1992). Emerging Infections: Microbial Threats to Health in the United States. Washington: National Academies Press.

Lefevre, T., Ohm, J., Dabiré, K. R., Cohuet, A., Choisy, M., Thomas, M. B., & Cator, L. (2017). Transmission traits of malaria parasites within the mosquito: Genetic variation, phenotypic plasticity, and conse-quences for control. Evolutionary Application, 11, 456–469. https://doi.org/10.1111/eva.12571

Levin, S. A. (1998). Ecosystems and the biosphere as Complex Adaptive Systems. Ecosystems, 1, 431–436. https://doi.org/10.1007/s100219900037

     |  393EDITORIAL

Lourenço, J., Tennant, W., Faria, N. R., Walker, A., Gupta, S., & Recker, M. (2017). Challenges in dengue research: A computational perspective. Evolutionary Application, 11, 516–533. https://doi.org/10.1111/eva. 12554

McMichael, A. J., & Wilcox, B. A. (2009). Climate Change, Human Health, and Integrative Research: A Transformative Imperative. EcoHealth, 6, 163–164. https://doi.org/10.1007/s10393-009-0262-9

McNeill, W. H. (1976). Plagues and peoples. New York: Anchor Press.Myers, S. S., Gaffikin, L., Golden, C. D., Ostfeld, R. S., Redford, H.,

Ricketts, K. H. T., … Osofsky, S. A. (2013). Human health impacts of ecosystem alteration. Proceedings of the National Academy of Sciences of the United States of America, 110, 18753–18760. https://doi.org/10.1073/pnas.1218656110

Myers, S. S., & Patz, J. A. (2009). Emerging Threats to Human Health from Global Environmental Change. Annual Review of Environment and Resources, 34, 223–252. https://doi.org/10.1146/annurev.environ.033108.102650

Nesse, R. (2008). What evolutionary biology offers public health. Bulletin of the World Health Organization, 86, 83. https://doi.org/10.2471/BLT.00.00000

Nesse, R. M. (2013). Tinbergen’s four questions, organized: A response to Bateson and Laland. Trends in Ecology & Evolution, 28, 681–682. https://doi.org/10.1016/j.tree.2013.10.008

Nesse, R. M., & Stearns, S. C. (2008). The great opportunity: Evolutionary applications to medicine and public health: Evolutionary applications to medicine and public health. Evolutionary Applications, 1, 28–48. https://doi.org/10.1111/j.1752-4571.2007.00006.x

Packard, R. M. (2007). The making of a tropical disease: A short history of malaria. Baltimore, MD, USA: JHU Press.

Restif, O. (2009). Evolutionary epidemiology 20 years on: Challenges and prospects. Infection, Genetics and Evolution, 9, 108–123. https://doi.org/10.1016/j.meegid.2008.09.007

Stearns, S. C., & Koella, J. C. (2008). Evolution in Health and Disease, 2nd edn.Oxford ,NewYork:OxfordUniversityPress.

Sternberg, E. D., & Thomas, M. B. (2017). Insights from agriculture for the management of insecticide resistance in disease vectors. Evolutionary Application, 11, 404–414. https://doi.org/10.1111/eva.12501

Tarleton, R. L., Reithinger, R., Urbina, J. A., Kitron, U., & Gürtler, R. E. (2007). The challenges of Chagas disease— grim outlook or glimmer of hope? PLoS Medicine, 4, e332.

Valen, V. (1973). A new evolutionary law. Evolutionary Theory, 1, 1–30.Viana, M., Faust, C. L., Haydon, D. T., Webster, J. P., & Lamberton, P. H.

L. (2017). The effects of subcurative praziquantel treatment on life- history traits and trade- offs in drug- resistant Schistosoma mansoni. Evol­utionary Application, 11, 488–500. https://doi.org/10.1111/eva.12558

Whitmee, S., Haines, A., Beyrer, C., Boltz, F., Capon, A. G., de Dias, B. F., … Yach, D. (2015). Safeguarding human health in the Anthropocene epoch: Report of The Rockefeller Foundation- Lancet Commission on planetary health. The Lancet, 386, 1973–2028. https://doi.org/10.1016/S0140-6736(15)60901-1

WHO. (2016). World malaria report: 2016.Wilcox, B. A., & Echaubard, P. (2016). Balancing biomedical and ecologi-

cal perspectives in research framing of liver fluke and cholangiocarci-noma in NE Thailand. Parasitology International, 66, 372–377. https://doi.org/10.1016/j.parint.2016.10.002

World Health Organization & UNICEF. (2004). Prevention and control of schistosomiasis and soil­transmitted helminthiasis. Geneva: World Health Organization.