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Evolution
of
the
indoor
biome
NESCent
Working
Group
on
the
Evolutionary
Biology
of
the
Built
Environment,
Laura
J.
Martin
1
,
Rachel
I.
Adams
2
,
Ashley
Bateman
3
,
Holly
M.
Bik
4
,
John
Hawks
5
,
Sarah
M.
Hird
4
,
David
Hughes
6
,
Steven
W.
Kembel
7
,
Kerry
Kinney
8
,
Sergios-Orestis
Kolokotronis
9
,
Gabriel
Levy
10
,
Craig
McClain
11
,
James
F.
Meadow
12
,
Raul
F.
Medina
13
,
Gwynne
Mhuireach
14
,
Corrie
S.
Moreau
15
,
Jason
Munshi-South
9,16
,
Lauren
M.
Nichols
17
,
Clare
Palmer
18
,
Laura
Popova
19
,
Coby
Schal
17,20
,
Martin
Ta¨
ubel
21
,
Michelle
Trautwein
22
,
Juan
A.
Ugalde
23
,
and
Robert
R.
Dunn
17,24
1
Department
of
Natural
Resources,
Cornell
University,
Ithaca,
NY
14853,
USA
2
Department
of
Plant
and
Microbial
Biology,
University
of
California
Berkeley,
Berkeley,
CA
94720,
USA
3
Department
of
Biology,
Institute
of
Ecology
and
Evolution,
University
of
Oregon,
Eugene,
OR
97403,
USA
4
UC
Davis
Genome
Center,
University
of
California
Davis,
Davis,
CA
95616,
USA
5
Department
of
Anthropology,
University
of
Wisconsin–Madison,
Madison,
WI
53706,
USA
6
Department
of
Entomology,
Penn
State
University,
University
Park,
PA
16802,
USA
7
De´
partement
des
Sciences
Biologiques,
Universite´
du
Que´
bec
a`
Montre´
al,
Montre´
al,
QC
H3C
3P8,
Canada
8
Department
of
Civil,
Architectural,
and
Environmental
Engineering,
University
of
Texas
at
Austin,
Austin,
TX
78712,
USA
9
Department
of
Biological
Sciences,
Fordham
University,
Bronx,
NY
10458,
USA
10
Department
of
Philosophy
and
Religious
Studies,
Norwegian
University
of
Science
and
Technology,
NO-7491
Trondheim,
Norway
11
National
Evolutionary
Synthesis
Center,
Durham,
NC,
27705,
USA
12
Biology
and
the
Built
Environment
Center,
Institute
of
Ecology
and
Evolution,
University
of
Oregon,
Eugene,
OR
97403,
USA
13
Department
of
Entomology,
Texas
A&M
University,
College
Station,
TX
77843,
USA
14
Department
of
Architecture,
University
of
Oregon,
Eugene,
OR
97403,
USA
15
Department
of
Science
and
Education,
Field
Museum
of
Natural
History,
Chicago,
IL
60605,
USA
16
Louis
Calder
Center–Biological
Field
Station,
Fordham
University,
Armonk,
NY
10504,
USA
17
Department
of
Biological
Sciences,
North
Carolina
State
University,
Raleigh,
NC
27695,
USA
18
Department
of
Philosophy,
Texas
A&M
University,
College
Station,
TX
77843,
USA
19
Barrett
Honors
College,
Arizona
State
University,
Tempe,
AZ
85287,
USA
20
Department
of
Entomology,
North
Carolina
State
University,
Raleigh,
NC
27695,
USA
21
National
Institute
for
Health
and
Welfare,
Department
of
Health
Protection,
70210
Kuopio,
Finland
22
California
Academy
of
Sciences,
San
Francisco,
CA
94118,
USA
23
Centro
de
Geno´
mica
y
Bioinforma´
tica,
Facultad
de
Ciencias,
Universidad
Mayor,
Santiago,
Chile
24
Center
for
Macroecology,
Evolution
and
Climate,
Natural
History
Museum
of
Denmark,
University
of
Copenhagen,
Universitetsparken
15,
DK-2100
Copenhagen
Ø,
Denmark
Few
biologists
have
studied
the
evolutionary
processes
at
work
in
indoor
environments.
Yet
indoor
environ-
ments
comprise
approximately
0.5%
of
ice-free
land
area
–
an
area
as
large
as
the
subtropical
coniferous
forest
biome.
Here
we
review
the
emerging
subfield
of
‘indoor
biome’
studies.
After
defining
the
indoor
biome
and
tracing
its
deep
history,
we
discuss
some
of
its
evolu-
tionary
dimensions.
We
restrict
our
examples
to
the
species
found
in
human
houses
–
a
subset
of
the
envir-
onments
constituting
the
indoor
biome
–
and
offer
pre-
liminary
hypotheses
to
advance
the
study
of
indoor
evolution.
Studies
of
the
indoor
biome
are
situated
at
the
intersection
of
evolutionary
ecology,
anthropology,
architecture,
and
human
ecology
and
are
well
suited
for
citizen
science
projects,
public
outreach,
and
large-scale
international
collaborations.
Review
0169-5347/
ß
2015
Elsevier
Ltd.
All
rights
reserved.
http://dx.doi.org/10.1016/j.tree.2015.02.001
Corresponding
author:
Martin,
L.J.
(LJM222@cornell.edu).
Keywords:
urban
ecology;
anthrome;
microbiome;
phylogeography;
built
environ-
ment.
Glossary
Biome:
Robert
H.
Whittaker
first
developed
the
biome
concept
to
classify
the
different
realms
of
life
found
on
Earth.
His
classification
scheme
was
based
on
two
abiotic
factors
–
precipitation
and
temperature
–
that
he
viewed
to
have
the
largest
impact
on
the
distribution
of
species
and
their
traits
and
function.
Subsequent
biome
classification
systems
have
considered
the
biomes
found
in
the
absence
of
human
agency
and
so
exclude
much
of
Earth’s
terrestrial
area.
One
exception
is
the
anthrome
framework,
which
includes
biomes
engendered
by
humans
[2].
However,
even
anthromes
deal
only
with
outdoor
environments.
Indoor
biome:
the
ecological
realm
comprising
species
that
reside
and
can
(although
do
not
necessarily
always)
reproduce
in
enclosed
and
semi-enclosed
built
structures.
Indoor
environment:
the
space
enclosed
by
walled
and
roofed
structures
built
by
organisms
to
shelter
themselves,
their
symbiotic
partners,
or
stored
goods.
For
the
purposes
of
this
review
we
focus
on
the
indoor
environments
created
by
humans.
TREE-1909;
No.
of
Pages
10
Trends
in
Ecology
&
Evolution
xx
(2015)
1–10
1
The
indoor
biome
Evolution
occurs
everywhere,
even
in
the
most
densely
settled
places.
Indeed,
Darwin
based
his
arguments
for
natural
selection
on
domesticated
plants
and
animals.
Recent
work
in
the
fields
of
evolutionary
biology,
ecology,
anthropology,
and
building
sciences
turns
our
attention
back
to
species
that
coexist
with
humans.
Much
of
this
work
is
conducted
in
outdoor
spaces
[1],
but
a
growing
body
of
work
addresses
evolution
in
the
indoor
biome
(see
Glossary).
The
indoor
biome
is
expansive.
Estimates
of
the
extent
of
residential
and
commercial
buildings
range
between
1.3%
[3]
and
6%
[4]
of
global
ice-free
land
area,
an
area
as
extensive
as
other
small
biomes
such
as
flooded
grass-
lands
and
tropical
coniferous
forests
(Figure
1).
In
addi-
tion,
whereas
the
area
of
flooded
grasslands
and
tropical
coniferous
forests
is
shrinking,
that
of
the
indoor
biome
is
rapidly
growing
[5],
as
is
our
ability
to
study
indoor
species
thanks
to
citizen
science,
new
approaches
in
genetics,
and
calls
to
integrate
humans
into
the
ecosystem
concept
[6–
10]
(Figure
2).
Here
we
review
the
rich
but
fragmented
literature
on
evolution
in
the
indoor
biome.
For
the
purpose
of
brevity
we
restrict
our
examples
to
one
type
of
built
structure
–
human
dwellings
–
although
the
indoor
biome
encom-
passes
all
built
structures
(Box
1,
Table
1).
A
brief
history
of
the
indoor
biome
The
nests
of
birds,
termites,
and
ants
are
part
of
the
extended
phenotype
of
those
organisms,
as
are
those
of
our
closest
living
relatives,
the
great
apes,
which
construct
nests
across
a
broad
range
of
environments.
Our
common
ancestors
would
probably
also
have
used
regular
sleeping
places
with
constructed
nests
[11].
Primate
nests,
like
modern
built
environments,
are
places
where
bodies
ha-
bitually
rest
and
thus
suitable
places
for
organisms
that
depend
on
access
to
bodies
to
reproduce.
How
the
nest
is
constructed
thus
influences
the
species
to
which
the
build-
er
is
exposed.
Chimpanzees
choose
nesting
sites
and
con-
struction
methods
that
reduce
arthropod
parasites
[12],
suggesting
that,
in
the
past,
parasites
imposed
selection
on
primate
nesting
behavior.
Meanwhile,
the
evolutionary
history
of
many
human
ectoparasites
and
commensals,
including
body
lice,
Demodex
mites,
and
bacterial
sym-
bionts,
predates
the
origin
of
apes
(and
hence
almost
Deserts & xeric shrublands
0% 5% 10%
15%
20%
Tropical & subtropical coniferous forests
Tropical & subtropical dry broadleaf forests
Mediterranean forests, woodlands & shrub
Temperate coniferous forests
Montane grasslands & shrublands
Tundra
Biome
Proporon of earth’s terrestrial area
Temperate grasslands, savannas & shrublands
Temperate broadleaf & mixed forests
Boreal forests
Tropical & subtropical moist broadleaf forests
Tropical & subtropical grasslands, savannas & shrublands
Flooded grasslands & savannas
Indoor
TRENDS in Ecology & Evolution
Figure
1.
The
relative
areas
of
13
outdoor
biomes
and
the
indoor
biome.
Box
1.
Built
structures
other
than
houses
In
this
review
we
have
focused
on
houses,
but
many
other
buildings
constitute
the
indoor
biome.
These
include
places
of
worship,
food
storage
areas,
commercial
spaces,
factories,
offices,
and
restaurants
[2].
In
addition,
houses
are
not
closed
systems;
many
materials
flow
into
and
out
of
them.
For
instance,
a
diverse
range
of
microorgan-
isms
is
present
in
municipal
water
supply
and
piping
biofilms
that
enter
homes
via
water
lines,
so
mapping
the
inflow
and
outflow
of
organisms
into
the
indoor
biome
may
be
a
nontrivial
challenge.
Furthermore,
it
should
be
recognized
that
studies
of
indoor
biomes
cannot
avoid
intersecting
questions
of
politics
and
justice.
It
should
not
be
taken
for
granted
that
humans
live
in
houses.
An
estimated
100
million
people
were
homeless
in
2005
[United
Nations
Commission
on
Human
Rights
(2005)
Press
briefing
by
special
rapporteur
on
right
to
adequate
housing
(http://www.un.org/News/
briefings/docs/2005/kotharibrf050511.doc.htm)],
while
human
struc-
tures
are
sometimes
abandoned
and
may
persist
as
indoor
environments
without
a
human
presence.
It
should
also
not
escape
notice
that
structures
also
vary
widely
by
place.
For
example,
approximately
50%
of
Canadians
live
in
houses
with
seven
or
more
rooms,
while
only
9%
of
people
from
Burkina-Faso
do
so
[United
Nations
Department
of
Economic
and
Social
Affairs
(2012)
Table
21.
In
Compendium
of
Housing
Statistics
(http://unstats.un.
org/unsd/demographic/sconcerns/)].
It
is
therefore
important,
as
with
all
biological
studies,
to
be
context
specific
[75].
Review Trends
in
Ecology
&
Evolution
xxx
xxxx,
Vol.
xxx,
No.
x
TREE-1909;
No.
of
Pages
10
2
certainly
the
first
ape
nest)
[13,14].
Other
species
that
inhabit
contemporary
houses,
including
dust
mites,
some
beetles,
and
webbing
clothes
moths
–
many
of
which
are
found
in
contemporary
nests
of
mammals
or
birds
–
may
have
first
become
associated
with
our
ancestors
subse-
quent
to
their
construction
of
nests
(e.g.,
[15]).
With
time,
some
primates
began
to
use
caves
as
sleeping
sites
[16].
Caves
share
more
similarities
with
human
houses
than
do
nests,
as
they
are
less
variable
in
terms
of
climate
than
the
outdoor
environment
and
represent
places
where
ectoparasites
and
other
associates
of
homi-
nids
could
reliably
find
bodies
and
food.
Bed
bugs
(Cimex
lectularius),
for
example,
are
speculated
to
have
moved
from
bats
onto
humans
during
a
time
when
humans
occu-
pied
cave
environments
[17].
The
first
human
houses
emerged
approximately
20
000
years
ago
[18].
Before
the
origin
of
agriculture,
houses
were
places
where
humans
slept,
mated,
and
ate
and
where
refuse
accumulated.
After
the
origin
of
agricul-
ture,
trajectories
differed
among
regions.
In
some
regions,
Manhaan
Land area
Indoor biome
Esmated residenal
living space
Esmated commercial
indoor space Lo
apartments
Tenement
building
Street
cleaning
Sewage systems by state law
Manhaan populaon (in millions)
AC
units
affordable
Colonial house
Pre-dutch
1609
1860
1910
1980
2015
0.5
1
2
2.5
1.5
Lenape
wigwam
Evoluon of the indoor biome
172 km2
59 km2
TRENDS in Ecology & Evolution
Figure
2.
The
trajectory
of
the
indoor
biome
in
one
exemplar
area,
the
island
of
Manhattan.
The
indoor
biome
in
Manhattan
is
now
nearly
three
times
as
large,
in
terms
of
its
floor
space,
as
is
the
geographical
area
of
the
island
itself.
Historically
Manhattan
was
an
outlier,
but
as
urban
populations
grow
much,
perhaps
most,
of
the
world’s
population
will
soon
be
living
in
areas
with
more
floor
space
than
dirt.
Included
on
this
figure
are
key
changes
in
the
development
of
the
indoor
biome,
as
manifested
in
Manhattan.
These
changes
are
neither
universal
in
the
indoor
biome
nor
necessarily
unidirectional
(the
population,
for
instance,
in
Manhattan
declined
in
the
early
1900s),
yet,
as
emphasized
in
the
text,
when
they
occur
have
the
potential
to
have
large
but
poorly
studied
consequences
on
evolution
indoors.
Review Trends
in
Ecology
&
Evolution
xxx
xxxx,
Vol.
xxx,
No.
x
TREE-1909;
No.
of
Pages
10
3
people
shifted
from
sedentary
to
nomadic
lifestyles
or
from
high-
to
low-density
settlements
[19].
Eventually,
however,
in
virtually
all
inhabited
regions,
urbanism
arose,
and
with
it
higher-density
living.
Initially,
humans
designed
houses
to
take
into
account
the
climatic
conditions
of
specific
places
[20].
Increasingly,
however,
technological
and
political
developments
have
changed
the
relationship
between
house
design
and
the
outdoor
environment
in
affluent
countries,
cities,
and
neighborhoods.
As
a
result,
apartments
in
Finland
and
Singapore
may
now
be
very
similar,
independent
of
their
very
different
settings.
These
developments
include:
the
adoption
of
indoor
plumbing
in
the
late
1800s;
electrifica-
tion
and
air
conditioning
of
residences
in
the
1920s;
elec-
trification
of
farms
in
the
USA
in
the
1930s;
and
new
standards
for
ventilation
and
insulation
following
energy
crises
in
the
1970s
(Figure
3).
Nevertheless,
modern
analogs
of
many
historic
indoor
biomes
still
exist
(and
in
some
regions
predominate).
As
a
result,
the
global
diversity
of
conditions
within
the
indoor
biome
is
likely
to
be
as
great
as
it
has
ever
been.
For
the
purposes
of
this
review
we
attempt
to
consider
the
evolu-
tion
of
the
indoor
biome
in
light
of
the
great
modern
and
historical
variation
in
homes,
but
note
that
most
studies
of
indoor
evolution
are
done
in
relatively
new,
relatively
large
houses
in
North
America
and
Europe.
Species
of
the
indoor
biome
Thousands
of
species
–
perhaps
hundreds
of
thousands
–
live
in
the
indoor
biome,
many
of
them
preferentially
or
even
obligately.
A
study
of
just
nine
habitats
(e.g.,
kitchen,
bedroom)
in
each
of
40
houses
in
North
Carolina,
USA,
documented
more
than
8000
bacterial
and
archaeal
taxa
through
molecular
detection
[21],
while
a
study
of
50
hous-
es
in
North
Carolina,
USA
noted
more
than
750
arthropod
species,
with
often
more
than
100
species
of
arthropod
per
house
(M.
Trautwein,
unpublished).
Similarly,
a
molecu-
lar-based
survey
of
11
houses
in
California,
USA,
found
hundreds
of
fungal
taxa
[22],
and
dozens
of
fungal
species
have
been
cultured
from
showers
and
drains
alone
[23].
Strong
biogeographical
patterns
have
been
identified
for
bacteria
in
residential
kitchens
[24]
and
inhabitants
in
a
new
home
can
drastically
influence
the
home
microbiome
within
a
matter
of
days
[25].
Molecular
surveys
have
also
identified
a
suite
of
microscopic
species
in
treated
drinking
water
[26].
What
we
know
today
about
the
natural
history
of
the
indoor
biome
derives
from
the
relatively
small
proportion
of
indoor
species
that
have
been
studied
in
any
detail
(Box
2),
a
group
biased
toward
species
that
humans
at-
tempt
to
exclude
from
the
indoor
biome.
It
is
from
these
species
that
we
begin
to
derive
a
more
general
story
of
the
evolution
of
the
indoor
biome.
Selection
pressures
in
the
indoor
biome
Perhaps
the
only
intentional
actions
humans
take
to
alter
evolution
in
the
indoor
biome
are
attempts
to
extinguish
disliked
species,
whether
through
cleaning
practices,
the
use
of
biocides,
or
attempts
to
prevent
species
from
colo-
nizing
in
the
first
place.
The
organisms
subject
to
biocide
differ
across
regions
and
cultures
as
a
function
of
which
animals
are
feared
or
disliked.
What
does
not
seem
to
vary
is
a
dislike
or
fear
of
at
least
a
few
organisms
that
live
in
the
home
[27].
In
many
instances,
the
use
of
biocides
has
led
to
the
local
extinction
of
susceptible
genotypes
and
the
in-
crease
of
less
susceptible
ones.
Many
insect
species
have
evolved
resistance
to
insecticides
[28],
for
example,
and
multiple
rodent
species
have
evolved
resistance
to
roden-
ticides
[29].
Such
species
have
evolved
both
the
ability
to
tolerate
biocides
and
the
behavior
of
avoiding
biocide
ingestion.
German
cockroaches
(Blattella
germanica)
have
evolved
an
adaptive
behavioral
aversion
to
glucose
in
poison
baits
[30].
Many
bacteria
have
evolved
resistance
in
response
to
the
use
of
antibiotics
in
living
facilities
and
hospitals
(e.g.,
[31])
and
in
the
production
of
domestic
food
animals
(e.g.,
[32]).
The
antimicrobial
triclosan
has
been
suggested
to
disfavor
some
microbial
lineages
in
sink
drains
while,
like
most
biocides,
favoring
others
[33].
Other
selective
pressures
in
houses
remain
unstudied.
These
selective
pressures
result
from
choices
humans
make
as
a
result
of
their
preference
for
living
conditions,
design,
or
indoor
climate.
Globally,
the
distribution
of
indoor
climatic
conditions
and
resources
varies
widely
because
of
both
variation
in
outdoor
climate
and
differ-
ences
in
the
extent
to
which
different
types
of
home
buffer
that
climate.
Many
of
the
Western
houses
that
have
been
the
focus
of
studies
on
indoor
taxa
are
relatively
decoupled
in
terms
of
their
climate
from
outdoor
conditions
(e.g.,
Figure
3A),
such
that
many
species
of
the
indoor
biome
are
likely
to
have
experienced
recent
selection
favoring
lineages
able
to
tolerate
dry,
warm
habitats
(Figure
3A,B)
relative
to
those
that
prefer
moist,
cool
habitats
[34].
While
seasonal
patterns
in
temperature
and
humidity
are
buff-
ered
by
houses,
the
extremes
at
smaller
scales
(centimeters
and
minutes
rather
than
kilometers
and
days)
can
be
as
great
as
those
outdoors.
Even
within
a
single
house,
tem-
perature,
humidity,
salinity,
pH,
and
other
environmental
variables
can
span
nearly
the
full
range
observed
globally
outside.
Bathroom
showerheads,
for
instance,
can
go
from
completely
dry
to
saturated
within
hours
(which
favors
microorganisms
able
to
take
advantage
of
moisture-pulse
events,
including
pathogens)
[23].
In
the
following
sections,
we
outline
three
questions
for
future
research.
(i)
How
did
species
come
to
populate
the
indoor
biome?
(ii)
Which
traits
does
the
indoor
biome
select
for?
(iii)
How
will
changes
in
human
culture
affect
indoor
evolution?
On
the
origin
of
indoor
species
Little
research
explores
how
species
come
to
populate
the
indoor
biome.
We
hypothesize
that,
in
many
cases,
pre-
adaptations
allow
species
to
colonize
built
structures
and
then,
having
colonized,
these
species
respond
to
local
selection
pressures.
The
grain
weevil
(Sitophilus
granar-
ius)
appears
to
have
evolved
to
feed
on
grains
stored
by
ants
and
rodents
and
thus
was
preadapted
to
make
the
transition
to
grains
stored
by
humans
[35].
However,
since
colonizing
human-stored
grains,
S.
granarius
is
likely
to
have
experienced
strong
selection
for
traits
that
facilitate
survival
in
the
very
different
conditions
of
granaries.
Sim-
ilarly,
rodents
of
the
genus
Rattus
appear
to
have
been
predisposed
to
success
as
human
commensals,
with
14
of
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in
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&
Evolution
xxx
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10
4
IA
HI
OH
AR
RI SC
LA
NC FL
KY
WV
TN
VA
OK
KS
AL
IL
MD
ID
SD
WA
MI
PA
UT MS
MN NJ
IN
MA MO
DC
NH
VT
CA
DE
CT
NE
ME
MT
UT
MN
Outdoor
Indoor
(A)
(B)
(C)
AK
VT
NH WI
SD
OR
RI
WA
MO
IA
DE
KS OH
AR
IN
HI
LA
FL
SC
MS
OK
GA
NC
TN
AL
KY
DC
WV
NJ
VA
NE
MEMI
CT PA
MA
IL MD
NY CA
WY
MT
CO ID
NM
AZ
NV
NV
NM
AK
WY
AZ
CO
WI
GA
OR
10
20
30
40
50
Relave humidity (%)
60
70
80
15 20 25
Temperature (°C)
AZ
HI
NV
MS
FL
GA
CA
LA
SC
NC
OK
AK
TN
OH
AR
KY
DE
DC
WV
PA
UT
VA
NM
MO
OR
CT
ID
CO
NJ
IN
MD
MA
MI
RI
IL
VT
NE
ME
IA
WA
WI
NH
KS
SD
MT
WY
MN
AK
–5 0
51012
Temperature (°C)
–40 –25 15
0
Relave humidity (%)
40
20
0
40
20
0
40
20
0
02/24
03/16
04/05
04/25
05/15
06/04
Date (2013)
Outdoor
Temperature (°C)
Relave humidity (%)
Sioux falls, SD
Las vegas, NV
Raleigh, NC
Indoor
06/24
02/24
03/16
04/05
04/25
05/15
06/04
06/24
0
100
50
0
50
100
0
50
100
TRENDS in Ecology & Evolution
Figure
3.
Ambient
conditions
in
the
indoor
biome
can
differ
substantially
from
outdoor
conditions.
(A)
Paired
outdoor
(light
gray)
and
indoor
(black)
values
of
mean
relative
humidity
and
mean
temperature
recorded
in
47
US
states
and
the
District
of
Columbia
across
a
4-month
period.
During
this
part
of
the
year,
most
houses
tend
to
be
warmer
and
less
humid
than
adjacent
outdoor
environments,
but
some
states,
particularly
in
the
southwest
USA,
do
not
follow
this
trend.
(B)
Localities
within
the
USA
differ
in
their
relative
differences
between
indoor
and
outdoor
ambient
conditions.
Orange
bars
show
the
difference
between
mean
indoor
and
outdoor
temperatures.
Gray
bars
show
the
same
difference
for
relative
humidity.
(C)
Three
examples
from
across
the
USA
demonstrate
the
difference
in
temporal
variability
depending
on
locality.
Hourly
point
temperature
(8C)
and
percentage
relative
humidity
measurements
outdoors
(gray)
and
indoors
(black)
across
three
states.
Data
recorded
by
iButton
1
data
loggers
(Hydrochron
iButton
model
DS1923;
Maxim/Dallas
Semiconductor,
Dallas,
TX)
between
February
24,
2013
and
June
24,
2013.
Review Trends
in
Ecology
&
Evolution
xxx
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Vol.
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No.
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TREE-1909;
No.
of
Pages
10
5
61
species
found
inside
the
indoor
biome
in
at
least
some
region
[36].
We
speculate
that
fungal
and
bacterial
species
in
the
home
may
also
include
taxa
that
were
preadapted
for
colonization,
but
in
most
cases
too
little
is
known
about
indoor
microbes
to
identify
their
colonization
history.
For
example,
Abe
and
Hamada
found
that
Scolecobasidium
fungus
isolated
from
bathrooms
and
washing
machines
formed
a
distinct
clade
most
closely
related
to
Scolecoba-
sidium
humicola
isolated
from
plant
litter
[37].
It
is
possi-
ble
that
fungal
isolates
from
bathrooms
represent
a
recently
evolved
lineage
adapted
to
indoor,
soapy
environ-
ments
([38]
suggested
as
much).
However,
it
is
also
possible
that
the
lineage
from
which
these
indoor
populations
derive
has
simply
not
yet
been
sampled.
As
another
exam-
ple,
the
bacterium
Thermus
aquaticus,
which
is
often
found
in
water
heaters,
was
originally
hypothesized
to
have
evolved
from
ancestors
from
hot
springs
[39]
but
no
one
has
yet
studied
how
this
colonization
event
might
have
occurred.
Phylogeographical
and
phylogenomic
advances
promise
to
elucidate
the
stories
of
both
indoor
species
and
the
humans
with
whom
they
have
traveled.
Studies
of
the
black
rat
(Rattus
rattus)
reveal
a
complex
history
in
which
rats
colonized
human
built
environments
multiple
times
independently
in
different
regions
[40].
The
subsequent
history
of
evolution
in
these
lineages
illuminates
patterns
of
human
migration
and
trade.
The
phylogeography
of
insular
populations
of
black
rats
reveals
that
many
distinct
lineages
have
evolved
since
the
human
colonization
of
Indian
Ocean
islands
and
these
lineages
reflect
the
indi-
vidual
colonization
histories
of
different
islands
[41,42].
The
spread
of
the
Norway
rat
(Rattus
norvegicus)
was
later
than
that
of
the
black
rat
(although
also
out
of
Asia)
and
as
it
spread
the
Norway
rat
displaced
the
black
rat
in
many
regions
[43],
setting
the
stage
for
the
possibili-
ty
of
evolution
in
both
species
in
response
not
only
to
climatic
gradients
and
isolation
but
also
to
each
other’s
presence.
Given
that
R.
rattus
has
colonized
most
of
the
world
and,
in
doing
so,
now
experiences
great
variation
in
human
living
conditions,
the
species
represents
a
potential
model
organism
for
the
indoor
biome.
Most
indoor
taxa,
despite
being
encountered
every
day,
have
evolutionary
histories
that
are
poorly
resolved.
The
case
of
roaches
is
emblematic
of
the
huge
gaps
that
exist
even
for
species
that
are
considered
well
studied.
For
decades,
it
has
been
known
that
the
center
of
species
diversity
of
the
cockroach
genus
Blattella
is
Southeast
Asia,
but
only
one
of
the
51
species,
the
German
cockroach
(B.
germanica),
has
become
so
specialized
in
the
built
environment
that
it
is
not
known
to
occur
anywhere
else
[44].
Although
several
studies
have
considered
local
popu-
lation
dynamics
in
B.
germanica,
none
has
considered
its
evolution
relative
to
its
likely
sister
taxa
or
wild
popula-
tions
in
the
region
in
which
it
is
putatively
native.
The
situation
is
similar
for
most
indoor
species,
be
they
ani-
mals,
plants,
fungi,
bacteria,
or
others.
Our
knowledge
of
the
indoor
biome
would
benefit
from
phylogeographical
and
phylogenomic
comparisons
that
include
both
indoor
taxa
and
outdoor
congeners
(e.g.,
[46]).
The
common
bed
bug
(C.
lectularius),
for
example,
occurs
only
in
the
built
environment
and
has
congeners
in
nature
–
bat
bugs
–
that
could
inform
us
about
evolution
in
the
indoor
biome
[45].
The
challenge
in
many
cases
will
be
identifying
potential
sister
lineages
to
include
in
analyses.
Exophiala,
for
example,
is
a
black
yeast
commonly
found
in
sinks
and
dishwashers
in
houses
and
on
steam-bath
walls.
Its
known
counterparts
in
outdoor
areas
are
found
on
the
skins
of
tropical
fruits
and,
because
of
its
occurrence
patterns,
thermotolerance,
acid
tolerance,
osmotolerance,
and
melanization,
its
natural
life
cycle
is
thought
to
be
tied
to
that
of
frugivorous
animals
in
the
tropical
rain
forest
[47].
However,
closer
relatives
might
live
in
other
habitats
but
have
not
yet
been
studied.
Which
traits
does
the
indoor
biome
select
for?
Many
household
organisms
share
phenotypes
and
beha-
viors
with
cave-dwelling
organisms.
Many
indoor
arthro-
pods
have
flattened
bodies
(e.g.,
bed
bugs,
cockroaches,
silverfish),
presumably
because
this
body
type
better
fits
in
crevices
within
houses.
Some
arthropods
in
houses,
like
those
that
live
in
caves,
have
less
acute
vision
but
longer
antennae,
which
are
often
used
to
orient
to
edges
(e.g.,
cockroaches,
silverfish,
crickets).
Cave-dwelling
microbes
are
relatively
unstudied
but,
based
on
the
similarity
of
food
sources,
substrates,
and
climates
in
caves
and
homes,
some
species
of
house-dwelling
microbes
may
have
evolved
in
caves.
In
caves,
animals
tend
either
to
lose
their
ability
to
disperse
(because
dispersal
is
costly
and
the
odds
of
finding
a
new
cave
are
low)
or
to
evolve
the
ability
to
disperse
passively
with
animals
able
to
travel
to
new
caves,
such
as
bats.
We
predict
a
similar
pattern
in
the
indoor
biome,
particularly
in
regions
in
which
indoor
and
outdoor
condi-
tions
are
very
different.
Urban
populations
of
the
weed
Crepis
sancta
that
inhabit
tree
pits
surrounded
by
concrete
Box
2.
Categorizing
species
of
the
indoor
biome
The
species
of
the
indoor
biome
can
be
separated
into
‘intended
introductions’
and
‘unintended
introductions’.
Intended
introductions
are
species
that
humans
intentionally
bring
into
indoor
environments,
often
supporting
their
metabolism
and
sometimes
reproduction.
These
species
include
pets,
house-
plants,
and
species
used
for
food
fermentation.
Such
species
possess
traits
that
increase
their
probability
of
being
indoors;
these
traits
and
species
evolve
as
humans
select
some
lineages
over
others,
either
intentionally
or
otherwise.
While
some
intended
introductions
may
be
true
mutualists
of
humans,
the
fitness
advantage
of
living
with
humans
for
some
other
organisms,
such
as
domestic
cats
or
flowering
plants,
is
less
clear
(but
see
[76]).
Unintended
introductions
constitute
the
other
species
found
in
the
indoor
biome
–
species
that
have
long
been
associated
with
humans
but
have
been
ignored
by
humans
or
deterred
from
occupying
human
dwellings.
These
species
include
human
com-
mensals,
pathogens,
and
parasites
as
well
as
mammals,
arthropods,
fungi,
and
other
species
that
use
indoor
environments
opportunis-
tically.
Many
of
these
species,
such
as
rats
(Rattus
spp.)
and
the
house
mouse
(Mus
musculus),
have
ancient
relationships
with
humans
and
have
spread
with
humans
and
particular
human
cultures.
The
above
framework
excludes
species
that
passively
drift
into
houses
from
surrounding
environments
but
are
not
metabolically
or
reproductively
active
inside
houses.
For
these
species,
houses
are
essentially
restaurants,
hotels,
or
cemeteries
(ecological
sinks
or
traps).
‘Peridomestic’
species,
for
example,
feed
indoors
and
reproduce
outdoors
[77].
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in
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&
Evolution
xxx
xxxx,
Vol.
xxx,
No.
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TREE-1909;
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10
6
have
adapted
to
produce
non-dispersing
seed
types
at
a
higher
frequency
than
rural
populations
[48]
because
it
is
better
to
stay
in
a
crowded
pit
than
to
die
on
the
cement.
Wingless
and
blind
invertebrates
are
common
in
barns,
where
stored
products
are
predictably
transported,
and
are
patchily
distributed
at
geographical
scales
that
are
large
relative
to
the
ability
of
most
invertebrates
to
actively
disperse
[49].
Similarly,
many
indoor
species
appear
to
have
reduced
dispersal
ability.
Camel
crickets,
some
roach
species,
bed
bugs,
silverfish,
and
booklice
lack
flight,
al-
though
flightlessness
is
relatively
rare
among
insects
[50,51].
Even
winged
animals
found
indoors,
such
as
web-
bing
clothes
moths,
are
often
poor
flyers
[15].
Many
bacteria
in
homes
and
human-dominated
envir-
onments
appear
to
be
sufficiently
ubiquitous
in
the
air
that
they
are
neither
dispersal
limited
[52]
nor
able
to
prevent
dispersal
into
bad
habitats.
For
these
taxa,
selection
may
favor
tolerance
of
indoor
conditions
(and
their
fluctuation)
rather
than
particular
dispersal
traits.
Other
taxa
of
bac-
teria
and
other
microbes
are
able
to
reliably
enter
houses
on
humans
and
their
pets
[21,25]
or
arthropods
[53]
and
some
food-borne
taxa
arrive
in
houses
within
food.
In
all
organisms
in
homes,
except
those
able
to
easily
move
in
and
out,
the
fluctuating
conditions
experienced
at
small
scales
in
homes,
such
as
on
showerheads,
should
favor
tolerance
of
fluctuating
stresses
[23].
For
arthropods,
this
often
involves
reduction
in
metabolic
activity.
Indoor
ectoparasites
(e.g.,
fleas,
bed
bugs)
have
evolved
metabolic
strategies
to
withstand
long
periods
without
their
human
or
pet
host
(e.g.,
lower
metabolic
rate,
delayed
molting,
ability
to
engorge
to
several
times
their
body
mass)
[54].
Indoor
silverfish
(Lepisma
saccharina)
and
firebrats
(Thermobia
domestica)
can
survive
long
periods
of
starva-
tion
and
firebrats
can
actively
absorb
water
from
the
atmosphere
[55].
Meanwhile,
one
of
the
most
common
fungi
in
houses,
Aspergillus
fumigatus,
can
grow
across
a
broader
range
of
temperature
conditions
than
other
related
taxa
–
an
ability
that
may
facilitate
its
survival
in
varied
indoor
habitats
[56].
Additionally,
the
bacterium
Deinococcus
radiodurans,
known
for
its
extreme
desicca-
tion
and
UV
tolerance,
appears
to
accumulate
in
building
dust
over
time
indoors
[57].
The
adaptations
that
allow
microbes
to
survive
in
episodically
stressful
conditions,
such
as
those
present
in
dishwashers,
showers,
and
sinks,
may
also
favor
pathogenic
species
and
perhaps
even
the
evolution
of
pathogenecity
[58]
–
a
worrisome
hypothesis,
given
that
we
have
recreated
these
conditions
in
houses
across
the
world.
Interestingly,
the
dependence
of
many
indoor
species
on
passive
or
facilitated
dispersal
means
that
the
composition
of
species
in
a
particular
built
structure
is
likely
to
be
stochastic
(with
the
stochasticity
being
greater
where
the
amount
of
movement
into
the
home
is
lower
and
for
taxa
with
poorer
dispersal
abilities).
Both
roaches
and
bed
bugs
in
apartments
seem
often
to
derive
from
single
introduc-
tion
events
[59].
Until
relatively
recently,
Norway
rats
were
unable
to
colonize
Phoenix,
AZ
due
to
the
relatively
inhospitable
climate
around
the
city
[36].
As
a
consequence
of
the
stochasticity
of
colonization,
parthenogenetic
repro-
duction
may
be
favored
indoors.
At
least
some
species
that
thrive
indoors
are
facultatively
parthenogenetic
[e.g.,
the
American
cockroach
(Periplaneta
americana),
the
Surinam
cockroach
(Pycnoscelus
surinamensis)]
[60].
Whether
the
incidence
of
parthenogenesis
in
indoor
species
is
unusually
high
has
not
been
formally
tested.
A
priori,
animal
species
that
reproduce
indoors
may
also
have
evolved
the
ability
to
tolerate
extensive
inbreeding.
Whether
particular
repro-
ductive
strategies
might
also
be
favored
in
microbes
in
indoor
environments
does
not
appear
to
have
been
consid-
ered.
How
will
changes
in
human
culture
affect
indoor
evolution?
Subtle
features
of
human
culture
have
the
potential
to
have
large
impacts
on
evolution
indoors.
The
spread
of
parasites
and
other
infectious
agents
often
depends
on
intimacy
among
humans
and
between
humans
and
other
animals.
For
example,
genital
lice
(Pthirus
pubis)
moved
from
the
ancestor
of
gorillas
to
humans
in
a
moment
of
some
form
of
intimacy
[61].
Close
interaction
has
allowed
new
microbes
to
enter
human
habitats
through
meat,
milk,
dung,
and
common
vectors
(like
flies,
fleas,
and
ticks).
Classic
epidemic
viral
diseases
of
humans
have
their
ori-
gins
in
the
animals
that
were
domesticated
early
[62,63].
In
some
cases,
intimate
interactions
with
nonhu-
man
animals
lead
to
the
colonization
of
humans
and
homes
with
species
that
spread
globally;
in
others,
they
seem
likely
to
lead
to
more
local
populations.
A
related
aspect
of
human
culture
that
may
affect
the
evolutionary
trajectories
of
indoor
species
is
a
preoccupa-
tion
with
purity
and
pollution
[64].
Many
of
the
visible
organisms
found
in
houses
have
a
‘disgust-evoking
status’.
However,
the
organisms
that
elicit
these
responses
vary
from
place
to
place
(although
see
[27]),
as
do
the
social
stigmas
related
to
these
organisms.
Cultural
conceptions
of
what
is
clean
or
dirty
ultimately
drive
how
we
behave
toward
indoor
species,
especially
those
that
we
label
‘pest
species’,
and
consequently
how
we
shape
the
indoor
biome
[65].
One
could
argue,
for
example,
that
the
widespread
presence
of
antibiotic
resistance
in
the
USA
is
due
to
an
industry-driven
response
to
a
cultural
construct:
the
idea
of
‘germs’
[66].
The
study
of
the
influence
of
culture
on
indoor
evolution
offers
rich
potential
for
new
discoveries
and
important
case
examples
of
rapid
evolution.
Ecological
theory
suggests
that
the
spatial
arrangement
and
density
of
indoor
spaces
within
a
region
may
also
have
an
impact
on
the
evolution
of
indoor
species,
particularly
for
those
whose
fitness
is
higher
indoors
than
outdoors
[67].
Species–area
relationships,
island
biogeographical
models,
and
even
metabolic
theory
predict
that,
as
the
habitat
and
resources
available
in
a
particular
biome
increase,
so
too
should
its
total
(gamma)
diversity.
To
the
extent
that
houses
vary
within
and
among
cities,
we
might
predict
that
beta
diversity
is
also
likely
to
remain
high.
We
hypothesize
that
urbanization
will
increase
the
number
of
species
that
evolve
to
persist
indoors,
with
the
differences
among
homes,
settlements,
and
regions
being
a
more
complex
function
of
the
relative
differences
among
them
in
culture
and
connectedness.
A
trend
toward
sustainable
building
practices
may
also
influence
indoor
evolution.
Strategies
to
improve
energy
efficiency
and
control
of
the
indoor
biome
include
tighter
Review Trends
in
Ecology
&
Evolution
xxx
xxxx,
Vol.
xxx,
No.
x
TREE-1909;
No.
of
Pages
10
7
sealing
of
building
envelopes
[68],
which
has
the
potential
to
influence
all
selection
pressures
indoors,
favoring
the
subset
of
lineages
that
are
best
able
to
enter
sealed
envir-
onments
and
deal
with
self-contained
climate
systems
[69]
and
the
novel
chemistry
of
new
building
materials.
Al-
though
the
impacts
of
sustainable
building
and
new
build-
ing
materials
remains
to
be
fully
explored,
they
seem
likely
to
have
lasting
influences
on
evolution
in
the
indoor
envi-
ronment
–
effects
we
are
likely
to
experience
long
before
they
are
well
studied.
Concluding
remarks
and
future
directions
Although
many
biologists
have
studied
the
evolutionary
processes
at
work
in
indoor
environments,
such
studies
focus
disproportionately
on
pest
organisms.
As
a
result,
most
taxa
of
the
indoor
biome
remain
to
be
considered
in
an
evolutionary
ecological
framework.
As
a
research
field,
the
evolutionary
biology
of
the
indoor
biome
is
interdisciplin-
ary,
situated
at
the
intersections
of
evolutionary
biology,
ecology,
anthropology,
archaeology,
engineering,
architec-
ture
and
design,
human
ecology,
urban
planning,
environ-
mental
history,
and
political
ecology.
There
are
many
avenues
open
for
future
research
on
the
ecology
and
evo-
lution
of
the
indoor
biome
(Box
3).
Arguably,
the
indoor
biome
is
one
of
the
realms
in
which
the
field
of
evolution
offers
the
most
to
humanity.
The
study
of
the
indoor
biome
intersects
with
the
field
of
public
health
and
medicine.
Houses
with
increased
levels
of
fungal,
cockroach,
and
mouse
allergens
are
associated
with
higher
rates
of
asthma
in
children,
for
example,
and
the
absence
of
beneficial
species
indoors
has
been
linked
to
autoimmune
and
allergic
disorders
[70].
Evolutionary
biol-
ogists
have
the
opportunity
to
engage
with
these
basic
and
applied
research
topics
through
the
study
of
indoor
biomes.
Perhaps
more
than
any
other
evolutionary
examples,
the
stories
of
the
species
that
evolve
indoors
are
accessible
to
students
and
other
members
of
the
public
[71].
Already
conservation
biologists
are
engaged
in
a
parallel
movement
to
bring
conservation
stories
to
inhabited
places
[9,72].
Study
of
the
indoor
biome
could
bring
evolution
to
our
doorsteps.
One
framework
in
which
this
could
occur
is
through
citizen
science.
Citizen
science
offers
an
ap-
proach
to
the
study
of
indoor
species
that
simultaneously
engages
the
public,
allows
scientists
to
sample
many
hous-
es,
and
generates
stories
about
ecology
and
evolution
of
which
the
public
is
intricately
a
part
[73].
Recent
studies
engaging
citizens
in
the
study
of
their
own
homes
have
revealed
the
spread
of
two
species
of
giant
invasive
camel
cricket
among
North
American
basements
and
crawl-
spaces
[50],
patterns
of
bacterial
composition
within
and
among
houses
[21],
and
the
distribution
and
composition
of
ants
in
backyards
[74].
Given
that
our
understanding
of
the
indoor
biome
remains
heavily
weighted
toward
North
America
and
parts
of
Europe,
it
will
be
important
to
our
understanding
of
indoor
evolution
to
distribute
projects
more
evenly
across
geographical
regions
[75].
Acknowledgments
This
review
emerged
from
a
catalysis
meeting
at
the
National
Evolutionary
Synthesis
Center
[National
Science
Foundation
(NSF)
EF-
0905606]
supported
by
the
Sloan
Foundation
(2012-5-47
IE).
R.R.D.
was
supported
by
NSF
grant
551819-0654
and
by
the
Southeast
Climate
Science
Center
while
writing
this
review
and
L.J.M.
by
an
NSF
Graduate
Research
Fellowship
Program.
The
authors
thank
S.
Crane,
L.
Fellman,
C.E.
Kraft,
H.
Menninger,
M.
Siva-Jothy,
J.
Siegel,
W.
Wilson,
and
two
anonymous
reviewers
for
their
helpful
feedback.
References
1
Martin,
L.J.
et
al.
(2012)
Mapping
where
ecologists
work:
biases
in
the
global
distribution
of
terrestrial
ecological
observations.
Front.
Ecol.
Environ.
10,
195–201
2
Ellis,
E.C.
and
Ramankutty,
N.
(2008)
Putting
people
in
the
map:
anthropogenic
biomes
of
the
world.
Front.
Ecol.
Environ.
6,
439–447
3
Kitzes,
J.
et
al.
(2007)
Current
methods
for
calculating
national
ecological
footprint
accounts.
Sci.
Environ.
Sustain.
Soc.
4,
1–9
Box
3.
Outstanding
questions
Are
houses
similar
enough
to
consider
them
a
single
biome
or
are
they
more
akin
to
remote
islands
(multiple
biomes)?
Would
one
expect
convergent
or
divergent
evolution
to
appear
across
habitats
in
the
indoor
biome?
How
will
climate
change
affect
both
building
design
and
the
outdoor
environment
and,
subsequently,
determine
which
spe-
cies
thrive
indoors?
Was
there
an
adaptive
evolutionary
syndrome
of
phenotypic
or
genomic
changes
that
accompanied
the
evolution
of
house
living
in
many
species
in
many
regions?
Has
evolution
of
indoor
microbes
(or
colonization
by
preadapted
microbes)
influenced
our
own
microbiome
health?
Can
we
design
buildings
to
function
as
healthier
human/microbe
habitats?
Are
ecological
interactions
specific
or
unique
in
any
way
indoors
or
are
they
analogous
to
outdoor
interactions?
How
many
and
which
species
are
found
exclusively
in
the
biome?
Have
any
species
moved
from
the
indoor
biome
to
other,
outdoor
biomes?
Is
there
speciation
indoors?
What
is
the
role
of
horizontal
gene
transfer
in
the
indoor