An
evolutionary
framework
for
studying
mechanisms
of
social
behavior
NESCent
Working
Group
on
Integrative
Models
of
Vertebrate
Sociality:
Evolution,
Mechanisms,
and
Emergent
Properties,
Hans
A.
Hofmann
1
,
Annaliese
K.
Beery
2
,
Daniel
T.
Blumstein
3
,
Iain
D.
Couzin
4
,
Ryan
L.
Earley
5
,
Loren
D.
Hayes
6
,
Peter
L.
Hurd
7
,
Eileen
A.
Lacey
8
,
Steven
M.
Phelps
1
,
Nancy
G.
Solomon
9
,
Michael
Taborsky
10
,
Larry
J.
Young
11
,
and
Dustin
R.
Rubenstein
12
1
The
University
of
Texas
at
Austin,
Department
of
Integrative
Biology
and
Institute
for
Cellular
and
Molecular
Biology,
2415
Speedway,
Austin,
TX
78712,
USA
2
Smith
College,
Department
of
Psychology
and
Program
in
Neuroscience,
Northampton,
MA
01063,
USA
3
University
of
California,
Department
of
Ecology
and
Evolutionary
Biology,
621
Young
Drive
South,
Los
Angeles,
CA
90095-1606,
USA
4
Princeton
University,
Department
of
Ecology
and
Evolutionary
Biology,
Princeton,
NJ
08644,
USA
5
University
of
Alabama,
Department
of
Biological
Sciences,
300
Hackberry
Lane,
Box
870344,
Tuscaloosa,
AL
35487,
USA
6
University
of
Tennessee
at
Chattanooga,
Department
of
Biological
and
Environmental
Sciences,
Chattanooga,
TN
37403,
USA
7
University
of
Alberta,
Department
of
Psychology
and
Centre
for
Neuroscience,
Edmonton,
Alberta,
T6G
2E9,
Canada
8
University
of
California
at
Berkeley,
Museum
of
Vertebrate
Zoology
and
Department
of
Integrative
Biology,
3101
Valley
Life
Sciences
Building,
Berkeley,
CA
94720-3160,
USA
9
Miami
University,
Department
of
Biology,
Oxford,
OH
45056,
USA
10
University
of
Bern,
Institute
of
Ecology
and
Evolution,
Division
of
Behavioural
Ecology,
Wohlenstrasse
50a,
3032
Hinterkappelen,
Switzerland
11
Emory
University,
Center
for
Translational
Social
Neuroscience,
Yerkes
National
Primate
Research
Center,
954
Gatewood
Road,
Atlanta,
GA
30329,
USA
12
Columbia
University,
Department
of
Ecology,
Evolution
and
Environmental
Biology,
1200
Amsterdam
Avenue,
New
York,
NY
10027,
USA
Social
interactions
are
central
to
most
animals
and
have
a
fundamental
impact
upon
the
phenotype
of
an
individual.
Social
behavior
(social
interactions
among
conspecifics)
represents
a
central
challenge
to
the
integration
of
the
functional
and
mechanistic
bases
of
complex
behavior.
Traditionally,
studies
of
proximate
and
ultimate
ele-
ments
of
social
behavior
have
been
conducted
by
dis-
tinct
groups
of
researchers,
with
little
communication
across
perceived
disciplinary
boundaries.
However,
recent
technological
advances,
coupled
with
increased
recognition
of
the
substantial
variation
in
mechanisms
underlying
social
interactions,
should
compel
investi-
gators
from
divergent
disciplines
to
pursue
more
inte-
grative
analyses
of
social
behavior.
We
propose
an
integrative
conceptual
framework
intended
to
guide
researchers
towards
a
comprehensive
understanding
of
the
evolution
and
maintenance
of
mechanisms
gov-
erning
variation
in
sociality.
The
study
of
social
behavior
in
the
21st
century
All
animals
interact
with
conspecifics
at
some
point
in
their
lives.
Members
of
the
same
species
tend
to
be
each
other’s
fiercest
competitors
and
strongest
allies,
as
evidenced
by
the
intense
cooperation
and
conflict
that
characterize
many
intraspecific
interactions
[1].
These
interactions
are
the
products
of
genetic,
epigenetic,
endocrine,
and
neural
mechanisms
that
–
in
conjunction
with
environ-
mental
conditions
–
affect
Darwinian
fitness
and
evolve
via
natural
selection.
Building
upon
Aristotle’s
four
questions,
Tinbergen
[2]
posited
that
understanding
behavior
requires
the
integration
of
studies
of
mechanism
and
function.
Only
by
asking
questions
both
from
a
proximate
perspective
(i.e.,
focusing
on
causation
and
development)
and
an
ultimate
perspective
(i.e.,
focusing
on
adaptive
value
and
evolutionary
descent)
can
behavior
be
fully
understood.
Social
behavior
in
particular
lends
itself
to
such
an
integrative
approach
not
only
because
it
com-
mands
the
attention
of
many
disciplines
[3]
but
also
be-
cause
even
many
behaviors
commonly
considered
non-
social
often
occur
in
a
social
context
(e.g.,
mating,
fighting,
parental
care).
Social
behavior
is
also
special
because
the
selective
agents
are
other
members
of
the
same
species,
and
this
results
in
intriguing
evolutionary
dynamics.
Nev-
ertheless,
in
the
intervening
decades
since
Tinbergen’s
Corresponding
authors:
Hofmann,
H.A.
(hans@utexas.edu);
Rubenstein,
D.R.
(dr2497@columbia.edu).
Keywords:
evolution;
social
behavior;
complex
sociality;
group-living;
neural
circuits;
hormones;
genomics.
581
Konstanzer Online-Publikations-System (KOPS)
URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-0-290994
Erschienen in: Trends in Ecology & Evolution ; 29 (2014), 10. - S. 581-589
https://dx.doi.org/10.1016/j.tree.2014.07.008
seminal
work
[2]
studies
of
behavioral
mechanisms
have
proceeded
largely
independently
of
analyses
of
ultimate-
level
explanations
for
social
behavior
[4].
Among
the
fac-
tors
contributing
to
this
disconnect
are
the
challenges
of
applying
laboratory
methods
to
field
research
where
most
complex
social
behaviors
are
studied,
as
well
as
long-
standing
differences
in
terminology,
conceptual
foci,
and
study
taxa
[3,5–7].
Progress
towards
an
integrated
under-
standing
of
the
evolution
of
social
behavior
has
been
limit-
ed.
Only
now,
50
years
after
Tinbergen’s
seminal
1963
publication
[8],
efforts
to
integrate
neural,
genetic,
epige-
netic,
physiological,
ecological,
and
evolutionary
studies
of
behavior
are
gaining
increased
prominence
[7,9–11,101],
facilitated
by
multiple
factors,
including
innovative
tech-
nologies
(e.g.,
high-throughput
sequencing
[12]),
and
analytical
procedures
(e.g.,
improved
statistical
methods
for
modeling
and
comparative
analyses
[13])
as
well
as
the
increasing
ease
of
application
of
these
advances
to
field
studies
(e.g.,
biotelemetry
[14,15]).
As
a
result,
it
is
in-
creasingly
possible
to
address
all
four
of
Tinbergen’s
ques-
tions
concurrently
for
the
same
species
[3,7,10,11,16],
which
is
most
effective
when
using
modern
comparative
methods
[13].
Such
integration
is
crucial
if
studies
of
behavior
are
to
contribute
to
solutions
to
pressing
biologi-
cal
problems.
For
example,
only
by
understanding
the
evolutionary
origins
of
diverse
mechanisms
can
we
begin
to
predict
how
species
will
respond
to
global
change
[17].
Similarly,
a
thorough
understanding
of
the
adaptive
con-
sequences
of
diverse
mechanisms
can
help
to
identify
novel
model
systems
for
studies
of
specific
neuropsychiatric
dis-
orders
[18].
Integrating
Tinbergian
levels
of
analysis
is
especially
appropriate
for
the
study
of
social
behavior
which,
given
its
complexity,
must
be
approached
from
an
integrative
perspective.
Historical
perspectives
Although
most
current
textbooks
on
animal
behavior
prominently
feature
Tinbergen’s
four
questions
[19–21],
researchers
have
been
slower
to
adopt
the
type
of
truly
integrative
approach
that
Tinbergen
originally
proposed
[2].
Indeed,
studies
of
behavior
remain
to
some
extent
divided
into
efforts
to
understand
ultimate-
versus
proxi-
mate-level
reasons
for
variation
in
social
interactions
[3].
Each
tradition
offers
important
impulses
for
the
integra-
tive
conceptual
framework
we
outline
below.
Ecological
and
evolutionary
traditions
Ethologists
and
behavioral
ecologists
have
emphasized
field
studies
of
ultimate-level
aspects
of
social
behavior.
Crucial
concepts
addressed
by
such
studies
include
the
roles
of
kinship
and
inclusive
fitness
in
shaping
social
interactions,
as
well
as
the
effects
of
specific
ecological
parameters
on
social
structure
[8,22].
Such
studies
have
the
advantage
of
documenting
patterns
of
behavior
and
the
associated
adaptive
consequences
in
the
environments,
and
under
the
selective
regimes
experienced
by
the
study
organisms.
However,
such
analyses
have
tended
to
ignore
the
physiological,
neural,
and
genetic
mechanisms
under-
lying
these
behavioral
patterns
as
part
of
a
‘phenotypic
gambit’,
a
heuristic
construct
positing
that
detailed
knowledge
of
the
mechanistic
bases
for
behavior
is
not
required
for
an
understanding
of
its
function
and
evolution
[23,24].
As
a
result,
such
studies
have
been
typically
unable
to
determine
how
underlying
mechanisms
shape
observed
behavioral
responses
to
external
environments,
including
generating
significant
individual
variation
in
response
to
similar
external
environments.
Neuroendocrine
and
genetic
foundations
Psychologists
and
neuroscientists
interested
in
social
be-
havior
have
followed
an
often
parallel
but
distinct
research
tradition
that
emphasizes
its
physiological,
neuroendocrine,
and
genetic
bases.
Prominent
themes
have
included
the
roles
of
learning
and
ontogenetic
experience
on
social
inter-
actions,
as
well
as
the
effects
of
hormone
levels
in
both
generating
and
mediating
specific
patterns
of
behavior.
Such
studies
are
typically
conducted
under
laboratory
conditions
and
involve
a
limited
number
of
‘model’
study
organisms,
thereby
offering
important
opportunities
for
controlled
experimentation,
often
employing
tools
specific
to
the
organisms
under
study.
However,
these
analyses
have
tended
to
employ
highly
inbred
study
organisms
that
live
in
simplistic
laboratory
environments
[25],
thereby
largely
precluding
consideration
of
the
functional
contexts
in
which
behavior
–
particularly
complex
social
behavior
–
occurs
and
has
evolved
[26].
As
a
result,
studies
of
proximate-level
mechanisms
of
social
behavior
generally
cannot
address
the
potential
impacts
of
variable
environmental
conditions.
The
power
of
integration
Although
numerous
opportunities
exist
for
multidisciplin-
ary
research,
at
present
we
lack
an
appropriate
conceptual
framework
–
including
a
common
language
for
describing
social
behavior
–
to
develop
an
integrative
understanding
of
the
evolution
of
social
behavior.
To
capitalize
upon
emerging
opportunities
we
need
predictive
models
of
social
interactions
that
integrate
function
and
mechanism,
and
that
can
be
applied
to
diverse
taxa
over
a
range
of
social
and
ecological
contexts.
We
offer
here
such
an
integrative
framework
of
sociality
(Figure
1A),
one
that
incorporates
individual
variations
in
ecology,
fitness,
and
experience
as
well
as
the
neural,
physiological,
genetic,
and
developmen-
tal
mechanisms
underlying
social
behavior.
We
outline
ways
in
which
researchers
can
use
this
framework
to
dissect
mechanisms
of
social
behavior
in
free-living
ani-
mals
exposed
to
the
real-world
ecological
and
evolutionary
factors
that
shape
such
behavior.
We
do
so
in
a
manner
that
will
open
up
innovative
avenues
for
comparison
across
disparate
taxonomic
groups.
Importantly,
this
framework
can
be
extended
to
other
types
of
complex
behaviors
(e.g.,
finding
food
or
a
suitable
habitat,
migratory
behavior,
learning
and
memory
formation)
and
therefore
acts
as
a
blueprint
for
the
integrative
study
of
behavior.
An
integrative
framework
Clearly,
combining
proximate
and
ultimate
approaches
to
the
same
phenomenon
generates
opportunities
for
understanding
social
behavior
that
are
not
possible
through
either
tradition
alone.
For
example,
because
the
genetic,
molecular,
and
neural
mechanisms
underlying
behavior
are
subject
to
selection
and
have
a
phylogenetic
582
(A)
(B)
Internal attributes External attributes
Neural and
mo
lecular
attr
ibutes
Sensory, memory, valuati
on
, a
nd
motor centers
rJ
Neuro
anatomy
Neural gene Receptor
expres
si
on
ligand binding
Ufe-h istory traits
Neural
activ
it
y
lndi
viduall
Individual 2
Individual n
Behavior
I>D
0
0
u
UJ
"'
·o
0
Vl
Ha
bi
tat
Re
so
u
rc
e Predation/
structure di
st
ribution
pa
r
as
itism
Di
stribu
tio
n
Ki
ns
hip
Dem
ogra
ph
y
Functional contexts
of
social grouping
Predator
Re
so
urce
avo
id
anc
e
ac
qu
is
ition
Mate
Offs
pring
Ho
me
o-
acq
uisition
ca
re
stas
is
Internal attributes Functional External
attributes
Neuromolecular Life-history contexts Ecological Social
SpeciesA • • • • • • • • •
SpeciesB • • • • • • • • • • • • • • • • •
SpeciesC • • • • • • • • • • • • • • • • • •
SpeciesD • •
••
• • • • • • • • • • • • • •
SpeciesE •
••
• • • • •
•••••
• •
TRENDS
i1
Ecology &
E10/tA/on
Figure
1.
An integrative framework
for
the study
of
social behavior. !AI The framework incorporates external (ecology and social environment) and internal attributes
(neural and molecular measures together
with
intrinsic life-history traits) in which individuals and populations can vary. Note that even subtle differences over
time
and
among individuals
or
species in neuraVmolecular characteristics can result
in
functional variation, giving rise to behavioral diversity. Triangles
with
gradients represent! he
continuous
or
semi-<>Ontinuous
nature
of
the variables, indicating a range from high to low. (B) Evolutionary processes influence internal attributes (such as neural and
molecular mechanisms and life-history traits) in relation
to
external attributes (ecological characteristics and social group traits) and determine social behavior within
different functional contexts. Multivariate approaches can be used
to
identify co-variance patterns within and across populations
or
species
at
ecological, individual, socia
I,
and/or mechanistic levels. Variation
in
color intensity represents quantitative variation
in
the attributes similar
to
the gradients
in
the triangles
in
(A).
history,
they
need
to
be understood
in
a
variety
of social
and
ecological contexts
within
an
explicitly integrative
framework
[1]. Conversely, understanding
the
nature
of
these
mechanisms
can
help
to
reveal why responses to
variable environmental conditions
take
the
forms
that
they
do [
27]
.
The
study
of
social behavior,
in
particular,
is
uniquely positioned
to
benefit from
such
integration
for
several reasons.
First,
as
noted
above, social behavior is
583
nearly
ubiquitous,
with
clear
functional
ties
to
crucial
issues
such
as
conservation
and
human
health.
Second,
previous
research
has
been
remarkably
productive
in
iden-
tifying
the
ecological
conditions
that
shape
the
social
be-
havior
of
a
wide
range
of
taxa
(e.g.,
[9,28,29]).
Third,
detailed
investigations
of
the
mechanistic
bases
for
social
behavior
have
been
completed
for
several
model
organisms
(e.g.,
[30,31]),
providing
an
important
baseline
for
studies
of
other
taxa.
Although
studies
of
social
behavior
are
not
unique
in
offering
such
opportunities,
few
aspects
of
or-
ganismal
biology
are
as
clearly
and
firmly
poised
to
forge
innovative
and
integrative
perspectives
on
phenotypic
variation
[32].
Developing
a
truly
integrative
view
of
social
behavior
requires
an
appropriate
conceptual
framework
that
will
(i)
facilitate
identification
of
general,
potentially
causal,
rela-
tionships
between
behavior
and
other
aspects
of
the
biolo-
gy
of
an
organism,
(ii)
improve
our
ability
to
generate
testable
predictions
regarding
these
relationships,
and
(iii)
enhance
our
ability
to
identify
the
most
suitable
study
systems
for
a
given
behavioral
attribute.
We
propose
here
such
a
framework
that
is
aimed
at
(i)
facilitating
under-
standing
of
the
diversity
of
regulatory
processes
of
social
behavior
in
an
ecological
and
evolutionary
context,
(ii)
providing
a
roadmap
for
generating
testable
predictions
from
existing
data,
and
(iii)
identifying
suitable
model
systems
for
simultaneous
study
in
the
laboratory
and
field.
We
believe
that
this
framework
serves
to
bridge
the
his-
torical
conceptual
gap
between
relevant
biological
disci-
plines,
thereby
paving
the
way
for
a
comprehensive
and
truly
integrated
understanding
of
social
behavior.
Functional
explanations
for
proximate
mechanisms
Causes
for
social
grouping
Social
behavior
occurs
in
many
forms
and
contexts,
but
group-living
organisms
exhibit
some
of
the
most
complex
forms
of
social
behavior.
Understanding
how
and
why
animals
form
groups
represents
an
ideal
situation
in
which
to
develop
an
integrative
framework
of
complex
social
behavior
because
it
involves
many
forms
of
positive
and
negative
social
interactions.
Empirical
studies
of
verte-
brates
and
invertebrates
have
demonstrated
that
animals
typically
form
groups
for
one
or
more
of
five
functional
reasons:
(i)
predator
avoidance;
(ii)
resource
acquisition;
(iii)
mate
acquisition;
(iv)
offspring
care;
and
(v)
homeosta-
sis
[33]
(Figure
1A).
These
functional
contexts,
however,
cannot
always
be
clearly
distinguished
when
conspecifics
interact
under
natural
conditions.
Understanding
the
mechanisms
underlying
social
grouping
can
provide
insights
into
why
groups
form
and,
perhaps
more
impor-
tantly,
why
group-living
has
evolved.
For
example,
we
are
only
beginning
to
understand
that
the
neural
and
molecu-
lar
mechanisms
underlying
social
behaviors
–
as
is
the
case
for
all
phenotypes
–
are
the
result
of
interactions
between
genetic,
environmental,
developmental,
and
epigenetic
processes
[7].
Comparative
studies
have
illuminated
the
behavioral,
neural,
and
molecular
underpinnings
of
social
behavior,
suggesting
that
mechanisms
regulating
behavior
in
similar
contexts
might,
in
part,
be
highly
conserved
across
diverse
vertebrate
taxa,
as
has
been
suggested
for
paternal
care
in
mammals
and
teleost
fishes
[34].
By
contrast,
similar
behaviors
in
different
contexts
or
time-
periods
can
also
result
from
different
mechanisms.
For
example,
territorial
aggression,
in
the
context
of
mate
acquisition,
is
often
modulated
by
sex
steroids,
such
as
androgens,
whereas
aggression
outside
of
reproduction
is
often
modulated
by
other
hormonal
mechanisms
[35].
Im-
portantly,
temporal
differences
in
neurochemical
and
mo-
lecular
regulatory
mechanisms
or
variation
across
individuals
or
species
result
in
functional
variation
in
sensory,
memory,
valuation,
and
motor
centers.
Thus,
the
expression
of
seemingly
identical
behavioral
patterns
in
different
reproductive
contexts
or
seasons
–
or
in
differ-
ent
individuals
or
species
–
might
involve
diverse
regula-
tory
processes.
Understanding
these
processes
in
the
context
of
social
behavior
can
help
to
inform
us
how
and
when
groups
form,
and
whether
similar
associations
in
different
species
are
driven
by
the
same
or
different
un-
derlying
mechanisms.
Neural
mechanisms
in
social
species
Modern
biology
has
long
moved
beyond
the
fruitless
debate
about
the
relative
contributions
of
nature
versus
nurture,
and
instead
has
come
to
the
insight
that
behavior
–
in
common
with
any
other
phenotype
–
is
the
result
of
inter-
actions
among
genetic,
environmental,
developmental,
and
epigenetic
processes.
Nevertheless,
how
these
neural
and
molecular
mechanisms
evolve
is
much
less
well
under-
stood.
Four
different
hypotheses
have
been
proposed
[7,36]:
(i)
the
neural
and
molecular
substrates
of
behavior
might
be
conserved
even
though
the
resulting
behavior
patterns
have
evolved
in
parallel
(deep
homology
[37]);
(ii)
independently
evolved
mechanisms
might
result
in
similar
behavioral
functions
(e.g.,
[38]);
(iii)
molecular
and
neural
pathways
might
diverge
through
time
with
no
concomitant
change
in
the
phenotype
(developmental
system
shift
[39]);
or
(iv)
conserved
molecular
mechanisms
can
become
asso-
ciated
with
divergent
functions
and
phenotypes
over
evo-
lutionary
time
(phenologs
[40]).
These
apparently
opposing
scenarios
are
in
fact
not
mutually
exclusive,
and
all
can
shape
different
behavioral
phenotypes
across
populations
or
species
such
that
a
given
functionally
equivalent
behav-
ioral
phenotype
might
arise
from
several
different
mecha-
nisms.
Support
can
be
found
for
all
four
hypotheses
in
a
diver-
sity
of
social
organisms.
For
example,
monogamous
mating
systems
have
evolved
independently
numerous
times
in
many
taxa,
but
the
formation
of
pair
bonds
might
involve
different
(e.g.,
prairie
vole
vs
California
mouse
[38])
or
conserved
(e.g.,
prairie
voles
and
convict
cichlid
fish
[30,41])
neuroendocrine
pathways.
Similarly,
there
is
sig-
nificant
neuroendocrine
variation
in
the
regulation
of
ter-
ritorial
aggression,
but
the
central
role
of
the
biogenic
amine
serotonin
appears
to
be
conserved
across
animals
[42–44].
A
well-known
example
of
developmental
system
drift
(i.e.,
developmental
pathways
diverge
in
response
to
selection,
although
the
resulting
phenotypes
do
not
change)
concerns
sex-determining
mechanisms,
where
very
different
underlying
mechanisms
involving
chromo-
some
dosage,
sex-determining
genes,
or
environmental
factors
such
as
temperature
or
social
status
[45–47]
give
rise
to
males
and
females
with
sex-specific
behaviors.
In
584
the
context
of
social
behavior,
developmental
system
drift
can
mean
that
behavioral
responses
or
brain
regions
that
regulate
behavior
can
be
homologous
even
though
their
morphological
substrates
or
developmental
origins
are
not
[7].
Phenologs,
by
contrast,
comprise
conserved
gene
net-
works
which
become
associated
with
very
different
pheno-
types
over
the
course
of
evolution
[40].
For
example,
nonapeptides
regulate
pair-bonding
behaviors
across
ver-
tebrates
[30,41],
and
orthologs
of
the
oxytocin
or
vasopres-
sin
ancestral
gene
also
regulate
mating
behavior
in
nematodes
[48]
and
leeches
[49].
The
study
of
these
con-
vergent
and
divergent
pathways
in
conjunction
with
a
detailed
understanding
of
the
survival
value
and
fitness
consequences
of
specific
behavior
patterns
promises
to
yield
insights
into
general
principles
underlying
social
evolution
at
both
proximate
and
ultimate
levels.
Conceptual
relationships
between
mechanisms
and
function
A
comprehensive
understanding
of
variation
in
sociality
requires
not
only
the
study
of
social
behavior
(i.e.,
the
interactions
among
conspecifics)
but
also
of
reproductive
behavior
(i.e.,
the
regulation
of
who
mates
with
whom)
and
social
organization
(i.e.,
the
patterns
of
association
within
and
between
groups)
(see
[22]
for
detailed
discussion).
Moreover,
a
truly
integrative
understanding
of
social
evo-
lution
requires
the
reconstruction
of
the
evolutionary
histo-
ries
of
social
traits
and
the
characterization
of
relationships
among
the
different
regulatory
mechanisms
responsible
for
patterns
of
social
behavior.
Distinct
behavioral
traits
do
not
operate
independently
and
are
not
acted
upon
by
selection
in
isolation
from
one
another,
even
though
they
are
usually
studied
in
this
manner
[26].
Instead,
suites
of
behavioral
patterns
commonly
co-vary,
forming
overall
social
systems
and
life-history
strategies
that
can
differ
within
and
among
individuals
[50],
as
well
as
across
populations
and
species
[51].
Similarly,
behavioral
patterns
generally
co-vary
with
endocrine
and
neural
measures.
For
example,
across
verte-
brates,
competing
phenotypes
often
differ
in
trade-offs
be-
tween
traits
that
affect
fitness,
including
body
coloration,
aggression,
and
immune
function
[52,53].
Strong
correla-
tional
selection
is
generally
thought
to
result
in
such
co-
adapted
trait
complexes
[54],
with
pleiotropic
hormonal
systems
playing
a
central
role
[55,56].
Neuroendocrine
sys-
tems
might
thus
promote
or
constrain
divergence
and
spe-
ciation
because
the
effects
of
disruptive
selection
on
one
trait
are
transferred
to
the
other
trait
in
either
a
synergistic
or
antagonistic
manner
[53,56].
We
propose
a
framework
for
the
integrative
study
of
complex
social
behavior
that
formalizes
conceptual
rela-
tionships
between
mechanisms
and
function
(Box
1).
Spe-
cifically,
we
propose
a
list
of
attributes,
either
external
(e.g.,
ecological
characteristics
or
social
and/or
demograph-
ic
traits
of
the
group)
or
internal
(i.e.,
neural
and
molecular
characteristics,
life-history
traits)
that
can
be
quantified
(repeatedly
and
simultaneously,
if
necessary)
in
multiply-
interacting
individuals
(Figure
1A).
Importantly,
these
attributes
are
much
broader
than
the
kinds
of
elemental
behavior
patterns
(e.g.,
aggression
towards
an
intruder;
dichotomous
female
mate-choice)
that
are
typically
exam-
ined
in
most
mechanistic
studies
conducted
in
laboratory
settings.
We
also
propose
a
multivariate
approach
for
identifying
patterns
of
covariance
and
for
reducing
com-
plexity
in
such
datasets
(e.g.,
principal
components
at
ecological,
individual,
social,
and
mechanistic
levels)
with
the
goal
of
unraveling
the
processes
that
govern
the
evo-
lution
of
the
neural
and
molecular
mechanisms
underlying
social
behavior
(Figure
1B).
These
insights
provide
quan-
tifiable
variables
that
can
facilitate
a
thorough
under-
standing
of,
and
generate
testable
predictions
on,
the
causes,
origins,
and
functional
consequences
of
behavioral
variation
within
and
across
populations
and
species.
External
attributes:
ecological
characteristics
and
social
group
traits
The
mechanisms
regulating
social
behaviors
are
affected
by
external
conditions
including
the
ecology
and
social
environment
of
an
individual
(Figure
1A).
Importantly,
these
attributes
can
differentially
affect
group
members.
For
example,
habitat
structure,
resource
distribution,
or
risk
of
predation
and
parasitism,
can
differentially
influ-
ence
the
behavior
of
dominant
and
subordinate,
or
male
and
female,
group
mates
[57].
Such
parameters
can
also
influence
the
distribution
and
behavior
of
one
sex,
which
in
turn
can
affect
the
behavior
of
the
opposite
sex
[58].
Likewise,
the
demographic
and
kin
composition
of
a
popu-
lation
can
affect
decision-making
in
juveniles
(Box
2)
[59–
61].
The
costs
and
benefits
of
living
in
groups
can
affect
the
evolution
of
neural
pathways
underlying
aggressive
and
cooperative
behaviors,
which
in
turn
might
affect
group
composition
and
persistence,
and
ultimately
population
structure
(e.g.,
estrildid
finches
[62]).
Internal
attributes:
life-history
traits
The
neural
processes
underlying
social
behaviors
are
also
influenced
by
a
variety
of
attributes
of
the
individual,
including
sex,
reproductive
state,
age,
condition,
and
expe-
rience
(Figure
1A),
all
of
which
can
affect
the
opportunities
Box
1.
An
integrative
framework
of
sociality
Our
framework
explains
patterns
of
social
behavior
that
are
most
frequently
studied
(e.g.,
mating
behavior,
offspring
care).
In
reality,
these
apparently
disparate
behavioral
patterns
are
linked
by
ecological
factors
at
one
causal
level
and
a
common
neuromole
cular
substrate
at
another.
Thus,
both
ultimate
and
proximate
forces
will
shape
and
constrain
behavioral
strategies
to
vary
along
principal
component
dimensions.
Similarly,
there
are
functional
relationships
between
individual
neural
and
molecular
attributes
(e.g.,
hormone
levels
are
functionally
linked
to
receptor
densities).
Components
of
variation
in
these
dimensions
will
reflect
the
organization
of
parts
of
the
mechanism
into
a
functioning
whole.
For
example,
behavioral
patterns
cluster
into
functional
sets
(e.g.,
monogamous
pair bonding,
parental
care,
territorial
defense,
etc.).
Each
principal
component
of
variation
in
traits
such
as
neurotrans
mitter
and
neuromodulator
expression
and
reception
in
the
nuclei
of
the
social
decision making
network
in
these
organisms
should
relate
to
biologically
meaningful
variation
in
behavior.
A
reasonable
starting
point
is
to
model
a
one to one
correspondence
between
the
principal
components
of
behavior
and
those
of
the
mechanistic
underpinnings.
Aside
from
this
larger
aim
of
identifying
correlations
between
axes
of
mechanisms
and
axes
of
behavior,
there
is
a
practical
benefit
to
analyzing
principal
components
of
behavioral
variation,
or
variation
in
mechanism:
to
identify
the
set
of
the
most
robust,
efficient,
proxy
measures
for
causal
mechanisms
and/or
behavioral
variation.
585