DOI: http://dx.doi.org/10.7551/978-0-262-31050-5-ch025
TheEvolutionofTemporalPolyethism
1 , Neem Serra
1
2
Heather J. Goldsby
, Fred Dyer
, Benjamin1K err , Charles2 Ofria
1 Uni
v ersity of W ashington, Seattle, W A 98195
State Uni v ersity , East Lansing, MI 48824
2 Michigan
Abstract
that include foraging, caring for the brood, b uilding hone ypots, guarding the hi v e, or cooling the hi v e through f anning (Jandt and Dornhaus, 2009).
T emporal polyethism is a method of di vision of labor e xhibited by m an y eusocial insect colonies, where the type of task
One form of task-related di vision of labor e xhibited by
an indi vidual attempts is correl ated with its age. The e v oluman y eusocial colonies istempor al polyethism
, where a
tionary pressures that gi v e rise to this widely-observed pattern are still not fully kno wn. The long generation times of
w ork er’ s age is correlated with the type of task it per eusocial insects combined with the complications associated
forms (Franks et al., 1997; H ¨olldobler and W ilson, 2009;
with performing artificial selection e xperiments on colonies
of or g anisms mak es this topic challenging to in v estigate us- Robson and Beshers, 1997; Sendo v a-Franks and Franks,
ing or g anic systems. In this paper , we use digital e v olution to 1993; T ofilski, 2002; T ofts, 1993; T raniello and Rosengaus,
1997). F or e xample, within a hone ybee colon y , a w ork er bee
e xplore whether temporal polyethism may result from pressures to preserv e colon y members in the f ace of v arying de- may progress sequentially through four castes: cell cleangrees of risk associated with dif ferent tasks. Specifically , we ing caste, broodnest caste, food storage caste, and forager
require a colon y of digital or g anisms to repeatedly perform a
W ithin ant colonies, a similar shift
set of tasks in order for the colon y to replicate. W e associate caste (Seele y , 1982).
is
performed
from
acti
vities within the nest, such as brood
the dif ferent tasks with dif ferent lethality risks. Under these
conditions, we observ e that the digital or g anisms e v olv e to care, to foraging acti vities outside the nest (H ¨olldobler and
perform the less risk y tasks earlier in their life and more risk y W ilson, 2009).Researchers are still acti v ely e xploring the
tasks later in life, re g ardless of the order in which the tasks
causes and mechanisms underlying this di vision of labor patwere performed by the ancestor or g anism at the start of the
tern. In this paper , we study the e v olutionary conditions that
e xperiment. These results demonstrate that pressures resultcan gi v e rise to temporal polyethism.
ing from the relati v e riskiness of v arious tasks and aging is
suf ficient to f a v or the e v olution of temporal polyethism.
T w o h ypotheses ha v e bee n proposed to e xplain tempo-
ral polyethism. Thetask-riskinessh ypothesis posits that an
indi vidual’ s age i s causally link ed to the task that it per Introduction
forms (H ¨olldobler and W ilson, 2009; Robson and Beshers,
Division of labor, where indi viduals specialize on specific 1997; T raniello and Rosengaus, 1997).
This causal relaroles and cooperate to survi v e, is hailed as a strate gy central
tionship is thought to ha v e e v olv ed because of a pressure
to the success of eusocial insect, crustacean, and mammal to conserv e w ork force members and thus to ha v e older
colonies (Crespi, 2001; Duf fy, 2003; H ¨olldobler and W ilson,
members (who are closer to death) perform more risk y
2009; Jandt and Dornhaus, 2009; Queller and Strassmann, tasks (H ¨olldobler and W ilson, 2009).
F or e xample, forag2003; W ilson, 1980). W ithin nature, eusocial or g anisms ing, a task commonly responsible for the loss of 1% to 10%
are reno wned for e xhibiting
r epr oductive division of labor
,
of the colon y population per day (H ¨olldobler and W ilson,
where members of the reproducti v e caste (i.e., queens) pro2009), is performed when the or g anism is lik ely to die of
duce of fspring and members of the non-reproducti v e castenatural age-related causes and thus is more e xpendable. In
care for the brood and perform other duti es central to the this w ay , the colon y optimizes the use of its w ork ers. (T ofilmaintenance of the eusocial colon y (Jandt and Dornhaus, ski, 2002). In contrast, the for a ging for workh ypothesis
2009). Moreo v er , man y eusocial or g anisms, such as leafassumes that as or g anisms are born the y perform tasks closcutter ants (W ilson, 1980), b umblebees (Jandt and Dorn- est to them and proceed to perform tasks further from the
haus, 2009), and aphids (Pik e and F oster , 2008), also e x-center of the nest (Franks et al., 1997; H ¨olldobler and W ilhibit task-r elated division of labor
, where indi viduals speson, 2009; Sendo v a-Franks and Franks, 1993; T ofts, 1993).
cialize on performing a particular task.F or e xample, nonThis e xplanation depends only upon or g anisms’ reacti v e rereproducti v e w ork er b umblebees specialize to perform roles
sponses to task stimuli. Thus, according to the foraging
© 2012 Massachusetts Institute of Technology
Artificial Life 13: 178…
The Evolution of Temporal Polyethism
for w ork h ypothesis, colonies e xhibit a temporal polyethism2007). Digital or g anisms ha v e rapid generation times (e.g.,
pattern as a result of the spatial or g anization of the colon y’thousands
s
of generations in a fe w hours), thus enabling us to
nest without an y inherent e v olutionary adv antage related to
study this comple x e v olutionary phenomenon.
the riskiness of an y task.
In this paper , we use A vida to e xplore whether v arying the
amount
of risk associated with tasks is suf ficient to e v olv e
Studies ha v e produced e vidence in support of both h ycolonies that e xhibit a temporal polyethism structure.
We
potheses (Franks et al., 1997; H ¨olldobler and W ilson, 2009;
created a w orld in which dif ferent tasks were associated with
Robson and Beshers, 1997; T raniello and Rosengaus, 1997).
Specifically , studies with monomorphic ants pro vide sup- dif ferent le v els of risk. W e used colonies of clonal (i.e., geport for the foraging for w ork h ypothesis by presenting e v- netically identical) or g anisms, where the colonies competed
idence that the task riskiness h ypothesis is too rigid to ac- for limited space in the A vida w orld. Each colon y w as recount for the unstable situation of ants and an y correlation quired to perform each type of task a certain number of times
for the colon y to replicate. An ancestor or g anism performed
of age and task is merely a byproduct (Sendo v a-Franks and
Franks, 1993). In the original foraging for w ork mathemat- each of the required tasks once. W e e xplicitly remo v ed an y
ical model created by T ofts, ants change tasks when w ork spatial component to task performance to determine whether
or g anisms were responding to the spatial structure of the
w as una v ailable at the current location (T ofts, 1993). In one
study , marking the ants sho wed that older ants were fle xi- nest, or the risk associated with tasks. In response to these
ble in the tasks the y performed, and all ants, re g ardless of pressures, the or g anisms e v olv ed di vision of labor strate gies
in which tasks associated with less risk were done earlier in
age, foraged for w ork, meaning that the y acti v ely sought out
an or g anisms life and riskier tasks were performed later in
tasks to perform (Sendo v a-Franks and Franks, 1993). Ho wlife, re g ardless of the initial order of the tasks. These data
e v er , critiques of T ofts’ model of foraging for w ork highlight
pro vide support for the h ypothesis that risks associated with
that the w ay in which w ork ers can mo v e between tasks creates a biologically unrealistic colon y (Robson and Beshers, aging and v arious tasks are suf ficient to produce temporal
polyethism.
1997). Others ha v e noted that T ofts’ model does not account
for man y other eusocial insects, such as termites, that ha v e
Methods
a well-de v eloped age-based di vision of labor strate gy that is
not a byproduct of foraging for w ork (T raniello and Rosen- T o use A vida to study the e v olution of temporal polyethism,
g aus, 1997). In addition, an alternati v e mathematical model
we created a w orld consisting of competing colonies that
testing the task-riskiness h ypothesis w as created with a seteach contain a set of clonal or g anisms. Each of digital or g anof tw o tasks that each had a dif ferent mortality rate (T ofil- isms has a virtual CPU, a genome (a circular list of computer
ski, 2002). This model sho ws that the longe vity of w ork ersinstructions), and a location within the colon y . The virtual
in a colon y that perform tasks without re g ard to the amountCPU of an or g anism consists of three general-purpose re gisof risk associated with them is significantly lo wer than the ters and tw o stacks. Each digital or g anism e x ecutes instruclonge vity of w ork ers a colon y that perform tasks in order oftions on its virtual CPU. The instruction set in A vida allo ws
risk (T ofilski, 2002).
for basic computational tasks, such as addition, multiplicaWhile these studies ha v e e xamined potential proximate tion, and bit-shifts, controlling the e x ecution flo w , and selfcauses of temporal polyethism e xhibited by current eusocialreplication. An or g anism performs logic operations
NOT,
(
colonies, it is challenging to e xplore the e v olutionary con- NAND, etc.) called tasks by e x ecuting the instructions in
ditions that may gi v e ri se to this pattern. Both field obser - their genome.
v ations and e xperimental studies of e v olution in lineages of F or a colon y to replicate, the or g anisms within that colon y
actual or g anisms are infeasible because of long generationmust perform each type of task in a set a certain number of
times and the comple xity of studying lar ge social groups in times. F or e xample, in our initial e xperiments, a colon y had
a controlled w ay .
to perform taskNOT 250 times and taskNAND 250 times.
T o address these challenges, we use A vida, a digital e v Ao-natural analog is a colon y of eusocial insects in which the
lution softw are platform that maintains a population of self- w ork ers must both forage for food and tend to the brood.
replicating computer programs in a user -defined en viron- In addition, because each colon y starts with only one or ment (Ofria and W ilk e, 2004). Each computer program is a g anism, or g anisms must also replicate to produce other or g anisms that can assist them in the performance of tasks to
digital or g anism that e x ecutes its genome (a list of computer
v e the o v erall colon y objecti v e. During colon y replicainstructions) to perform tasks, where the tasks enable the or achie
g anism to collect resources and thus compete with its neigh-tion, the genome of the colon y is potentially mutated (i.e.,
bors. A vida meets all of the requirements for e v olution: instructions are potentially ins erted, remo v ed, or e xchanged
for other instructions). This ne w genome is used to seed
replication, v ariation, and dif ferential selection.
A vida has
a daughter colon y , which is selected randomly from the
pre viously been used to study topics such as di vision of labor
(Goldsby et al., 2012), origin of comple x features (Lenski colon y population.
et al., 2003), and e v olution of cooperation (Knoester et al., T o address our central question re g arding the e v olution of
179
Artificial Life 13
The Evolution of Temporal Polyethism
T ask
Risk T reatments
temporal polyethism, we added the capability for each task
NOT risk y NAND risk y No risk Both risk y
to be associated with lethality
a
risk that specifies the probNOT
25%
0%
0%
25%
ability of the or g anism dying before completing the task.
0%
25%
0%
25%
Non-risk y (or safe) tasks ha v e a lethality risk of 0. Our most NAND
risk y tasks ha v e a lethality risk of 25%.
If an or g anism is
T able 1: The four risk treatments for a tw o-task en vironkilled while performing a task, then the task is not completed
ment. The ro ws describe the lethality risks associated with
and thus does not count to w ard the task count of the colon y .
tasksNOT and NAND. (E.g., A 25% risk means that while
In most other A vida e xperiments,or g anisms are reset
performing the task, the or g anism has a 25% chance of dyupon producing an of fspring, in order to emulate the beha ving.) The columns describe a specific treatment.
ior of bacteria that di vide into tw o daughter cells when the y
replicate. Ho we v er , since age and internal state play a k e y
role in these e xperiments, we modified the or g anisms so that
atomic units within this Figure to denote order , to actually
the y do not reset after replication, b ut rather just continue perform a task an or g anism must e x ecute se v eral instrucrunning.
tions. By v arying the ancestor or g anism, we are able to v er At the outset of these e xperiments, we seed the colonies ify that an y patterns of temporal polyethism result from the
with an ancestor or g anism that performs all the types of
riskiness associated with the tasks, not the initial genomic
tasks necessary for completion of the colon y task.
In our
structure of the or g anisms. F or each ancestor , we performed
e xperiment, an ancestor or g anism performsNOT
task and
all four risk treatments. If task riskiness is a suf ficient prestaskNAND once. Because each colon y contai ns only one in-sure to result in temporal polyethism, then we should see
di vidual at the onset of the e xperiment and also after colon that
y or g anisms e v olv e to perform the less risk y task first and
replication, or g anisms must self replicate to fill the colon y .the more risk y task second, re g ardless of whether
NOT or
Each e xperiment comprises se v eral dif ferent treatments that
NAND is the risk y task, and the initial order of the tasks with
randomize the order in which the tasks appear in the ances- the ancestor or g anism’ s genome.
tor or g anisms’ genomes, as well as the riskiness associated
with the tasks.
NOT−NAND
NAND−NOT
ancestor
ancestor blah
The starting w orld for each e xperiment had 400 colonies
each of which contained one ancestor or g anism. Or g anisms
were subject to three mutation rates during colon y reproducNOT
NAND
tion: a cop y mutation rate of 0.0075 (0.0003 per instruction),
an insertion mutation rate of 0.05 (0.002 per replication),
and a deletion mutation rate of 0.05 (0.002 per replication).
NAND
NOT
F or each e xperiment, we conducted 30 trials to account for
the stochastic nature of e v olution. Each trial ran for 100,000
updates, where an
updateis the amount of time it tak e an a vreplication
replication
erage or g anism to e x ecute
cycles
30 – each ins truction tak es
one c ycle to e x ecute.
Figure 1: The layout of the ancestor or g anisms for tw o-task
temporal polyethism e xperiments.
The NOT-NAND ancestor performs taskNOT, performs taskNAND, and then repliNAND, per The primary topic of this study is whether the risks associ- cates. TheNAND-NOT ancestor performs task
taskNOT, and then replicates. Because the genomes
ated with aging and tasks are suf ficient to e v olv e coloniesforms
of
or g anisms that e xhibit temporal polyethism. F or our study are
, circular , after each or g anism replicates, it resumes e x ewe created a tw o-task en vironment in which colonies had cution at the top of its genome.
to perform taskNOT 250 times and taskNAND 250 times
in order for the colon y to replicate.W e created four risk
Figures 2 and 3 depict the results of the e xperimental
treatments (described in T able 1) that v ary the lethality riskstreatments. F or all results, the mean age at which a task is
associated with the tasks.Specifically , the treatments are: performed includes the age of or g anisms who died attemptNAND is risk y , (3) neither task ing to perform that task. Figure 2 depicts the treatments in
(1) taskNOT is risk y , (2) task
NOT and taskNAND
is risk y (a control), and (4) both task
which taskNOT is risk y . In both treatments that v ary the anNOT is performed
are risk y (a control).
cestor or g anism, the mean age at which
NAND
Additionally , we created tw o possible ancestor or g anisms
is significantly greater than the mean age at which
(depicted in Figure 1).Each ancestor completes each task is performed (Mann-Whitne y U T est). F or e xample, for the
NOT-NAND
NOT-NAND ancestor NOT
once and then self-replicates. Ho we v er , ancestor
,
is performed at the mean age of
performs theNOT task first and ancestorNAND-NOT per 750.37± 27.45 c ycles andNAND is performed at the mean
forms the NAND task first. While we depict the tasks as
age of 453.43
± 29.12c ycles. The treatment seeded with the
Results
180
Artificial Life 13
The Evolution of Temporal Polyethism
were performed in 26 out of 30 replicates. Additionally ,
NAND-NOT ances23 out of 30 replicates seeded with the
tor performed the riskier taskNOT at a later age than task
NAND.
Figure 3 depicts the treatments where task NAND is
NAND
risk y .F or both treatments, the mean age at which
is performed is significantly greater than the mean age at
which NOT is performed (Mann-Whitne y U test).27 out
of 30 replicates with theNOT-NAND ancestor and 28 out of
30 replicates with theNAND-NOT ancestor performed the
NOT. These treatriskier taskNAND at a later age than task
ments support our h ypothesis that task riskiness can result
in temporal polyethism in which the more risk y task is per formed later in the lifetime of the or g anisms.
1000
800
600
400
A
ge
(in
cy
cl
es
)
NOT-NAND ancestor re v ersed the order in which the tasks
200
0
0
NOT (0%)
NAND (25%)
2
4
6
Time (in updates)
8
10
x 10
4
NAND is risk y
(a) Ancestor:NOT-NAND; T reatment:
1000
800
1000
600
800
400
A
ge
(in
cy
cl
es
)
600
200
NOT (0%)
NAND (25%)
A
ge
(in
cy
cl
es
)
400
200
0
0
0
0
NOT (25%)
NAND (0%)
2
4
6
Time (in updates)
8
10
x 10
800
600
4
6
Time (in updates)
8
10
x 10
4
NAND is risk y
(b) Ancestor:NAND-NOT; T reatment:
4
NOT is risk y
(a) Ancestor:NOT-NAND; T reatment:
1000
2
Figure 3: T ask ordering o v er time in treatments where task
NAND is risk y compared across dif ferent ancestors. F or each
plot, the x-axis is e v olutionary time and the y-axis is the
mean age in c ycles when the associated task is performed.
Dotted lines represent standard errorT .askNAND is consistently performed later in the lifetime of the or g anisms,
re g ardless of the starting order .
A
ge
(in
cy
cl
es
)
400
formed earlier or later in the or g anisms’ lifetimes. Figure 4
depicts the results of the control treatments in which neither
task is risk y . F or these control treatments, the a v erage age
0
0
2
4
6
8
10
at which or g anisms perform tasks increases o v er the dura4
Time (in updates)
x 10
tion of the e xperiment. This change results from indi vidual
NOT is risk y
(b) Ancestor:NAND-NOT; T reatment:
or g anisms e v olving to perform the same task multi ple times
within their lifetime resulting in the a v erage age of task per Figure 2: T ask ordering o v er time in treatments where taskformance increasing. Ho we v er , the mean age at which task
NOT is risk y compared across dif ferent ancestors. F or eachNOT is performed is not significantly dif ferent than the mean
age at which task NAND is performed (Mann-Whitne y U
plot, the x-axis is e v olutionary time and the y-axis is the
mean age in c ycles when the associated task is performed. T est). Figure 5 depicts the results of the control treatments
in which both tasks are risk y . F or both treatments, the mean
Dotted lines represent standard error
T ask
. NOT is consistently performed later in the lifetime of the or g anisms, re- age at which the or g anisms perform the tasks reflects their
g ardless of the starting order .
order in the genome.One thing to note about this control
is that the high le v el of risk associated with both tasks deFigures 4 and 5 depict the results of our controls, which creases the rate of colon y replication. In f act, man y colonies
are designed to v erify that, gi v en the same le v el of risk, there
lost the ability to replicate altogether and survi v ed merely
is nothing inherent in the tasks that results in one being per -because other colonies within their trial were also unable
200
181
NOT (25%)
NAND (0%)
Artificial Life 13
The Evolution of Temporal Polyethism
1000
800
600
400
1000
A
ge
(in
cy
cl
es
)
to replicate. Thus, these colonies are not actually e v olving
in an adapti v e f ashion.
Ho we v er , the data pro vided by the
NOT
controls indicate that there is nothing inherent in the
or NAND tasks that implies an ordering. T ak en together ,
these treatments indicate that more risk y tasks are, on a verage, performed later within the lifetime of the or g anisms.
800
0
0
200
2
600
8
10
x 10
4
A
ge
(in
cy
cl
es
)
1000
200
NOT (0%)
NAND (0%)
2
4
6
Time (in updates)
8
800
10
x 10
4
600
400
1000
A
ge
(in
cy
cl
es
)
(a) Ancestor:NOT-NAND; T reatment: No risk
800
0
0
200
600
2
NOT (25%)
NAND (25%)
4
6
Time (in updates)
8
10
x 10
4
(b) Ancestor:NAND-NOT; T reatment: All risk y
A
ge
(in
cy
cl
es
)
400
200
0
0
4
6
Time (in updates)
(a) Ancestor:NOT-NAND; T reatment: All risk y
400
0
0
NOT (25%)
NAND (25%)
NOT (0%)
NAND (0%)
2
4
6
Time (in updates)
8
10
x 10
4
(b) Ancestor:NAND-NOT; T reatment: No risk
Figure 5: T ask ordering o v er time in control treatments
where both tasks are risk y . F or each plot, the x-axis is e v olutionary time and the y-axis is the mean age in c ycles when
the associated task is performed. Dotted lines represent standard error . In these results, the controls indicate that there is
nothing intrinsic about the tasks that is dri ving the temporal
polyethism results.
Figure 4: T ask ordering o v er time in control treatments
where neither task is risk y . F or each plot, the x-axis is e v oNAND-NOT maintained the ordering
lutionary time and the y-axis is the mean age in c ycles whenthe ancestral or g anism
NOT later in
present
in
the
ancestor
genome and performed
the associated task is performed. Dotted lines represent stanlife.
Ho
we
v
er
,
these
data
also
re
v
eal
that
at lo wer risk le v els,
dard error . In these results, the controls indicate that there is
fe
wer
replicates
were
able
to
e
v
olv
e
the
temporal
polyethism
nothing intr insic about the tasks that is dri ving the temporal
pattern
if
the
ancestral
or
g
anism
started
with
the
riskier
task
polyethism results.
being done earlier in life. F or e xample, fe wer replicates with
NOT-NAND were able to rearrange
T o better understand ho w the colonies were re sponding the ancestral or g anism
their
genomes
such
that
the risk y NOT
task w as done later in
to the amount of risk associated with a task, we performed
life
when
the
lethality
risk
w
as
lo
wer
. These results indicate
se v eral additional treatments in which we set the lethality
that
the
le
v
el
of
risk
plays
an
important
role in the e v olution
risk for the risk y task to 7%, 15%, and 20%. F or these ne w
of
temporal
polyethism.
risk conditions, we again v aried the ancestor and also which
task w as risk y . Figure 6 sho ws the number of replicates out
Analyses
of 30 that e v olv ed a temporal polyethism pattern, where the
more risk y task w as performed later in life. F or all risk le v-W e ha v e demonstrated that colonies e v olv e to perform more
els, if the ancestor or g anism had properly ordered the tasksrisk y tasks, on a v erage, later within their lifetime than safe
(i.e., it performed the risk y task last), then most replicates tasks. Ne xt, we e xamine ho w this beha vior interacts with
were able to maintain the temporal polyethism pattern. F or reproduction and then conduct a case study analysis of a
NOT is the risk y task, most replicates with
e xample, when
colon y that e xhibits this beha vior .
182
Artificial Life 13
The Evolution of Temporal Polyethism
26!
!
25!
1000
27! 26! 26!
23!
22!
20!
7%!
15!
600
15%!
12!
20%!
6!
25%!
R
ep
lic
at
es
ou
t
of
30
10!
800
5!
400
A
ge
(in
cy
cl
es
)
30!
NOT (25%)
NAND (0%)
Replication
200
0!
not-nand!
0
0
nand-not!
NOT is risk y
(a) T reatment:
!
30!
!
25!
25! 26! 24!
28!
27!
25!
20!
7%!
15!
15%!
10!
6!
8!
25%!
R
ep
lic
at
es
ou
t
of
30
5!
20%!
2
4
6
Time (in updates)
8
10
4
x 10
Figure 7: These results depict the mean age at which task
NOT (blue line with circles), taskNAND (red line with triangles) and replication (black line with stars) are performed
NOT is risk y and the runs
for the case study treat ment where
were started with theNOT-NAND ancestor .These results
suggest that the or g anisms are performing NAND
task one
NOT.
or more times, replicating, and then performing task
0!
NOT-NAND ancestor and in which
ment that be gins with the
task NOT is risk y to ascertain ho w it managed task per NAND is risk y
(b) T reatment:
formance and replication (results depicted in Figure 2a).
The or g anisms within this colon y e x ecuted a precise beha vFigure 6: The results of the temporal polyethism treatments, ioral plan that is depicted in the phenotype portion of Figwhere risk le v el w as v aried. The y-axis of both plots is theure 8. The y performed task
NAND, replicated, performed
number of replicates out of 30 that were able to do the risk ytask NAND ag ain, replicated ag ain, and then repeatedly per task later in life. The x-axis sho ws the results from tw o dif- formed taskNOT (the risk y task) until it killed them.The
NOT-NAND and NAND-NOT. (a) sho ws referent ancestors:
or g anisms in this case study clearly e xhibit the temporal
NAND does not
sults from whenNOT is the risk y task and
polyethism pattern of performing the risk y task after their
NAND is the
ha v e an y risk.
(b) sho ws results from when
other duties had been completed.
NOT does not ha v e an y risk. The k e y denotes
risk y task and
phenotype
the lethality risk for the risk y task.
genotype
not-nand!
nand-not!
NAND
replication
TaskPerformanceandReplication. W ithin these e xper 1 4 7
NOT
8...
iments, or g anisms ha v e a pressure not just to perform tasks,
NAND
6
3
b ut also to replicat e and produce clones capable of performreplication
NAND
ing these same tasks.One topic we were interested in e x2 5
NOT
ploring is when the or g anisms replicated.
T o address this
replication
topic, we e xamined a case study treatment from our original
NOT
NOT-NAND
tw o-task e xperiment that be gins with
the
ancesNOT
NOT is risk y . Figure 7 depicts the mean
tor and in which task
age at which the tasks were performed and at which the or - Figure 8: Diagrams of the phenotype (left) and genotype
g anisms replicated.Intriguingly , the or g anisms performed (right) of a case study or g anism whose colon y e xhibited
the less risk y taskNAND
(
), replicated, and then much later
temporal polyethism with tw o tasks. The numbered arro ws
NOT( ). In this e xin their life performed the more risk y task
surrounding the genotype indicate the order in which inample, this result suggests that the or g anisms ha v e e v olv
ed
structions
were e x ecuted to produce the phenotype. In this
a strate gy that balances their need to perform tasks, the riskcase, the genotype is v ery similar to NOT-NAND
the
ancesassociated with these tasks, and their need to replicate.
tor . The risk-based order in which the tasks were performed
depended upon control-flo w instructions in the genome.
Two-Task Colony Case Study. Ne xt, we e xamined the
beha vior of a successful colon y from our tw o-task e xperi-
183
A second topic we e xplored w as ho w the genome archi-
Artificial Life 13
The Evolution of Temporal Polyethism
NOT
NAND
tecture of this case study supported this beha vior . F or e xam- Measurement
Mean Age
1103.78± 25.93 236.43± 5.69
ple, or g anisms may ha v e rearranged their genome to support
Mean First Age
964± 0
232.90± 4.28
task ordering (i.e., by mo ving the instructions that performed
more risk y task to the end of their genome) or or g anisms Mean Age No Lethality 1515.02± 58.71 215.89± 9.02
may ha v e e v olv ed to use control-flo w instructions that enT able 2: Three dif ferent measurements of the age at which
able them to skip o v er portions of their genome. In this case,
or g anisms perform a task. While all three ha v e similar rethe or g anisms e v olv ed to use the control-flo w instructions.
sults for the non-risk y taskNAND
(
), the results dif fer a bit
The architecture of the genome, which is depicted in the
NOT
more
for
the
risk
y
task
(
).
Ho
we
v er , all three measuregenotype portion of Figure 8, is e xtremely similar to the anments
report
a
highly
significant
and
substantial dif ference
NOT is encoded first, then task
NAND,
cestor or g anism: task
in
mean
ages
between
the
tw
o
tasks
and thus capture the
and lastly repl ication.Ho we v er , the or g anisms e v olv ed to
temporal
polyethism
structure.
NOT until the reha v e both jump instructions (to skip task
mainder of the genome had been e x ecuted twice) and a loop
to continue to perform tasNOT
k until death. Or g anis ms set to perfor ming the more risk y task at the end of their life.
and used the v alue of a re gister that w as preserv ed duringThis strate gy balances a colon y’ s need to maintain members
replication to track which genome iteration the y were on andof the colon y and also to complete risk y tasks.
As such,
to modify their beha vior accordingly . The numbered arro wsthis temporal polyethism structure enables the colon y to be
in Figure 8 depict the order in which the elements of the
more ef ficient at g athering resources by ha ving older or g angenome were e x ecuted.
isms complete riskier tasks when the y are closer to dying.
In our analyses, we found further e vidence that or g anisms
Measuring Temporal Polyethism. There are tw o chalmade use of control flo w instructions and genomic architeclenges associ atedwith measuring temporal polyethism:
ture modifications to achie v e this beha vior .
First, each or g anism may perform each task multiple times
While our study sheds light on the e v olutionary pressures
o v er its lifetime.Second, an or g anism may die while per that can gi v e rise to a temporal polyethism pattern, the proxforming a task as either the consequence of the lethality risk
imate mechanisms emplo yed by colonies to e xhibit this patassociated with that task or as the result of being replicated
tern could rely on either spatial structure (as proposed by the
o v er by a neighboring or g anism . Thus f ar , to measure temforaging for w ork h ypothesis) or de v elopmental hormones
poral polyethism, we ha v e e xamined the mean age at which
re gulated by aging (as proposed by the task-riskiness h yor g anisms perform a task. Here we assess this measurement
pothesis). F or e xample, since the spatial structure of the nest
by comparing it to tw o other potential measurements:
(1)
corresponds with the riskiness of tasks, or g anisms may emthe mean age at which the or g anisms
fir stperform a task,
plo y a foraging for w ork mechanism to achie v e this pattern.
and (2) the mean age at which the or g anism s perform a task
Thus, w ork ers may start within the nest taking care of the
when all lethality risks are remo v ed from the system.
brood and then progress outw ard to more risk y tasks, such as
F or this analysis, we used the case study colon y whose
guard, undertak er , or forager (H ¨olldobler and W ilson, 2009).
genotype and phenotype are depicted in FigureThe
8. reEv en within T ofts’ foraging for w ork model, w ork ers switch
sults of the three measurements are sho wn in T able
All 2.
between tasks based on colon y need, and riskier tasks on the
three measurements pro vide similar results for the age of
outside of the nest are a constant dra w for w ork, trapping
the non-risk y task NAND
(
). The results v ary for the risk y
older w ork ers outside of the nest (T ofts, 1993; Robson and
NOT (964) is
task. Specifically , the mean first age for task
Beshers, 1997).
substantially less than the mean age (1103.78), which, in
T ask switching may also be re gulated by age using a v aturn, is substantially less than the mean age without lethalriety of de v elopmental hormones. Juv enile hormone (JH) is
ity (1515.02). Ho we v er , all three measurements capture the
considered a mediator for temporal polyethism in adv anced
NAND is per temporal polyethism structure in which task
eusocial insects and e v en in some primiti v e w asps (Robinformed much earlier than taskNOT within an or g anism’ s
son, 1987; Shorter and T ibbetts, 2009; Sulli v an et al., 2000).
lifetime.
Studies of hone ybees and some species of w asps sho w that
when w ork ers were treated with JH, the y transitioned from
Discussion
nursing to foraging earlier in life (Robinson, 1987; Shorter
In this paper , we ha v e described ho w we ha v e used A vida
andtoT ibbetts, 2009; Sulli v an et al., 2000). In particular , hone xplore a set of e v olutionary conditions that gi v e rise to teme ybees ha v e higher concentration of JH when the y are older
poral polyethism, a di vision of labor pattern.
Specifically ,
and foraging than the y do when the y are younger and taking
we found that assigning dif ferent lethality risks to v arious care of the brood (Shorter and T ibbetts, 2009).
Knocking
types of tasks w as a suf ficient pressure to produce a tem- do wn vitellogenin, a gene associated with JH, in bees simiporal polyethism pattern, where or g anisms performed the larly results in earlier task switching to foraging and shorter
least risk y task earlier in their lifetime and then switched
lifespans (Nelson et al., 2007). This e xample highlights
184
Artificial Life 13
The Evolution of Temporal Polyethism
ho w de v elopmental genes can re gulate the performance of
Lenski, R. E., Ofria, C., Pennock, R. T ., and Adami, C. ( 2003). The
e v olutionary origin of comple x featureNatur
s. e
, 423:139–
risk y tasks so that the y are done later in life and increase
w ork er bee longe vity . This proximate mechanism is compat- 144.
ible with the e v olutionary pressures associated with ordering
Nelson, C., Ihle, K., F ondrk, M., P age, R., and Amdam, G. (2007).
tasks according to risk.
The gene vitellogenin has multiple coordinating ef fects on
social or g anization.
PLoS biolo gy
, 5(3):e62.
An additional pressure that may reinforce ordering the
performance of tasks according to risk is the benefit of con- Ofria, C. and W ilk e, C. O. (2004). A vida: A softw are platform for
serving viable reproducti v es within the colonInyspecies
.
research in computational e v olutionary biology
J ournal
.
of
Artificial Life, 10:191™.
in which w ork ers ha v e the option of reproducing when the
queen dies, younger w ork ers may ha v e viable e ggs and
Pik e, N. and F oster , W . A. (2008).
Ecolo gy of Social Evolution
.
higher reproducti v e success than older sisters.
By ha vSpringer Berlin Heidelber g.
ing younger w ork ers perform safer tasks within the nest,
Curr. ent
the colon y as a whole preserv es its reproducti v e potential Queller , D. C. and Strassmann, J. E. (2003). Eusociality
Biolo gy, 13(22):R8613.
(Sendo v a-Franks and Franks, 1993).
W ithin this study , we ha v e demonstrated that associating
Robinson, G. (1987). Re gulation of hone y-bee a ge polyethism
by juv enile-hormone.
Behavior al Ecolo gy and Sociobiology
,
tasks with lethality risks is suf ficient for e v olving a temporal
20(5):329à.
polyethism pattern. In the future, we will e xplore the ef fect
of adding additional tasks and le v els of risk. In additi on, weRobson, S. K. and Beshers, S. N. (1997).
Di vision of labour and
will add in task-switching costs to address a limitation of
‘foraging for w ork’: simulating reality v ersus the reality of
simulations.Animal Behaviour
, 53(1):214•.
T ofts’ model, which assumes (unrealistically) that w ork ers
can switch between tasks without an y delays. The e v olutionSeele y , T . D. (1982). Adapti v e significance of the age polyethism
ary conditions leading to the rise of temporal polyethism is
schedule in hone ybee colonies.
Behavior al Ecolo gy and Soan important step i n understanding the di vision of labor patciobiolo gy
, 11(4):287Ë.
terns we see in eusocial insects.
Sendo v a-Franks, A. and Franks, N. R. (1993).
T ask allocation in
ant colonies within v ariable en vironments (a study of temAcknowledgements
poral polyethism: e xperimental).Bulletin of Mathematical
Biolo gy, 55(1):75Î.
This w ork has been supported in part by NSF grants CCF-
0643952, DBI- 0939454, CCF-0820220, OCI-1122620,
DGE-0718124.
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