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ORIGINAL ARTICLE
Decreasing worker size diversity does not affect colony performance
during laboratory challenges in the ant Temnothorax nylanderi
T. Colin
1
&C. Doums
2,3
&R. Péronnet
1
&M. Molet
1
Received: 10 February 2017 /Revised: 25 April 2017 /Accepted: 2 May 2017
#Springer-Verlag Berlin Heidelberg 2017
Abstract
Within-colony phenotypic diversity can play an essential role
in some eusocial insect taxa by increasing the performance of
division of labor, thereby increasing colony fitness. Empirical
studies of the effect of phenotypic diversity on colony fitness
mostly focused on species with discrete castes (workers, sol-
diers) or with continuously and highly morphologically vari-
able workers, which is not the most common case. Indeed,
most species exhibit continuous but limited worker morpho-
logical variation. It is still unclear whether this variation im-
pacts colony fitness. To test this, we reduced the worker size
diversity in 25 colonies of the ant Temnothorax nylanderi and
compared their performances to 25 control colonies. We
reared these colonies in the laboratory and measured the effect
of treatment (reduced diversity or control) and colony size
(number of workers) on colony performance at six challenges,
as well as on worker mortality and brood production. The
reduction of worker size diversity did not affect colony per-
formance nor mortality and brood production. As expected,
colony performance and brood production increased with col-
ony size. These results suggest that worker size diversity may
not be under positive selection in this species, but rather the
product of a lack of developmental canalization. We propose
that social life could decrease the selective pressures maintain-
ing developmental canalization, subsequently leading to
higher size diversity without necessarily increasing colony
performance.
Significance statement
In social insects, nestmate size diversity is commonly thought
to improve division of labour and colony performance. This
has been clearly demonstrated in species with high size diver-
sity, either discrete or continuous, but this is unclear in most of
the social insects that exhibit low size diversity. We experi-
mentally decreased worker size diversity in the ant
Temnothorax nylanderi, a species with low worker size diver-
sity. Reducing worker size diversity had no effect on colony
performance, worker mortality, or brood production. Our find-
ings support the hypothesis that low size diversity is merely
the product of developmental noise and is not necessarily
adaptive. We propose that social life could relax the selective
pressures maintaining developmental and social canalizations,
subsequently leading to size diversity.
Keywords Canalization .Division of labor .Fitness .
Phenotypic plasticity .Size variation
Introduction
Phenotypic diversity, whether environmentally or genetically
determined, plays a central role in the ecology and evolution
of organisms. At the population scale, phenotypic diversity
decreases intraspecific competition for food (Bolnick et al.
Communicated by W. Hughes
Electronic supplementary material The online version of this article
(doi:10.1007/s00265-017-2322-4) contains supplementary material,
which is available to authorized users.
*M. Molet
mathieu.molet@upmc.fr
1
Institute of Ecology and Environmental Sciences of Paris UMR7618,
UPMC Univ Paris 06, CNRS, Sorbonne Universités,
7 quai St Bernard, 75252 Paris, France
2
Institut de Systématique, Évolution, Biodiversité (ISYEB), EPHE,
CNRS, UPMC Univ Paris 06, MNHN, Sorbonne Universités,
45 rue Buffon, CP 39, 75005 Paris, France
3
EPHE, PSL Research University, 75005 Paris, France
Behav Ecol Sociobiol (2017) 71:92
DOI 10.1007/s00265-017-2322-4
2011). At the individual scale, phenotypically differentiated
cells facilitate simultaneous processes, such as digestion, res-
piration, and movement and can improve the efficiency of the
organism (Ispolatov et al. 2012). Similarly, within a social
group, inter-individual diversity may improve division of la-
bor among group members and enhance group efficiency
(Pruitt and Riechert 2011). In eusocial insects such as ants,
bees, wasps,and termites, phenotypic diversity among colony
members is often associated with a strong division of labor.
This division of labor often relies on morphological differ-
ences and is thought to be one of the keys to the ecological
success of social insects (Wilson 1987). For example in ants,
queens are large females that specialize in reproduction with
developed ovaries and in dispersal with wings, while workers
are smaller females that take care of non-reproductive tasks.
Workers are cheaper to produce because they are small, they
lack wings, and in some species they also lack ovaries (Peeters
1997). These two phenotypes are examples of distinct
Bcastes^as they exhibit discrete morphological differences
that are generated by distinct growth rules during develop-
ment. They are generally the product of phenotypic plasticity
(e.g., Sumner et al. 2006;Huntetal.2011;Linksvayeretal.
2011; but see Schwander et al. 2010).
Non-reproductive individuals within a colony can also be
highly diversified in terms of body size and morphology.
Morphological variation is often associated with behavioral
specialization. This has been shown in species where workers
are highly variable morphologically or where a discrete sol-
dier caste exists such as harvester ants (Wilson 1984;Arnan
et al. 2011), turtle ants (Powell 2009), and leaf-cutter ants
(Evison et al. 2008) among others (e.g., Porter and Tschinkel
1986; Foster 1990;Hasegawa1993a,b; Passera et al. 1996;
Harvey et al. 2000; Perry et al. 2004; Tóth and Duffy 2008;
Grüter et al. 2012). However, Fjerdingstad and Crozier (2006)
highlighted the fact that worker size diversity is limited in the
majority of ant species, including some of the most successful
species. Of the 35 species that they studied, the majority of the
body weight coefficient of variations of workers was lower
than 0.2 (the coefficient of variation (CV) is a measure of
variance that is independent of absolute size and is computed
as the ratio between standard deviation and mean (Sokal and
Rohlf 1970)). Very few studies investigated the potential ben-
efits of having limited morphological diversity among
workers and showed contrasted results. A positive effect of
diversity was mainly observed in polyandrous and/or polygy-
nous species for which morphological diversity can be asso-
ciated with genetic diversity given that worker size has often
been found to be heritable (Hughes et al. 2003; Rheindt et al.
2005; Schwander et al. 2005; Jaffé et al. 2007;Evisonand
Hughes 2011; Huang et al. 2013; Jandt and Dornhaus 2014;
Table 1).
Focusing our attention on species with low level of mor-
phological diversity could improve our understanding of how
diversity evolved. As described above, a common thought is
that selective pressures could favor an increase in morpholog-
ical diversity through a better colony-level efficiency and
could subsequently lead to the evolution of worker subcastes
even in species with low worker size diversity. Alternatively,
size diversity could primarily evolve through relaxed selective
pressures on worker size provided by social life. Relaxing
selective pressures is known to decrease developmental cana-
lization (the developmental processes that keep the phenotype
constant in spite of genetic or environmental variation, see
Debat and David 2001) and could hence increase worker size
diversity (Hunt et al. 2011). In ants, worker size diversity
could result from the active process of workers providing dif-
ferent environmental conditions to larvae and/or from devel-
opmental response of larvae to external environmental factors
as observed in the ant Messor pergandei where larvae develop
into workers of different sizes depending on the season
(Rissing 1987). Whatever the mechanisms at the origin of
worker size diversity, the first hypothesis (directional selec-
tion) predicts that worker size diversity should provide bene-
fits to the colony even in species with low worker size diver-
sity, whereas the second hypothesis (relaxed selection) does
not.
In this study, we tested whether size diversity affects colo-
ny fitness in the ant Temnothorax nylanderi, a species
exhibiting continuous but limited worker size diversity. This
species is widely distributed in Western Europe (Pusch et al.
2006), including urban areas, and is also easy to find, to iden-
tify, and to rear. It is mainly monogynous (Buschinger 1968;
Foitzik and Heinze 2000) and monoandrous (Foitzik et al.
1997; Foitzik and Heinze 2000). Most of worker size diversity
in this species should therefore result from phenotypic plas-
ticity. To study the effects of continuous diversity on colony
fitness and efficiency for particular tasks, researchers often
focused on the function of larger and smaller workers in the
colonies without manipulating worker diversity (e.g., Goulson
et al. 2002; Spaethe and Weidenmüller 2002;Peatetal.2005;
Couvillon and Dornhaus 2010; Westling et al. 2014). In order
to test whether colony fitness is affected by colony-level
worker size diversity, including the colony-level emerging
properties of worker size diversity and not only the functions
of large and small workers, we manipulated colonies to reduce
worker size diversity in test colonies while natural diversity
was retained in control colonies. Colony fitness was indirectly
assessed by challenging colonies with various tasks to per-
form, covering a wide range of usual colony activities such
as emigration, solid and liquid food collection, nest construc-
tion, and corpse removal. These colony-level tasks were cho-
sen because they are likely to rely on worker size diversity as
they classically involve large and small workers in other spe-
cies. The ability to transport load was indirectly assessed
through the foraging and nest construction tasks, a trait linked
with worker size in ants (Kaspari 1996). The ability to defend
92 Page 2 of 11 Behav Ecol Sociobiol (2017) 71:92
the nest and resist to competition was indirectly assessed
through emigration since a typical response of Temn oth ora x
colonies to worker loss and predation is emigration to another
nest (O’Shea-Wheller et al. 2015). We also tested colony re-
sistance to cold temperatures. Brood production and worker
survival at the end of the experiment were measured as fitness
parameters that integrated the overall resistance of the colony
to the various challenges.
Material and methods
Colony sampling and rearing
We collected 128 colonies of T.nylanderi in November
2014 and January 2015 in the Bois de Vincennes forest
(Paris, France 48° 50′22.14″N, 2°26′51.96″E).
Colonies were found in twigs. Back to the laboratory,
the twigs were opened to force colonies to move into
artificial nests made of two microscope slides separated
by a 1-mm auto-adhesive plastic foam in which cham-
bers had been cut out. Artificial nests were placed in
10 × 5 × 5 cm plastic rearing boxes (foraging areas)
with Fluon® on the walls to prevent ants from escap-
ing. The boxes were placed in climatic chambers at
23 °C. Water was provided in tubes plugged with cot-
ton. Every week, half a mealworm soaked in honey was
dropped in the foraging area as food. As soon as colo-
nies had settled in their artificial nests, workers and
larvae were counted under a stereomicroscope. We se-
lected 50 colonies containing 1 queen and at least 40
workers for subsequent experiments.
Experimental design
Colonies were assigned randomly to a control or a test group,
with a similar distribution of colony sizes between the two
treatments. In colonies of the test group, we decreased the
variance in worker size by removing 50% of workers, half
(25%) being the largest and half (25%) being the smallest,
using a stereoscopic microscope (Zeiss®, ×50 magnification).
The assignment of workers to the Bsmall^or Blarge^catego-
ries was done visually. In colonies of the control group, we
randomly removed the same proportion of workers (50%) in
order to control for the reduction in colony size. To randomly
remove the workers, we simply did not use a stereoscopic
microscope, so that worker size could not be assessed visually.
The validity of the method was confirmed at the end of the
experiment: we did successfully remove larger and smaller
workers in the test colonies while removing workers randomly
in the control colonies (Wilcoxon rank sum test between large
workers and remaining workers in test colonies W=575,
P< 0.001; between small workers and remaining workers in
test colonies W=98,P< 0.001; between removed workers
and remaining workers in control colonies W=273,P=0.45).
A potential issue is that small workers removed from the test
colonies could be old minim workers from the founding
phase; removing small workers would thus be equivalent to
removing old workers, that is to say foragers. However, we
only included in our experiment large colonies containing
more than 70 workers, so these were not young colonies and
they were unlikely to contain workers from the founding
phase. In addition, to our knowledge, incipient Te m not ho rax
colonies do not produce minim workers and young
Temn ot hor ax colonies have a unimodal worker size distribu-
tion (Howard 2006). All removed workers were killed and
Table 1 Continuous but limited within-colony worker size diversity in social insects has various effects on colony fitness based on literature
Species Polyandry/Polygyny Effect of worker size diversity Approach Quantification of diversity Reference
Temnothorax
longispinosus
No/No or rare
(Foitzik and Heinze
2000)
No effect on colony weight but
positive effect of behavioral
diversity on colony weight
Correlation Head width variation: factor 1.3. +
variations in brood care,
exploration and aggression
Modlmeier and
Foitzik (2011)
Modlmeier et al.
(2012)
Formica
neorufibarbis
?/Yes
(Ian Billick, pers.
comm.)
No effect on number of cocoon
produced per worker
Experiment Head width variation from 0.80 to
1.45 mm: factor 1.8
Billick (2002)
Trachymyrmex
septentrionalis
?/Occasional
(Mehdiabadi and
Shultz 2009)
Positive or negative effect on
biomass of sexuals produced
depending on population
Correlation Head width variation from 0.75 to
1.25 mm: factor 1.7
Bershers and
Traniello (1994)
Solenopsis
invicta
Yes/Yes (Lawson et al.
2012)/(Macom and
Porter 1996)
Positive effect on mass of brood
produced per gram of worker
Experiment Head width variation from 0.63
(or less) to 1.35 mm (or more):
factor 2.14 at least
Porter and Tschinkel
(1985)
Formica
obscuripes
Yes/Yes (Keller and
Reeve
1994)/(Brown and
Keller 2002)
Positive effect on dry mass of
adult workers
Experiment Head width variation from 0.94 to
2.1 mm: factor 2.2
Billick and Carter
(2007)
Behav Ecol Sociobiol (2017) 71:92 Page 3 of 11 92
stored in 70% ethanol to ultimately measure the coefficient of
variation of worker size in the original natural colonies. All
nymphs and last instar larvae were also removed from colo-
nies, and the remaining brood was standardized to 150 larvae
per colony. Accordingly, the nymphs weighed at the end of the
experiment had developed from early instar larvae over the
course of the experiment. Colonies were left undisturbed dur-
ing 6 weeks before we began the challenges.
During 5 months, colonies of both groups were confronted
to a series of six challenges (detailed in the following para-
graph) in order to measure their efficiency at various tasks. To
minimize observer bias, blinded methods were used when
behavioral data were recorded as the experimenter did not
know whether colonies belonged to the test or control group.
Mortality and brood production were monitored at the end of
the experiment. To do so, oncea week, deadworkers and fully
developed pupae were picked out and stored in 70% ethanol
or at −25 °C respectively. Removing fully developed pupae
prevented worker emergence and maintained constant worker
size diversity. At the end of the experiment, all brood was also
stored. Mortality was measured as the percentage of dead
workers, whereas brood productivity was measured as the
weight of all the pupae produced throughout the experiment.
Challenges
Six challenges were conducted sequentially in larger
31 × 24 × 10 cm plastic boxes with Fluon® on the walls.
The plastic boxes were cleaned with 96% ethanol between
each experiment. Artificial nests were transferred from their
rearing boxes into these challenge boxes 30 min before the
beginning of the challenge.
The first challenge was nest emigration following distur-
bance. We forced colonies to relocate, as their nests in nature
are exposed to desiccation, flooding, or destruction (McGlynn
2012), causing frequent relocations (Sendova-Franks and
Franks 1995). Although Temnot hor ax colonies can fight
against competitors, predators, and parasites, they commonly
respondtosuchpressuresbyemigratingtoanothernest
(Jongepier et al. 2014;O’Shea-Wheller et al. 2015).
Accordingly, emigration can be used as a measure of colony
defense. An empty artificial nest was placed 20 cm away from
the original nest containing the colony. The roof of the original
nest was removed at t= 0 so that the colony would relocate to
the new nest. Ants entering the new nest alone, carrying brood
inside the new nest, carrying other workers inside the new
nest, or leaving the new nest were counted and summed up
every 2 min. We then fitted the accumulation curves of the
total numberof larvae and workers to logisticcurves using the
Bgrofit^package for R v2.13.2 (R Development Core Team
2008). Initial values were automatically estimated by the
package, and data were fitted to the logistic function
ytðÞ¼ A
1þexp 4μ
A
*λ−tðÞþ2
, where Ais the maximum number of
ants or brood units inside the new nest, μis the maximum
slope, i.e., the maximum speed of the emigration process,
and λis the lag-phase, i.e., the time it took for emigration to
start (Fig. S1).
For the second challenge, we measured the performance of
colonies at collecting liquid food. We cut 1 × 1 cm pieces of
aluminum sheets covered with Agipa® reinforcement labels
and weighed them at a precision of 0.1 mg using an Ohaus
Pioneer® PA64C balance before and after adding 0.02 mL of
a 0.2 g/mL honey solution with a P200 Gilson’s Pipetman
Classic®. Reinforcement labels were used to constrain the
shape and size of the honey drop, in order to minimize the
differences in evaporation between colonies. Aluminum
sheets were then placed in the middle of the plastic boxes
and left for three hours with the ants. Aluminum sheets were
weighed at the end of the experiment to assess the honey
solution intake of each colony. We then calculated the percent-
age of honey solution evaporated or drank by the ants.
The third challenge was to force colonies to build walls for
their nests. Temnothorax ants prefer nests with a small entrance
and build walls whenever the entrance is too large (Pratt and
Pierce 2001). Colonies were forced to relocate to a new nest by
removing the roof of their nest. The new nest was made of a space
between two microscopes slides with only one wall. After 2 h, we
added 0.25 g of sawdust in the middle of the plastic boxes.
Twenty-four hours later, we collected the sawdust carried inside
the nests that the ants used to build walls, and we weighed it at a
precision of 0.1 mg using an Ohaus Pioneer® PA64C balance.
For the fourth challenge, we measured the performance of
colonies at collecting solid food. Wingless Drosophila flies
were reared, frozen at −25 °C for a few days, and thawed
30 min before the beginning of the experiments. Five dead
Drosophila were placed in the middle of the plastic boxes and
we measured the time it took for the first three Drosophila to
be brought into the nests.
The fifth challenge was to place ant corpses inside the nests
to assess the efficiency of hygienic behaviors. Hygienic be-
haviors are an important component of colony response
against pathogens (Cremer et al. 2007;Diezetal.2014)and,
like many other ants, Temnothorax workers carry dead
nestmates outside (Renucci et al. 2011). A colony of T.
nylanderi was frozen at −25 °C for 48 h and thawed 30 min
before the beginning of the experiments. At t=0,fivedead
ants from this colony were placed inside the artificial nests,
close to the entrance. We recorded the time it took for all
corpses to be discarded out of the nest. Challenges one to five
can also be used to assess colony ability at transporting load, a
trait that is typically linked with worker size (Kaspari 1996).
The final challenge was to inflict a cold shock to the colo-
nies. Colonies are exposed to negative temperatures during
winter. Preliminary experiments on nine colonies showed a
92 Page 4 of 11 Behav Ecol Sociobiol (2017) 71:92
high resistance to cold with 51% of workers surviving after
spending 30 min at −25 °C. Colonies were thus frozen at
−25 °C for 30 min and then placed at 23 °C for 24 h before
counting dead workers. All surviving ants were then frozen to
death and all ants were finally stored in 70° ethanol.
Morphological measurements
The heads of the 8361 stored workers were separated from
their bodies and stuck on double-sided tape. This included
ants picked before the experiments (50% random, 25% larg-
est, and 25% smallest) and the ants used for the experiment
including the ones that died during the experiment. Measuring
the ants removed at the beginning of the experiment allowed
us to test whether our manipulation was successful at decreas-
ing worker size diversity in the test groups and in maintaining
it in the control groups. Heads and a stage micrometer were
photographed with the Nikon® D810 camera and the
Nikkor® 105 mm macro lens with two Nikon® SB-26
flashes. Head widths were measured with ImageJ 1.48 avail-
able at http://imagej.nih.gov/ij/ (Abràmoff et al. 2004).
Statistical analysis
All statistics were conducted using R v3.2.3 available at http://
www.R-project.org/. We first checked whether our
manipulation of worker size diversity had the expected
effects. To do so, we first compared worker size diversity
before and after manipulation both in test and control groups
using a paired Wilcoxon test. We also directly tested whether
colonies of the test group had lower worker size diversity than
colonies of the control group using a Wilcoxon test. Worker
size diversity was assessed by estimating the coefficient of
variation (Sokal and Rohlf 1970).
We tested whether the experimental reduction of worker
size diversity affected colony performance using a
MANOVA. Dependent variables were lag-phase duration for
brood and workers before relocation(λparameter in the equa-
tion of BChallenges^section), maximum speed of brood and
workers relocation (μparameter in the equation of
BChallenges^section), time taken to bring three dead
Drosophila back to the nest, quantity of liquid food collected,
time taken to remove dead workers from the nest, mass of
wood dust carried to build nest walls, and the arcsine square
root transformed percentage of ants that survived cold shock.
Lag-phase duration for brood and workers were correlated
(Pearson’s product-moment correlation t= 12.422, df = 48,
P< 0.001), as well as maximum speed of brood and workers
relocation (Pearson’s product-moment correlation t=7.001,
df = 48, P< 0.001). To avoid multicollinearity, we only con-
sidered data on larvae for our analysis. Note though that the
same qualitative results were obtained if keeping data on
workers. We used treatment as an explanatory variable and
colony size as a covariate. We confirmed the general result
of the MANOVA by performing independent generalized lin-
ear models (GLMs) for each of the dependent variables of the
MANOVA with treatment and colony size and their interac-
tion as explanatory variables. For each model, we successively
removed the interaction (if not significant) and the explanato-
ry variables and performed pairwise comparison between the
models with and without the factors of interest using a Ftest.
We finally performed GLMs with natural mortality and
mass of brood produced as dependent variables, and treat-
ment, colony size, and their interaction as explanatory vari-
ables. Natural mortality was expressed as the ratio of the num-
ber of ants that died over the course of the experiment, before
the cold shock challenge, on the number of ants in the colony
(binomial GLM).
The assumptions of all tests were validated. Regarding
MANOVA, we checked normality (percentage of ants that
survived cold shock was arcsine square root transformed to
respect normality), absence of outliers, absence of
multicollinearity (we removed data on worker emigration
from our analysis), linearity, and equality of covariance matri-
ces. Regarding GLM, we checked homogeneity of variances
and normality of the residuals visually.
Results
Across all colonies, worker head size varied from 0.45 to
0.70 mm (1.55-fold variation; 0.57 mm ± 0.03 mm mean ± sd).
As expected, the manipulation effectively decreased the coef-
ficient of variation of worker size in the test group (Wilcoxon
paired test V=325,P< 0.001) but not in the control group
(Wilcoxon paired test V=184,P= 0.58) showing that random
removal of workers did not affect worker size diversity in
control colonies, whereas non-random removal did (Fig. 1).
Workers in control colonies were thus significantly more var-
iable in size (1.68 times) than in test colonies (Wilcoxon test
W=81,P<0.001;Fig.1).
Colonies successfully overcome all challenges.
Emigrations took less than 166 min and brood was relocated
in less than 158 min. All three Drosophila were carried back to
the nests in less than 150 min (mean = 58 min) and foragers of
all colonies collected liquid food. All five dead workers were
removed in less than 180 min (mean = 37 min). Up to
0.0259 g of sawdust (mean = 0.0086 g) was carried to the
nests to build walls. Mortality after cold shock ranged from
8.4to100%(mean=78.1%).
The treatment had no effect on colony efficiencies
(MANOVA with Pillai test, Pillai = 0.076, P= 0.85) but larger
colonies were more efficient (Pillai = 0.503, P<0.001;treat-
ment and colony size interaction: Pillai = 0.216, P=0.17).
Independent GLMs confirmed that there was no effect of treat-
ment and showed that larger colonies were faster at relocating
Behav Ecol Sociobiol (2017) 71:92 Page 5 of 11 92
brood (F=16,P< 0.001), at bringing dead Drosophila back
to the nest (F=4.39,P= 0.04), and at collecting liquid food
(F= 20.97, P< 0.001) (Fig. 2; Table 2). One interaction
between colony size and treatment was significant regarding
the mass of liquid food collected by the workers (Table 2).
Performance increased quicker with colony size in colonies
with reduced worker size diversity (Fig. 2). Small test colonies
were less efficient than small control colonies, but large test
colonies were more efficient than large control colonies.
There was no interaction between treatment and colony
size on natural mortality (deviance = −0.273, P= 0.60) and
on mass of brood produced (deviance = −2.18e-5, P=0.63).
Treatment had no effect on natural mortality (devi-
ance = −0.487, P= 0.49) and on the mass of brood produced
(deviance = 1.39e-4, P= 0.43). Colony size had no effect on
natural mortality (deviance = −2.05e-1, P= 0.65) but had a
positive effect on the total mass of brood produced (devi-
ance = 6.40e-3, P<0.001).
Discussion
The aim of this study was to assess whether worker size di-
versity in T.nylanderi has a positive effect on colony fitness
parameters. We found that experimentally reducing within-
colony worker size diversity hardly had any effect on colony
efficiency during various challenges, on natural worker mor-
tality, and on the mass of brood produced in the laboratory.
These results are in agreement withthe hypothesis that worker
size diversity could evolve through relaxed selective pressures
and do not support the hypothesis that worker size diversity is
beneficial for the colony and is under positive colony-level
selection.Our study isbased on six challenges that encompass
a wide range of tasks (emigration, foraging, hygienic behav-
iors, nest construction), resistance to an environmental stress-
or (cold), and two synthetic measurements of colony fitness
(worker mortality and brood production). To our knowledge,
this is the first study to investigate so many colony-level fit-
ness components. The significant positive correlation between
colony size and task efficiency found for half of the challenges
irrespective of the treatment (control or test) confirm the com-
monly found positive relationship between colony efficiency
and colony size (Hölldobler and Wilson 1990; Bourke and
Franks 1995; Luque et al. 2013). Our study emphasizes the
need to not overlook species with low worker size diversity.
Comparative studies using closely related species differing in
their degree of worker size diversity would help shed light on
the evolutionary processes that lead to the evolution of worker
size diversity. Experiments including more tasks such as nest
Fig. 1 Boxplot of the coefficient
of variation (CV) of worker head
width in the field and in the labo-
ratory, for control and test groups.
Boxes show median, quartiles,
and extremes. CV did not differ
between control colonies from
field to laboratory, but CV was
successfully lowered in test colo-
nies from field to laboratory due
to the removal of large and small
workers had been removed. The
dashed lines connect the same
colony before and after treatment
92 Page 6 of 11 Behav Ecol Sociobiol (2017) 71:92
defense, or investigating colony fitness directly in the field
should be performed to confirm our conclusion.
Our experimental design was based on the removal of 50%
workers. This could have led to a collapse of colony
Fig. 2 The experimental reduction of worker size diversity had no effect
on colony efficiency at any task. Test colonies are represented by empty
circles and control colonies by black circles. Independent GLMs showed
that larger colonies were faster at relocating brood (a), at bringing dead
Drosophila back to the nest (c), at collecting liquid food (d), and they
produced significantly more brood mass (h). Mortality after freezing (g)
and natural mortality (i) are represented as percentage to facilitate
interpretation of the results. The interaction between colony size and
treatment for the mass of liquid food collected is shown by the two
dotted regression lines (f). Statistics are presented in Table 2and in the
results
Table 2 Analysis of the effect of colony size and worker size diversity on the six variables taken separately using GLM and GLMER
Colony size Treatment Interaction
Analysis Statistical
value
P value Statistical
value
P value Statistical
value
Pvalue
Brood relocation lag-phase time GLM
log(y)
0.53
F
0.39 1.00×10
-3
F
0.97 0.52
F
0.47
Brood relocation speed GLM 16
F
2.22×10
-4
1.22
F
0.27 0.30
F
0.58
Time required to bring 3 dead Drosophila
back to the nest
GLM 4.39
F
0.04 0.71
F
0.40 1.36
F
0.25
Mass of liquid food intake GLM 20.97
F
3.43×10
-5
0.55
F
0.46 8.56
F
5.32×10
-3
Time required for the removal of alien worker corpses GLM 1.71
F
0.19 0.02
F
0.89 0.01
F
0.91
Mass of sawdust carried GLM 0.21
F
0.65 0.08
F
0.78 0.22
F
0.64
Mortality after freezing Binomial
GLMER
1.58
Chi2
0.21 1.52
Chi2
0.22 1.36
Chi2
0.24
Behav Ecol Sociobiol (2017) 71:92 Page 7 of 11 92
organization. However, we made sure that this manipulation
did not affect the colonies too much and this was confirmed by
our results. First, the size of our manipulated colonies
remained within the natural range of colony sizes as it was
not significantly different from the size of an independent
sample of 376 unmanipulated colonies (t=1.65,df=80.72,
P= 0.10). Second, even though reduced, the worker size di-
versity in test colonies fell within or not far below the natural
range of worker size diversity observed in field colonies
(Fig. 1). Third, we did not observe any abnormal mortality
either right after the removal of 50% of the workers, or
throughout the experiment (only 9.3 ± 6.0 workers per colony
died; mean ± sd). Fourth, emigrations were not less efficient
than in other studies; it took 68.1 ± 14.8 min for our manipu-
lated colonies to carry all the brood to their new nest 20 cm
away, whereas Dornhaus and Franks (2006) found that unma-
nipulated colonies of Temnothorax albipennis required about
100 min to transport the last piece of brood to a new nest
35 cm away. Finally, our colonies kept performing everyday
tasks and keptproducing eggs and rearing brood toadulthood.
In conclusion, our colonies of T.nylanderi were resilient to
worker loss. This is not a surprise in this genus: Dornhaus and
Franks (2006; with T.albipennis) and Pinter-Wollman et al.
(2012; with T.albipennis and Temnothorax rugatulus) per-
formed massive worker removals (75 and 20% respectively)
and found that colonies still behaved normally. The 6-week
window between manipulation and the beginning of the ex-
periments allowed colonies to recover and resume normal
activity.
Our results are in agreement with those obtained by
Modlmeier and Foitzik (2011)onTemnothorax longispinosus.
Based on a correlative approach in the laboratory, they found
no link between worker size diversity and per-capita produc-
tivity despite significant differences in worker size diversity
among field colonies. To our knowledge, a significant effect
of worker size diversity on colony fitness in species with lim-
ited worker size diversity has only been demonstrated in po-
lygynous and/or polyandrous species (see Table 1). In these
species, the manipulation of worker size diversity might have
also affected the within-colony level of genetic diversity if
worker size exhibits some level of heritability. Hence, al-
though the importance of worker size diversity for colony
performance has been demonstrated in species with high con-
tinuous worker size diversity, worker subcastes, or soldiers
(e.g., Passera et al. 1996, other references in introduction),
the benefits are far from clear in species with limited worker
size diversity (references in Table 1).
The absence of a treatment effect in our experiment cannot
be explained by a lack of division of labor as Te mn oth o ra x
workers have been shown to specialize in particular tasks
(e.g., Dornhaus et al. 2009; Pinter-Wollman et al. 2012)and
behavioral diversity in brood care and exploration has been
shown to positively correlate with colony productivity
(Modlmeier et al. 2012). However, little is known about the
link between division of labor and worker size in
Temn ot hor ax. Only foraging has been assessed, in two stud-
ies, and larger workers were more likely to forage than smaller
workers (Herbers and Cunningham 1983; Westling et al.
2014). In our study, the only task that was affected by the
treatment (through a significant interaction between colony
size and treatment) was foraging for liquid food. Small test
colonies are less efficient than small control colonies, but large
test colonies are more efficient than large control colonies.
Why colonies with reduced worker size diversity would be-
come more efficient at this task relative to control colonies as
colony size increases is difficult to explain. Considering that
test colonies have a higher proportion of medium workers
than control colonies, one possible explanation would be that
medium workers are more efficient at collecting liquid food
than small and large workers. This result may also simply
correspond to a type 2 error. More experiments are needed
to fully explore the role of worker size on task propensity
and efficiency in Te mno tho ra x.
If Temn ot hor ax colonies do not benefit from worker size
diversity in terms of division of labor, what other selective
pressures could favor such diversity? First, worker size is
known to affect individual resistance to environmental
stressors such as cold shock or starvation (Modlmeier et al.
2013). Accordingly, worker size diversity could help colonies
face different stressors (Couvillon and Dornhaus 2010 in
bumblebees). For instance, if large workers are advantageous
for starving colonies (Modlmeier et al. 2013 in T.nylanderi)
whereas small workers are advantageous when facing another
stressor, worker size diversity could provide benefits to colo-
nies exposed to various stress sources. In addition, even
though small workers are less efficient than large workers, it
can still be advantageous for the colony to produce small
workers when resources are limited. Indeed, as solitary organ-
isms, colonies face a size/number trade off in offspring pro-
duction (e.g., Hasegawa and Imai 2012), so producing more
small workers than few large ones could sometimes allow
colonies to increase growth rate. This is particularly true for
incipient colonies that are known to produce nanitic workers
in various species (e.g., Porter and Tschinkel 1986). Stressful
environmental conditions could therefore select for worker
size diversity. In our experiment, we did not find any treatment
effect on colony recovery from a cold shock, but confronting
colonies to various environmental stressors would be an inter-
esting perspective. Second, in most ant species including
Temn ot hor ax species, workers are able to produce male eggs
through arrhenotokous parthenogenesis. In Temnothorax,
workers rarely reproduce in the presence of the queen, but
conflicts over male production among workers quickly start
after queen removal (Heinze et al. 1997). In ants, larger
workershavemoreovariolesand are more fertile (e.g.,
Dietemann et al. 2002; Clémencet et al. 2008). In
92 Page 8 of 11 Behav Ecol Sociobiol (2017) 71:92
Temn ot hor ax, workers vary in ovariole number and workers
with more ovarioles are more likely to develop their ovaries
following queen removal (Heinze et al. 1997). The distribu-
tion of worker size within a colony might therefore not only
reflect colony-level selection but also individual-level selec-
tion and intra-colonial conflicts. Large workers could thus
sometimes evolve from selfish egg-laying workers (Gobin
and Ito 2003).
Finally, as pointed out in the introduction, worker size di-
versity might simply not be advantageous and result from
relaxed selective pressures on worker size because of social
buffering. Social buffering is a colony-level property that al-
lows for the regular production and survival of divergent phe-
notypes. These phenotypes do not inflict significant costs on
colony fitness because they are diluted among nestmates
(Molet et al. 2012). Social buffering is therefore expected to
reduce selective pressures for canalization, i.e., the mecha-
nisms that keep the phenotype constant in spite of genetic or
environmental variation (see Debat and David 2001 for a
review of the definitions of canalization). Social buffering
could therefore enhance the production of divergent pheno-
types, including slightly smaller and larger workers, because
these inflict no colony-level cost while avoiding the potential
cost of canalization. In social insects, canalization of the adult
phenotype during brood development is achieved by both the
individual developmental process of larvae (Debat and David
2001) and the social behavior of nestmate workers
(Linksvayer et al. 2011). For instance, in cell-building social
insects, the size of individuals is controlled by the quantity of
food provided by workers in the cell (Karsai and Hunt 2002;
Kapheim et al. 2011; Linksvayer et al. 2011;Brandand
Chapuisat 2012) and not only by the ability of larvae to grow.
Many species can also control the abiotic environment expe-
rienced by larvae; for example, Apis mellifera honeybees, red
wood ants of the Formica rufa group, and Temn oth ora x ants
limit temperature fluctuations in their nests (Rosengren et al.
1987; Fahrenholz et al. 1989;Karliketal.2016). Temn oth ora x
ants, despite nesting in small preformed nests, can display
social canalization: under deteriorated environmental condi-
tions, colonies readily migrate to better nests (Dornhaus et al.
2004). Social canalization and its potential cost would deserve
more attention in species with low worker size diversity.
Because our study revealed no effect of worker size diversity
on colony performance, it emphasizes the idea that the degree
of worker size diversity found in colonies of social insects
could result from a balance between the costs and benefits of
social canalization and not only from colony-level benefits of
division of labor as classically admitted in literature.
Acknowledgements This work was funded by Agence Nationale de la
Recherche grant ANTEVO ANR-12-JSV7-0003-01. We thank Jeffrey
Carbillet-Malherbe, Daphné Cahours, Alexandra Rocland, and Morgane
Bequet-Rennes for their help with colony collection, colony rearing, and
preliminary experiments and Ian Billick for the information on polyandry
and polygyny in Formica neorufibarbis. We thank two anonymous ref-
erees for their helpful comments on a previous version of the manuscript.
Authors’contributions TC collected colonies, reared them, performed
the experiments and statistical analyses, and wrote the manuscript. CD
designed the study, contributed to statistical analysis, and wrote the man-
uscript. RP collected colonies and assisted in rearing and experiments.
MM designed the study, wrotethe manuscript, and supervised the project.
All authors read and approved the final manuscript.
Compliance with ethical standards
Funding This work was funded by Agence Nationale de la Recherche
grant ANTEVO ANR-12-JSV7–0003-01.
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval All applicable international, national, and/or institu-
tional guidelines for the care and use of animals were followed.
Data availability statement The dataset analyzed during the current
study is available from the corresponding author on reasonable request.
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