EUSOCIALITY
Social regulation of insulin signaling
and the evolution of eusociality
in ants
Vikram Chandra1
*†, Ingrid Fetter-Pruneda1
*†, Peter R. Oxley1,2
, Amelia L. Ritger1
,
Sean K. McKenzie1,3
, Romain Libbrecht1,4
, Daniel J. C. Kronauer1
*
Queens and workers of eusocial Hymenoptera are considered homologous to the
reproductive and brood care phases of an ancestral subsocial life cycle. However, the
molecular mechanisms underlying the evolution of reproductive division of labor remain
obscure. Using a brain transcriptomics screen, we identified a single gene, insulin-like
peptide 2 (ilp2), which is always up-regulated in ant reproductives, likely because they are
better nourished than their nonreproductive nestmates. In clonal raider ants (Ooceraea
biroi), larval signals inhibit adult reproduction by suppressing ilp2, thus producing a colony
reproductive cycle reminiscent of ancestral subsociality. However, increasing ILP2 peptide
levels overrides larval suppression, thereby breaking the colony cycle and inducing a stable
division of labor. These findings suggest a simple model for the origin of ant eusociality via
nutritionally determined reproductive asymmetries potentially amplified by larval signals.
E
usocial insects exhibit a reproductive division
of labor in which queens lay eggs and
workers perform other tasks (1). Eusociality
in ants, and in many other Hymenoptera,
likely evolved from a subsocial state in which
a female wasp would lay an egg and then care for
the resulting larva until pupation (1–3). Such
brood care may have been induced by larval signals,
and observations of extant subsocial wasps
are consistent with this scenario (2–4). This temporal
reproductive and behavioral plasticity
was then modified into a fixed reproductive
asymmetry between queens and workers in
eusocial colonies (2, 5). This raises three important
mechanistic questions: (i) How are subsocial
reproductive cycles regulated? (ii) How is the
eusocial reproductive division of labor regulated—
i.e., what allows queens to lay eggs but prevents
workers from doing so? (iii) What is the evolutionary
trajectory that gave rise to fixed eusocial
division of labor from subsocial cycles? Here we
suggest that, in ants, evolutionary innovations in
insulin signaling may have played a crucial role
in each case.
Eusociality evolved once in a common ancestor
of ants and, with the exception of a few derived
social parasites, all extant ants are eusocial (6)
(Fig. 1). To identify conserved potential regulators
of division of labor between reproduction
and brood care in ants, we conducted an unbiased
screen for differentially expressed genes between
whole brains or heads of reproductives and nonreproductives
across seven ant species, including
four previously published datasets (Fig. 1 and
tables S1 and S2) (7–11). We sampled a range
of reproductive strategies, from species with
morphologically distinct queens and workers to
queenless species. Among all 5581 identified
single-copy orthologs, we found only one such
gene: insulin-like peptide 2 (ilp2). ilp2 was always
significantly up-regulated in reproductives (Fig. 1).
Thus, the differential expression of ilp2 is likely
conserved across ants. Consequently, the most
recent common ancestor of ants likely had ilp2
expression that was high in reproductives and
low in nonreproductives.
Although our approach is conservative and
probably misses genes, it has the advantage of
eliminating false positives. When we relaxed the
statistical stringency for classifying genes as differentially
expressed, our screen still returned
ilp2 as the single candidate gene (fig. S1). Relaxing
other inclusion criteria revealed additional genes
that might be expected to vary with reproductive
state. For example, a total of 24 genes were consistently
differentially expressed in subsets of five
of the seven studied species (fig. S2 and table S3).
This list includes insulin-like peptide 1 (ilp1), as
well as other genes implicated in insulin signaling
(fig. S3 and table S3). Non–single-copy orthologs
were excluded from our screen. One example
is vitellogenin (vg), a gene that has undergone
repeated duplications in ants (12). The vitellogenin
protein is a lipid carrier that provisions
developing oocytes with yolk and constitutes a
reliable indicator of female reproductive activity
(12, 13). Studies of bees and other insects have
shown that vitellogenin interacts with insulin
signaling (14–16). vg indeed showed consistently
higher expression in reproductives in our screen,
even though this difference was not statistically
significant in two of the ponerines (fig. S3). These
findings further bolster the conclusion that insulin
signaling played a major role in the evolution
of reproductive division of labor in ants.
Insulin regulates reproduction and food-seeking
behavior across a wide range of organisms, making
it a prime candidate for the regulation of subsocial
cycles and eusocial division of labor (17).
Most studied hymenopterans have two ILPs: ILP1
and ILP2 (fig. S4). Whereas ILP1 resembles insulinlike
growth factor, ILP2 is similar to canonical
insulin (fig. S5) (11). In other holometabolous
insects, these ILPs regulate larval growth, adult
metabolism, and reproduction (17–19). Moreover,
caste determination in most ant species
relies on nutritional asymmetries during development:
Queen-destined larvae eat more than
worker-destined larvae, which likely explains
how queens acquire higher ILP2 levels (20). A
study of Diacamma sp. found that the asymmetry
in reproductive potential between ants was correlated
with insulin receptor expression in the
ovaries (21). This suggests a possible secondary
mode of reproductive control downstream of
ILPs that may augment the initial reproductive
asymmetry reflected by differential ilp2 expression
in the brain.
ILPs have not been studied functionally in
eusocial insects in the context of reproductive
division of labor between adults. However, insulin
signaling has been implicated in other contexts,
such as caste development and nonreproductive
division of labor (18, 22–24). Current data from
wasps and bees do not typically indicate that ilp2
is differentially expressed between adult queens
and workers, suggesting that this expression pattern
may be ant specific (table S5). This apparent
inconsistency may be explained by the fact that
eusociality has evolved independently in ants,
bees, and wasps (1). Therefore, though insulin
signaling may have been co-opted repeatedly
during social evolution, the details likely differ
between independent lineages.
We used the clonal raider ant Ooceraea biroi
to study ILP2 in ants. O. biroi has secondarily
lost queens, resulting in a species in which workers
reproduce synchronously and asexually (13, 25).
Colonies alternate between reproductive and
brood care phases. This colony cycle is regulated
by the periodical presence of larvae, which
suppress reproduction and induce brood care
behavior in adults, and is reminiscent of the
subsocial cycle presumed to precede eusociality
in ants. Despite this unusual biology, O. biroi is
eusocial. Workers display cooperative brood
care, colonies contain overlapping generations
of adults, and reproductive asymmetry exists within
colonies (25).
We found that antibody staining of ILP2 exclusively
localized to the brain, primarily in a
single medial cluster of ~15 cells in the pars
intercerebralis (Fig. 2, A to C, and fig. S6). These
insulin-producing cells (IPCs) coincide in location
with those of other insects (26, 27). Axons
likely project to the corpora cardiaca, the only
other brain region staining positive for ILP2
(figs. S6 to S8). We quantified ILP2 in the IPCs
and found that its levels are higher in the brood
RESEARCH
Chandra et al., Science 361, 398–402 (2018) 27 July 2018 1 of 5
1
Laboratory of Social Evolution and Behavior, The Rockefeller
University, 1230 York Avenue, New York, NY 10065, USA.
2
Samuel J. Wood Library, Weill Cornell Medicine, 1300 York
Avenue, New York, NY 10065, USA. 3
Department of Ecology
and Evolution, University of Lausanne, Biophore Building,
1015 Lausanne, Switzerland. 4
Institute of Organismic and
Molecular Evolution, Johannes Gutenberg University,
Johannes-von-Müller-Weg 6, 55128 Mainz, Germany.
*Corresponding author. Email: vchandra@rockefeller.edu (V.C.);
ifetter@rockefeller.edu (I.F.-P.); dkronauer@rockefeller.edu
(D.J.C.K.) †These authors contributed equally to this work.
onJuly31,2018http://science.sciencemag.org/Downloadedfrom
care than in the reproductive phase (Fig. 2D and
fig. S6). Peptide levels are thus anticorrelated
with transcription. This pattern is known from
Drosophila melanogaster, in which the rate of
ILP secretion correlates with the rate of ilp transcription
(27). This suggests that the mechanisms
of ilp expression and ILP secretion are conserved
in holometabolous insects.
Because larvae regulate the O. biroi colony
cycle, we asked whether larval communication
altered ilp2 expression in adults. When larvae
are removed from colonies in the brood care
phase, ilp2 expression levels in adult brains increase
markedly within 12 hours (Fig. 2E) (28).
This increase occurs under identical nutritional
conditions. Conversely, when ants in the reproductive
phase are given larvae, their ilp2 levels
decrease (Fig. 2E). vgq, the vitellogenin gene upregulated
in ant queens, responds similarly, albeit
more slowly, to these changes (fig. S9A), raising
the possibility that ILP2 regulates reproduction
at least partly by acting on vgq. Although this
experiment is highly suggestive, the addition of
larvae was always correlated with the removal of
pupae, and changes in expression occurring after
the 24-hour time point were confounded by nutritional
differences. We therefore repeated this
experiment without pupae and under nutritionally
controlled conditions. We removed larvae
from colonies in the brood care phase, waited
until the ants in these colonies activated their
ovaries, and then compared brain gene expression
between these and control colonies. Again,
the removal of larvae increased ilp2 (Fig. 2F) and
vgq (fig. S9B) expression. This finding suggests
that social signals can mediate insulin signaling
independently of internal nutritional state and
that this is a key regulatory mechanism underlying
the O. biroi colony cycle. Given the conserved
association of caste and ilp2 expression in all ants,
social regulation of ilp2 may also underlie the life
cycle of the subsocial ancestor.
In D. melanogaster, insulin signaling is necessary
and sufficient to regulate the terminal differentiation
of germline stem cells into oocytes.
Moreover, it promotes yolk uptake in developing
oocytes and is crucial for ovary activation (29). It
is therefore plausible that the differential expression
of ilp2 in ants has a causal role in regulating
ovary activation and reproductive division of labor.
We further hypothesized that if the regulation of
ilp2 were freed, at least partially, from larval
control, this would yield ants whose physiology
is less susceptible to reproductive suppression.
Such a mechanism would allow the evolution
of distinct reproductive and nonreproductive
castes from an ancestral subsocial cycle. To test
Chandra et al., Science 361, 398–402 (2018) 27 July 2018 2 of 5
Fig. 1. Brain gene expression
in seven ant species identifies
one conserved differentially
expressed gene. The figure
shows the summary cladogram
of the seven ant species used in
this study in the context of the
entire ant phylogeny with all
subfamilies labeled. Five of the
focal species have queens,
whereas two (Dinoponera
quadriceps and O. biroi) are
queenless. Although Harpegnathos
saltator is not queenless, the
data compared reproductive
and nonreproductive workers
(table S1). The dot plots show
variance-stabilized transformed
read counts for ilp2. Blue and
orange dots indicate reproductive
(R) and nonreproductive
(NR) ants, respectively. Horizontal
bars indicate means, and
asterisks indicate statistically
significant differences between
groups (Wald test: *P < 0.05;
***P < 0.001). All photos
except for those of Acromyrmex
echinatior are from A. Nobile,
S. Hartman, and E. Prado
(www.antweb.org). Scale bars,
2 mm. The phylogeny is
based on (30). Species
numbers are from (6).
R NR
Camponotus planatus
Aneuretinae
Dolichoderinae
Formicinae
Ectatomminae
Heteroponerinae
Acromyrmex echinatior
Solenopsis invicta
Myrmicinae
Agroecomyrmecinae
Amblyoponinae
Apomyrminae
Harpegnathos saltator
Odontomachus ruginodis
Ooceraea biroi
Dinoponera quadriceps
Myrmeciinae
Proceratiinae
Leptanillinae
Martialinae
Paraponerinae
Ponerinae
Dorylinae
Pseudomyrmecinae
origin of ant
eusociality
formicoid
clade
poneroid
clade
Number of species
>3000
1000-3000
500-1000
100-500
5-100
7
8
9
10
R NR
*
***
R
7
8
9
10
11
12
NR
*
6
7
8
9
10
R NR
***
6
8
10
12
14
R NR
4
6
8
10
R NR
*
6
7
8
9
10
R NR
***
8
9
10
11
12
R NR
Reproductive
(R)
Non-
reproductive
(NR)
R NR
R/NR
R NR
R NR
ilp2mRNAilp2mRNAilp2mRNAilp2mRNAilp2mRNAilp2mRNAilp2mRNA
R/NR
***
11
<5
RESEARCH | REPORT
onJuly31,2018http://science.sciencemag.org/Downloadedfrom
this hypothesis, we injected synthetic O. biroi
ILP2 mature peptide into workers in colonies
with larvae. As a control, we injected the inactive
B chain of this peptide (fig. S11A) (19). Injecting
ILP2 mature peptide caused strong ovary activation
despite the presence of larvae (Fig. 3, A to C,
and fig. S10A). Higher doses of ILP2 caused ants
to develop more eggs simultaneously (fig. S10, B
and C), suggesting that quantitative differences
in ILP2 levels vary the ants’ positions along a
spectrum of reproductive potential. To ensure that
ILP2 does not have inhibitory effects during the
opposite phase of the colony cycle, we injected
ants in the reproductive phase with ILP2 and
found no detectable effect on ovary state (fig. S11,
B and C).
Finally, we hypothesized that as developmental
nutritional asymmetries determine caste in
most ants, this might be a general and natural
mechanism that produces asymmetries in baseline
adult ILP2 levels and consequently in reproductive
potential. Whereas most O. biroi workers have two
ovarioles, some individuals (“intercastes”) have
four or more (25) (fig. S12, A and B). We found
that these differences can be determined by the
amount of food a larva receives (fig. S13). Intercastes
have longer and more active ovaries compared
with those of regular workers in the brood
care phase, suggesting intercastes are less sensitive
to larval signals that suppress ovarian activity
(Fig. 4A and fig. S12C). This finding is
consistent with previous work showing that
some intercastes fail to regress their ovaries
during the brood care phase (25). Additionally,
we found that the IPCs of intercastes contained
more ILP2 than those of regular workers (Fig. 4,
B and C). As we have shown above, ILP2 peptide
levels are negatively correlated with ilp2 expression,
ovary state, and, by extension, circulating
ILP2 levels in workers between the different
phases of the cycle, probably owing to higher rates
of peptide release during the reproductive phase
(Fig. 2D). The phase-matched comparisons between
different types of workers, on the other
hand, show that intercastes consistently have
higher ILP2 levels in their IPCs, and, given their
more active ovaries and decreased sensitivity to
larval signals (25), it is likely that they also have
consistently higher levels of ILP2 in circulation.
How the ancestral subsocial cycle was regulated
remains unknown. However, assuming that
similar mechanisms underlie the O. biroi colony
cycle, our findings suggest a plausible scenario for
the evolution of ant sociality. First, during the
transition from solitary to subsocial life, some
signaling systems (probably including insulin
signaling) in adults must have become responsive
to larval signals. This shift allowed behavioral
and physiological responses in adults to
be appropriately modified for the nutritional
requirements of the larvae. During the transition
from subsocial to eusocial life, increased
developmental variation may have caused some
Chandra et al., Science 361, 398–402 (2018) 27 July 2018 3 of 5
50 µm
***10.0
9.5
9.0
8.5
8.0
7.5
ilp2mRNA No larvae Larvae0 50 100
8
9
Brood care to reproductive
Reproductive to brood care
10
11
feeding
ilp2mRNA
*
Reproductive Brood care
Totalintensity(a.u.)ofILP2inIPCs
6
4
2
0
100 µm
MB
AL
IPCs Fibers
Time in hours
Fig. 2. Larvae regulate ilp2 in adults. (A to C) Immunohistochemistry
with antibody against ILP2 (anti-ILP2) on an O. biroi brain localizes ILP2
peptide to a single cluster of insulin-producing cells (IPCs) in the pars
intercerebralis (body-axis dorsal view). Green, anti-ILP2; blue, DAPI (4′,6diamidino-2-phenylindole);
magenta, phalloidin. MB, mushroom body;
AL, antennal lobe. (D) Total intensity of ILP2 in the IPCs is higher in the brood
care phase than in the reproductive phase (n ≥ 14 ants, t test; *P = 0.046).
a.u., arbitrary units. (E) RNA sequencing (RNA-seq) time course shows
that the addition of larvae down-regulates ilp2, whereas the removal
of larvae up-regulates ilp2 [n ≥ 4 biological replicates, time-transition
interaction, likelihood ratio test with 5% false discovery rate (FDR)
correction; P < 10−15
]. The arrow indicates when ants with larvae
were fed (i.e., changes in expression beyond that time point are
confounded by differences in nutrition). Error bars depict SEM. Data are
from (28). (F) RNA-seq on ant brains shows that under nutritionally
controlled conditions, ilp2 is up-regulated 8 days after larvae are
removed from O. biroi workers in the brood care phase (n = 4 biological
replicates, Wald test with 5% FDR correction; ***P < 10−6
). Data
are variance-stabilized transformed read counts. Horizontal bars
indicate means.
RESEARCH | REPORT
onJuly31,2018http://science.sciencemag.org/Downloadedfrom
adults to emerge from the pupa with low nutritional
stores and low ILP2 levels. These subfertile
individuals would have been more sensitive
to larval signals that suppress reproduction and
would consequently have foregone nest founding
and ovary activation and instead assumed brood
care roles. Other adults, meanwhile, would have
emerged with high nutritional stores and high
ILP2 levels. These adults would have had reduced
sensitivity to larval signals and would have been
more likely to reproduce despite the presence of
larvae. This reproductive asymmetry could then
have been enhanced or modified by natural selection
to ultimately produce the obligately reproductive
queens and sterile workers of advanced
eusocial species (fig. S14). This scenario constitutes
an explicit molecular version of Mary Jane
West-Eberhard’s model for the evolution of hymenopteran
eusociality (5).
REFERENCES AND NOTES
1. E. O. Wilson, The Insect Societies (Belknap Press, 1971).
2. W. M. Wheeler, Ants: Their Structure, Development and
Behavior (Columbia Univ. Press, 1910).
3. J. Hunt, The Evolution of Social Wasps (Oxford Univ. Press, 2007).
4. J. Field, Behav. Ecol. 16, 770–778 (2005).
5. M. J. West-Eberhard, in Animal Societies:Theories and Facts, Y. Itô,
J. L. Brown, J. Kikkawa, Eds. (Japan Scientific Societies Press,
1987), pp. 35–51.
6. P. S. Ward, Annu. Rev. Ecol. Evol. Syst. 45, 23–43 (2014).
7. R. Libbrecht, P. R. Oxley, L. Keller, D. J. C. Kronauer, Curr. Biol.
26, 391–395 (2016).
8. S. Patalano et al., Proc. Natl. Acad. Sci. U.S.A. 112,
13970–13975 (2015).
9. Q. Li et al., Nat. Commun. 5, 4943 (2014).
10. J. Gospocic et al., Cell 170, 748–759.e12 (2017).
11. Materials and methods are available as supplementary materials.
12. M. Corona et al., PLOS Genet. 9, e1003730 (2013).
13. P. R. Oxley et al., Curr. Biol. 24, 451–458 (2014).
14. L. Badisco, P. Van Wielendaele, J. Vanden Broeck, Front.
Physiol. 4, 202 (2013).
15. M. Corona et al., Proc. Natl. Acad. Sci. U.S.A. 104, 7128–7133
(2007).
16. K.-A. Nilsen et al., J. Exp. Biol. 214, 1488–1497 (2011).
17. A. L. Toth, G. E. Robinson, Trends Genet. 23, 334–341
(2007).
18. Y. Wang, S. V. Azevedo, K. Hartfelder, G. V. Amdam, J. Exp.
Biol. 216, 4347–4357 (2013).
19. M. R. Brown et al., Proc. Natl. Acad. Sci. U.S.A. 105, 5716–5721
(2008).
20. W. Trible, D. J. C. Kronauer, J. Exp. Biol. 220, 53–62 (2017).
21. Y. Okada et al., J. Insect Physiol. 56, 288–295 (2010).
22. S. V. de Azevedo, K. Hartfelder, J. Insect Physiol. 54,
1064–1071 (2008).
23. D. E. Wheeler, N. Buck, J. D. Evans, Insect Mol. Biol. 15,
597–602 (2006).
24. S. A. Ament, M. Corona, H. S. Pollock, G. E. Robinson,
Proc. Natl. Acad. Sci. U.S.A. 105, 4226–4231 (2008).
25. S. Teseo, D. J. C. Kronauer, P. Jaisson, N. Châline, Curr. Biol.
23, 328–332 (2013).
26. M. A. Riehle, Y. Fan, C. Cao, M. R. Brown, Peptides 27,
2547–2560 (2006).
27. C. Géminard, E. J. Rulifson, P. Léopold, Cell Metab. 10,
199–207 (2009).
28. R. Libbrecht, P. R. Oxley, D. J. C. Kronauer, bioRxiv 223255
[Preprint]. 22 November 2017. https://doi.org/10.1101/223255.
29. L. LaFever, D. Drummond-Barbosa, Science 309, 1071–1073
(2005).
30. M. L. Borowiec et al., bioRxiv 173393 [Preprint]. 8 August 2017.
https://doi.org/10.1101/173393.
31. P. Oxley, V. Chandra, Social-evolution-and-behavior/
insulin_signaling: Data and code: Social regulation
of insulin signaling and the evolution of eusociality in ants,
Version 1.1, Zenodo (2018); https://doi.org/10.5281/
zenodo.1311222.
ACKNOWLEDGMENTS
We thank C. Zhao, H. Zebroski III, T. Tong, and the Rockefeller
University Resource Centers for sequencing, peptide synthesis,
and help with image analysis; M. Deyrup for assistance with ant
collection; L. Olivos-Cisneros for dissecting brains; and
Chandra et al., Science 361, 398–402 (2018) 27 July 2018 4 of 5
ILP2 ILP2 B chain
100 µm
largest oocyte largest oocyte
100 µm
0
10000
20000
30000
40000
50000
***
Brood care phase
Largestoocytesurfacearea(µm2
)
ILP2 ILP2 B chain
Fig. 3. ILP2 supplementation overrides larval suppression of adult
reproduction. (A) Workers injected with 100 mM ILP2 in the brood care
phase activate their ovaries relative to controls injected with 100 mM ILP2
B chain, despite being in contact with larvae [n ≥ 10, Welch’s t test with
Bonferroni correction (related data in fig. S8); ***P = 0.0005]. (B and
C) Confocal images of ovaries from ants injected with either 100 mM ILP2
(B) or 100 mM ILP2 B chain (C).Shown are the pairs ofovaries closest to themean
value from each treatment; the largest oocyte in each pair is circled in blue.
***
0
1000
2000
3000
4000
Brood care phase
***
Totalintensity(a.u.)ofILP2inIPCs
0
2
4
6
Brood care phase
**
Totalintensity(a.u.)ofILP2inIPCs
0
2
4
6
8
10
Reproductive phase
Largestoocytesurfacearea(µm2
)
Intercastes Workers Intercastes Workers Intercastes Workers
Fig. 4. Intercastes respond less to larvae and have more ILP2 than
regular workers. (A) Intercastes have more active ovaries than agematched
regular workers in the brood care phase, despite both groups
being in contact with larvae (n ≥ 16, Welch’s t test; ***P < 0.0001). (B) In
the brood care phase (n = 19, Mann-Whitney U test; ***P < 0.0001) and
(C) in the reproductive phase (n ≥ 12, Mann-Whitney U test; **P =
0.0043), intercastes have more ILP2 in their IPCs than age-matched
regular workers. Horizontal bars indicate means on all dot plots.
RESEARCH | REPORT
onJuly31,2018http://science.sciencemag.org/Downloadedfrom
L. Vosshall, C. Bargmann, B. Chait, H. Yan, C. Desplan, and
the entire Kronauer laboratory for helpful discussion. This is
Clonal Raider Ant Project paper no. 9. Funding: This work was
supported by grant 1DP2GM105454-01 from the NIH, a Searle
Scholar Award, a Sinsheimer Scholar Award, a Hirschl/WeillCaulier
Trusts Award, a Klingenstein-Simons Award, a Pew
Scholar Award, and an HHMI Faculty Scholar Award (D.J.C.K.);
a Leon Levy Neuroscience Fellowship (P.R.O.); a Rockefeller
University Women & Science Fellowship (I.F.-P.); and a Marie
Curie International Outgoing Fellowship (PIOF-GA-2012-327992;
R.L.). Author contributions: D.J.C.K., V.C., I.F.-P., and P.R.O.
designed the study; S.K.M., I.F.-P., and V.C. performed
fieldwork; P.R.O., V.C., R.L., S.K.M., I.F.-P., and A.L.R. performed
genomic analyses; I.F.-P., V.C., A.L.R., R.L., and S.K.M.
performed immunostains; V.C., A.L.R., I.F.-P., and P.R.O.
performed pharmacological experiments; V.C., I.F.-P., and
D.J.C.K. wrote the manuscript with feedback from all authors;
and D.J.C.K. supervised the project. Competing interests:
The authors declare no competing interests. Data and
materials availability: Raw sequence data are available
through NCBI (BioProject PRJNA472392); scripts are
available on GitHub (31).
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/361/6400/398/suppl/DC1
Materials and Methods
Supplementary Text
Figs. S1 to S14
Tables S1 to S6
References (32–76)
22 November 2017; resubmitted 1 April 2018
Accepted 30 May 2018
10.1126/science.aar5723
Chandra et al., Science 361, 398–402 (2018) 27 July 2018 5 of 5
RESEARCH | REPORT
onJuly31,2018http://science.sciencemag.org/Downloadedfrom
Social regulation of insulin signaling and the evolution of eusociality in ants
C. Kronauer
Vikram Chandra, Ingrid Fetter-Pruneda, Peter R. Oxley, Amelia L. Ritger, Sean K. McKenzie, Romain Libbrecht and Daniel J.
DOI: 10.1126/science.aar5723
(6400), 398-402.361Science
, this issue p. 398Science
of the associated peptide override these larval signals and establish eusociality.
clonal ant, larval signals disrupt this gene up-regulation, destabilizing the division of reproductive labor. Increasing levels
up-regulated in queens. This gene seems to confer reproductive status through integration with increased nutrition. In a
used a transcriptomic approach to show that a single gene is consistentlyet al.different species of ants, Chandra
sevenqueen. Although this system has evolved repeatedly, there is still much debate surrounding its origin. Working with
In eusocial insects, the vast majority of individuals sacrifice their reproductive potential to support the reproductive
The benefits of being well fed
ARTICLE TOOLS http://science.sciencemag.org/content/361/6400/398
MATERIALS
SUPPLEMENTARY http://science.sciencemag.org/content/suppl/2018/07/25/361.6400.398.DC1
REFERENCES
http://science.sciencemag.org/content/361/6400/398#BIBL
This article cites 68 articles, 19 of which you can access for free
PERMISSIONS http://www.sciencemag.org/help/reprints-and-permissions
Terms of ServiceUse of this article is subject to the
is a registered trademark of AAAS.Science
licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. The title
Science, 1200 New York Avenue NW, Washington, DC 20005. 2017 © The Authors, some rights reserved; exclusive
(print ISSN 0036-8075; online ISSN 1095-9203) is published by the American Association for the Advancement ofScience
onJuly31,2018http://science.sciencemag.org/Downloadedfrom