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Social cancer and the biology of the clonal ant Pristomyrmex punctatus (Hymenoptera: Formicidae)

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We review some aspects of the biology of the ant Pristomyrmex punctatus, in which the winged queen caste is absent and wingless females reproduce by thelytokous parthenogenesis. The majority of females have two ovarioles, whereas up to 50% of colonies contain large-bodied females which have four ovarioles. We call the former workers and the latter ergatoid queens. Males are rare. Some ergatoid queens have a spermatheca, but no inseminated individual has been found so far. Castes are morphologically defined, and workers engage in asexual reproduction in all colonies regardless of the presence of ergatoid queens. In colonies containing only workers, reproductive division of labor is regulated by age-polyethism: All young workers reproduce and fulfill inside-nest roles, and old workers become sterile and fulfill outside-nest roles. Colonies are founded by fission or budding, and consequently neighboring colonies are often re-lated. Nevertheless, populations are multi-colonial, with strong hostility among neighboring colonies. A genetic analysis revealed that colonies often have multiple genotypes (parthenogenetic lineages), and suggested that the majority of those lineages can produce both workers and ergatoid queens. However, a lineage in a population in central Japan pro-duces only ergatoid queens. We define these queens as cheaters, as they fulfill no other task than oviposition and therefore depend on the work force of other non-cheater lineages. Ergatoid queens in cheater lineages have three distinct ocelli, but those in non-cheater lineages usually have zero to two. As cheaters are likely to be horizontally transmitted, we draw an analogy to transmissible cancers. The coexistence of cheaters and non-cheaters is discussed in the frameworks of multilevel selection in the short term, and local extinction-immigration in the long term. However, many things re-main to be studied, such as the developmental origin of the ergatoid queens, the frequency of sexual reproduction, and how colony identity is maintained.
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Myrmecological News 15 91-99 Vienna, May 2011
Ross H. Crozier Memorial Volume
Social cancer and the biology of the clonal ant Pristomyrmex punctatus (Hymenoptera:
Formicidae)
Kazuki TSUJI & Shigeto DOBATA
Abstract
We review some aspects of the biology of the ant Pristomyrmex punctatus, in which the winged queen caste is absent
and wingless females reproduce by thelytokous parthenogenesis. The majority of females have two ovarioles, whereas
up to 50% of colonies contain large-bodied females which have four ovarioles. We call the former workers and the
latter ergatoid queens. Males are rare. Some ergatoid queens have a spermatheca, but no inseminated individual has been
found so far. Castes are morphologically defined, and workers engage in asexual reproduction in all colonies regardless
of the presence of ergatoid queens. In colonies containing only workers, reproductive division of labor is regulated by
age-polyethism: All young workers reproduce and fulfill inside-nest roles, and old workers become sterile and fulfill
outside-nest roles. Colonies are founded by fission or budding, and consequently neighboring colonies are often re-
lated. Nevertheless, populations are multi-colonial, with strong hostility among neighboring colonies. A genetic analysis
revealed that colonies often have multiple genotypes (parthenogenetic lineages), and suggested that the majority of
those lineages can produce both workers and ergatoid queens. However, a lineage in a population in central Japan pro-
duces only ergatoid queens. We define these queens as cheaters, as they fulfill no other task than oviposition and therefore
depend on the work force of other non-cheater lineages. Ergatoid queens in cheater lineages have three distinct ocelli,
but those in non-cheater lineages usually have zero to two. As cheaters are likely to be horizontally transmitted, we
draw an analogy to transmissible cancers. The coexistence of cheaters and non-cheaters is discussed in the frameworks
of multilevel selection in the short term, and local extinction-immigration in the long term. However, many things re-
main to be studied, such as the developmental origin of the ergatoid queens, the frequency of sexual reproduction, and
how colony identity is maintained.
Key words: Clonal ant, cheating, social cancer, genetic caste determination, parthenogenesis, ergatoid queen, colony
discrimination, review.
Myrmecol. News 15: 91-99 (online 20 April 2011)
ISSN 1994-4136 (print), ISSN 1997-3500 (online)
Received 27 September 2010; revision received 4 February 2011; accepted 8 February 2011
Prof. Dr. Kazuki Tsuji (contact author) & Dr. Shigeto Dobata, Department of Agro-Environmental Sciences, Faculty of
Agriculture, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan. E-mail: tsujik@agr.u-ryukyu.ac.jp
Introduction
In queenless ant species, the role of morphologically dis-
tinguishable queens as the primary reproductive females is
taken by mated workers called gamergates. Gamergates in
some members of the Amblyoponinae, Ponerinae, and Ec-
tatomminae are functional queens (MONNIN & PEETERS
2008), and colonies show reproductive division of labor be-
tween gamergates and sterile workers. In contrast, although
winged queens are also absent in the myrmicine ant Pristo-
myrmex punctatus (previously called P. pungens) and in
the cerapachyine ant Cerapachys biroi, the reproductive di-
vision of labor is unrelated to mating (TSUJI 1988a, RA-
VARY & JAISSON 2004). Instead, many wingless females
reproduce totally asexually by thelytokous parthenogenesis
(ITOW & al. 1984, TSUJI & YAMAUCHI 1995). These social
systems differ from those recently found in two, also ob-
ligatory parthenogenetic, myrmicine ants, Mycocepurus
smithii and Pyramica membranifera, in which winged
queens produce both sterile workers and new queens com-
pletely parthenogenetically (HIMLER & al. 2009, RABELING
& al. 2009, ITO & al. 2010). In this paper, we review some
aspects of the biology of Pristomyrmex punctatus to cla-
rify its peculiarity among "thelytokous ants". We also dis-
cuss that P. punctatus is a good system to study evolu-
tionary dynamics of cooperation and cheating.
Life cycle and division of labor
The majority of colonies in Pristomyrmex punctatus consist
of only workers that are morphologically defined (TSUJI
1988a, 1995), although some colonies have ergatoid queens
whose definition is described later in detail. First, we de-
scribe the biology of those colonies containing only wor-
kers. In ants and social bees, division of labor among wor-
kers is mostly age dependent, in that young workers ful-
fill inside-nest roles such as nursing, while old workers per-
form outside-nest tasks such as foraging (the temporal castes
or age-polyethism; OSTER &WILSON 1978). In P. puncta-
tus, reproductive division of labor is regulated by this age-
polyethism (TSUJI 1990a): Young workers reproduce and
simultaneously perform other inside-nest tasks, while old
workers cease reproduction and perform outside-nest tasks.
The distribution of the number of mature oocytes that nest-
workers have fits a Poisson distribution (TSUJI 1988a). This
means that all young workers have a similar probability of
egg-laying and the variation of short-term fecundity may
occur just by chance. All workers follow this same beha-
vioral development, and therefore there are neither perma-
nently reproductive nor permanently sterile workers. Fur-
thermore, neither dominance behavior nor policing has been
observed among workers (TSUJI 1988a, 1990a). This si-
tuation has raised semantic arguments of whether this ant
should be regarded as eusocial or not (TSUJI 1990a, 1992,
FUREY 1992). Reproductive division of labor in Cerapachys
biroi is likewise regulated by age-polyethism. Although
C. biroi colonies show cyclic phases as seen in some Eci-
ton army ants (RAVARY & JAISSON 2002, RAVARY & al.
2006), old workers do not reproduce even in the stationary
(non-migratory) phase, in which young workers lay eggs
(RAVARY & JAISSON 2004).
The reproductive biology of Pristomyrmex punctatus
and Cerapachys biroi markedly differ from any other ex-
ample of ants that are known to be able to reproduce by
thelytokous parthenogenesis in that the majority (possibly
all) of females participate in reproduction at least once in
their life. In these other ants, the majority of females are
sterile helpers, with reproductive division of labor regulated
either by the physical caste system (such as in Anoplolepis
gracilipes, see DRESCHER & al. 2007, Cataglyphis spp., see
PEARCY & al. 2004, TIMMERMANS & al. 2008, Pyramica
membranifera, see ITO & al. 2010, Mycocepurus smithii,
see HIMLER & al. 2009, RABELING & al. 2009, Messor ca-
pitatus, see GRASSO & al. 2000, Vollenhovia emeryi, see
OHKAWARA & al. 2006, KOBAYASHI & al. 2008, and Was-
mannia auropunctata, see FOURNIER & al. 2005) or by be-
havioral dominance and / or policing (in Platythyrea punc-
tata, see HARTMANN & al. 2003). Furthermore, Pristomyr-
mex punctatus and Cerapachys biroi contrast with Platy-
thyrea punctata in which either physical caste system or
behavioral interference regulates reproductive division of
labor depending on colonies and populations (HEINZE &
HÖLLDOBLER 1995, SCHILDER & al. 1999, HARTMANN &
al. 2003).
Although age-polyethism is the general pattern that in
turn regulates the reproductive division of labor in Pristo-
myrmex punctatus, individuals show large variation in be-
havioral development: The timing of the switch from inside-
nest tasks to outside-nest tasks occurs two to three weeks
before the worker's death (in lab-reared colonies), yet indi-
vidual life span is highly variable for unknown reasons
(TSUJI 1990a). Consequently, a long-lived worker tends to
have a longer inside-nest phase and therefore more oppor-
tunity for reproduction than a short-lived one. At least two
interpretations of the adaptive significance of this pheno-
menon are possible: either that the long lifespan in some
workers is a manifestation of the individuals' self-interest
(see our later discussion on cheaters), or that this is a means
to maintain the colony's efficient task allocation. The an-
nual reproductive cycle of colonies we studied in central
Honshu, the main island of Japan, shows why such flexi-
bility would be needed: New adults emerge from June to
September (peaking in early August). They withhold repro-
ducing until after overwintering. Overwintered adults begin
oviposition in April; they lay eggs and raise brood until
the end of fall, when they die. The adult emergence period
(June – September) is shorter than the breeding period
(April – September). Therefore, if all individuals followed
the same schedule of age-polyethism, inefficient task allo-
cation would happen at some time of the year; for example,
a shortage of foragers or of egg-layers. Such unbalanced
task allocation lowers colony efficiency under experimen-
tal conditions (TSUJI 1994) and probably also in the field
(TSUJI 1995).
Individual variation might enable a colony to evade such
a problem. TSUJI (1994) found that laboratory colonies of
which all foragers were removed at the outset of the ex-
periment later produced some brood. Indeed, during the ex-
perimental period for 20 days, some young workers which
had never previously foraged started to forage and obtained
food. Although this behavior might have been an artifact
caused by the small size of the lab cage, or more simply
aging (some might have become foragers) could account
for it, it is also possible that some nest-workers could be
flexibly recruited to foraging when a large work force is
needed. So far, division of labor of this species was ob-
served mostly in laboratories with constant conditions.
Behavior, in particular the flexibility of division of labor,
should be studied also under heterogeneous environments
like in the field.
Migration, colony founding, and nestmate discrimination
Despite its unusual biology, Pristomyrmex punctatus forms
a typical multi-colonial population (TSUJI & I 1986).
The colony size ranges from 4,000 to 320,000 adults (TSUJI
1988a, 1995). Neighboring colonies are strongly hostile to-
ward each other, and lethal fights sometimes occur in the
field (TSUJI 1988b). The absence of alate queens implies
that new colonies must be founded by fission or budding.
However, so far no one has directly observed a colony be-
ing founded in the field. In laboratories, small colonies,
with less than 100 individuals, always show very low per-
formance and often fail to produce any adult offspring
(K. Tsuji & S. Dobata, unpubl.). This suggests that colony
founding should occur with a large group of individuals,
i.e., possibly at least hundreds. Colonies do not construct
an elaborate underground nest, but instead use naturally pre-
existing cavities, such as the space under a stone. They
frequently move nest sites, and the average residence time
is around two to three weeks (TSUJI 1988c). Colonies are
usually monodomous, but become polydomous under some
conditions (TSUJI 1988c). Polydomous colonies are more
frequently found in summer, when they actively forage,
than in spring and fall, when foraging is less active (TSUJI
1988c). Colony fission is inferred to occur by chance as a
consequence of the frequent migrations, which can also
occasionally give rise to polydomy (TSUJI 1988c).
Neighboring colonies of fission-founding ants are likely
to be related. An isolation-by-distance pattern revealed by
genetic markers empirically supported this prediction in
Pristomyrmex punctatus (see DOBATA & al. 2011). This
situation raises the question of nestmate discrimination:
How can these ants discriminate colony membership so
strictly (TSUJI & I 1986, TSUJI 1988b) despite the gene-
tic similarity? They may use environmentally derived chem-
icals as colony-specific labels (TSUJI 1990b). Indeed, arti-
ficial mixing of different colonies and thus of the putative
92
93
Tab. 1: A list of names previously used to describe phenotypic variants of Pristomyrmex punctatus females. * + is present,
– is absent, ? means information insufficient or non-available (GOTOH & al. 2011). ** TERANISHI (1929) wrote that the
ergatoid queens he defined can be also called pseudogynes. *** In non-cheater lineages, ocelli (if any) are always vestigial
and can be observed only by using strong light that passes through the ant's head (DOBATA & al. 2011). Therefore, it is not
surprising that many previous authors did not recognize them.
Phenotype References and used terminology
Number of
ovarioles Number
of ocelli Sperma-
theca*
Description of its occurrence
This paper,
DOBATA &
al. (2011)
WANG (2003), ITOW &
al. (1984), TERA-NISHI
(1929)**
TSUJI (1988a,
1995), SASAKI
& TSUJI (2003)
DOBATA &
al. (2009)
2 0 More than 50% of colonies consist
of only this female category. worker worker small (or nor-
mal) worker S-type
0 – (?) (no name is provided)
1-2 ?
Found in 5 - 50% of colonies in all
populations. Its frequency varies
over years. Its intracolonial propor-
tion is 0 - 30%. (no name is provided) ***
4
3 + Very rare. So far, collection is re-
peatable only in 2 populations. Its
intracolonial proportion is 0 - 50%.
ergatoid
queen
ergatoid queen
large worker L-type
labels indicated that ants can absorb labels from outside
(TSUJI 1990b). Regardless of whether the colony label is
genetic or environmental, one can infer that neighboring
colonies tend to share more similar labels with each other
than with distant colonies. Therefore, one could predict a
positive correlation between geographical distance and in-
tercolonial hostility, like the "dear enemy" phenomenon
(FISHER 1954) that is known also in ants (e.g., HEINZE &
al. 1996). However, SANADA-MORIMURA & al. (2003) ob-
served the opposite in P. punctatus: Ants strongly attacked
their neighbors but ignored ants from distant nests! The
proximate behavioral explanation is that individual ants be-
come more aggressive to a specific foreign colony because
of frequent contact with members of that colony (SANADA-
MORIMURA & al. 2003): Outside the nest, ants should more
frequently meet neighbors than members of a distant nest
under natural conditions. Such a flexible response can be
adaptive, because neighbors should directly compete for re-
sources such as food and nest sites, and thus pose a threat,
but a worker from a distant nest is less likely to recruit
colony members en masse and is therefore less of a threat.
These phenomena might be more or less general in group-
foraging ants (see also BROWN & GORDON 1997). These
mechanisms assume that ants can discriminate nestmates
from non-nestmates, but do not attack those from distant
nests. However, colony-discrimination mechanisms in P.
punctatus still largely remain to be studied.
NISHIDE & al. (2007) discussed the possible occurrence
of colony fusion in a Pristomyrmex punctatus field popu-
lation, because of the frequently observed intracolonial var-
iation in microsatellite loci. However, we wonder about its
generality for two reasons.
First, there is a frequent misunderstanding here: Asex-
ual reproduction itself does not necessarily lead to a gen-
etically homogenous colony or population unless experi-
encing a bottleneck in their specific lifecycle or in their en-
tire population dynamics. High intracolonial genetic vari-
ation may simply reflect the long-lasting large effective
population size (Ne) in each colony, because neutral theory
predicts that a (nearly-)neutral mutant allele takes 4Ne gen-
erations to be fixed in a diploid population, and the muta-
tion rates of microsatellite loci in Pristomyrmex punctatus
were estimated as ca. 10-5 per generation (DOBATA & al.
2011). In the colony's lifecycle of P. punctatus, there is
seemingly no genetic bottleneck, such as the founding stage
of a single queen, similar to the single zygotic stage of an
embryo that grows into a multicellular organism. Therefore
"somatic" mutations can build up within the colony. Note
that this situation remarkably differs from that of another
parthenogenetic species, Platythyrea punctata, in which be-
havioral interaction among workers in queenless colonies
leads to monopolization of the colony's reproduction by a
single parthenogenetic worker (SCHILDER & al. 1999, HART-
MANN & al. 2003). Interestingly, for Platythyrea punctata,
KELLNER & al. (2010) discussed that the loss of intraco-
lonial genetic diversity is recovered by colony fusion.
Second, instead, high genetic differentiation among col-
onies within a local population is maintained in Pristomyr-
mex punctatus, contradicting the frequent occurrence of
colony fusion. As measured by intracolonial relatedness
(r), genetic differentiation among colonies was r = 0.4325
± 0.0749 (DOBATA & al. 2009). If colony fusions or inter-
colonial exchanges of individuals were frequent, such high
genetic differentiation among colonies would not be ex-
pected. Alternatively, colony fusion could occur by chance
when the colonies shared the same environmentally derived
cues, but such a "hybrid" colony would soon be eliminated
by colony-level selection. In fact, NISHIDE & al. (2007)
experimentally revealed the low performance of genetical-
ly polymorphic colonies, shown as slower nest relocation
and difficulty in aggregating, as is seen in chimeric slime
molds (FOSTER & al. 2002), but this is unlike examples of-
ten discussed in other social insects in which high genetic
diversity leads to high colony performance (e.g., MATTILA
& SEELEY 2007, WIERNASZ & al. 2008). Many aspects of
the maintenance of colony identity and the colony found-
ing process remain to be studied.
Morphological castes and cheaters
In Pristomyrmex punctatus, the majority of adult females
have two ovarioles (one in each ovary). In some colonies,
females that have four ovarioles (two in each ovary) are
also found. Different authors have used various terminolo-
gies for these morphological variants in P. punctatus (Tab. 1),
Fig. 1: The body-size distributions of workers and ergatoid
queens in Pristomyrmex punctatus that were re-drawn using
the data of DOBATA & al. (2009) studied in Kihoku popu-
lation. (a) Colonies containing only workers (N[indv.] = 90;
N[colony] = 9). (b) Colonies containing both workers and
ergatoid queens with zero to two ocelli (N[indv.] = 228;
N[colony] = 14). (c) Colonies containing cheaters (ergatoid
queens with three distinct ocelli) (N[indv] = 198; N[colony]
= 10). Workers, ergatoid queens with zero to two ocelli and
cheaters are shown in white, grey and black bars, respec-
tively.
causing confusion. Focusing on the discontinuity in the
ovariole number and judging from morphology of wor-
kers and queens in related species, DOBATA & al. (2011)
proposed calling the females with two ovarioles "workers"
and those with four ovarioles "ergatoid queens" (permanent-
ly wingless queens as defined in MOLET & al. 2009). The
se of the term "ergatoid queen" is justified also by the fact
that a portion of ergatoid queens, at least those with three
ocelli (see later), have a spermatheca (ITOW & al. 1984,
GOTOH & al. 2011). These morphological conditions in
"ergatoid queens" of P. punctatus resemble ergatoid queens
of other ants including some Pristomyrmex species (WANG
2003). However, we acknowledge that ergatoid queens in
P. punctatus are exceptional, because they reproduce asex-
ually (DOBATA & al. 2009, 2011), whereas most ergatoid
queens known in other ants reproduce sexually (MOLET &
al. 2009). Like in queenless colonies of other ants, P. punc-
tatus workers keep reproducing asexually even in the pres-
ence of ergatoid queens (TSUJI 1988a, 1995). This is also
an exceptional characteristic in P. punctatus.
u
The body size of ergatoid queens in Pristomyrmex punc-
tatus is on average larger than that of workers, but with an
overlapping distribution (Fig. 1b). Most ergatoid queens
have zero to two ocelli, but some have three and are dis-
tinctly larger. Those with three ocelli are usually very rare,
but are common in some populations. So far, the collec-
tion of ergatoid queens with three ocelli is repeatable only
in two populations, i.e., Kihoku on Honshu island (DOBATA
& al. 2009, 2011) and Takamatsu (Nomoto) on Shikoku is-
land (HASEGAWA & al. 2011). Colonies containing many
ergatoid queens with three ocelli have a bimodal distribu-
tion of body size (Fig. 1c; ITOW & al. 1984, SASAKI &
TSUJI 2003, DOBATA & al. 2009), forming a striking con-
trast to the unimodal distribution of the majority of col-
onies (Fig. 1a, b). Ergatoid queens without ocelli can be
found in most populations: depending on population and
year, in up to 50% of colonies within a population, and up
to 30% of individuals (TSUJI 1988a, 1995, DOBATA & al.
2011). The average proportion of ergatoid queens without
ocelli in the entire population is usually 0.01 - 5% (TSUJI
1988a, 1995). However, a thorough dissection might detect
ergatoid queens without ocelli at low proportions in most
colonies. Colony size is not correlated with the proportion
of ergatoid queens (TSUJI 1995). Much more rarely than
those without ocelli, some ergatoid queens have one or two
ocelli that seem more or less vestigial. The body-size dis-
tribution of these queens is in between those with three
ocelli and those with none (DOBATA & al. 2009) (Fig. 2).
We do not use the ocellus as the key character discrimi-
nating castes in P. punctatus, because we wonder about its
function. In insects, ocelli function as light meters and are
involved in stabilization reflexes during flight (KRAPP 2009);
accordingly, they are often lost in non-flying insects such
as workers of many ants. So ocelli are likely to be non-
functional in ergatoid queens of P. punctatus.
Workers have no spermatheca, but ergatoid queens with
three ocelli have a spermatheca with a seemingly normal ac-
cessory gland (GOTOH & al. 2011). Much less is known
about the spermathecal condition in ergatoid queens with
zero to two ocelli, though all ergatoid queens without ocelli
examined so far (N > 200) apparently had no spermatheca
(TSUJI 1988a, TSUJI 1995, SASAKI & TSUJI 2003, DOBATA
& al. 2009).
Irrespective of the number of ocelli, ergatoid queens
share the same behavioral characteristics: They lay more
eggs than workers but rarely perform other tasks such as
nursing (SASAKI & TSUJI 2003). Ergatoid queens were nev-
er observed to forage in the laboratory (SASAKI & TSUJI
2003), although they were occasionally collected on trails
in the field (TSUJI 1988a). This suggests that ergatoid queens
94
Fig. 2: The relationship between the body size (head width) of ergatoid queens and their number of ocelli. Data are from
DOBATA & al. (2009) from the Kihoku population. Measures of cheaters (filled triangle) and non-cheaters (open circles)
were combined. Correlation was positive and statistically significant (r = 0.760, p < 0.0001).
do not follow the age-polyethism and old individuals may
continue to lay eggs. This behavioral propensity of ergatoid
queens in Pristomyrmex punctatus is normal among queens
of species in which the division of labor between repro-
ductive queens and sterile workers enhances colony per-
formance, but, as TSUJI (1995) discussed, ergatoid queens
in P. punctatus could be harmful to the colony (see also
SASAKI & TSUJI 2003) for the following reasons. Empirical
evidence indicates that having only workers is enough for
P. punctatus colonies to prosper (MIZUTANI 1980, TSUJI
1990a, 1994). More importantly, it is known that colonies
with only workers are the most productive, and the average
lifetime reproductive success of nestmates is estimated to
decrease as the proportion of ergatoid queens increases in
field colonies (TSUJI 1995). The contextual analysis ap-
plied to a field population detected no fitness peak (no sta-
bilizing selection) at a small proportion of ergatoid queens
(TSUJI 1995: tab. 4), suggesting that the idea that a low
but non-zero ergatoid queen proportion in a colony en-
hances the colony's fitness through reproductive division of
labor is not supported. Although we need more data across
populations and years on the relationship between these
individual and colony phenotypes and their reproductive
outputs, their harmful effect to the colony is evident when
ergatoid queens are genetically distinct cheaters as de-
scribed below.
In Kihoku, central Japan, we found parthenogenetic
lineages that give rise only to ergatoid queens (DOBATA &
al. 2009). We defined these lineages as cheaters, because
they can obtain a large reproductive output at the cost of
fitness of other nestmate lineages that produce workers.
Non-cheaters, or cooperators, are defined as lineages that
can become workers. We use the plural term "lineages", be-
cause as mentioned previously, in Pristomyrmex punctatus,
colonies are often genetically heterogeneous, particularly
the colonies with cheaters always contain more than one
genotype. This is owing to their social-parasitic character-
istics, i.e., cheaters can exist only with workers that be-
long to a different lineage. In other words, cheaters de-
pend on the work force of other lineages. Cheating in P.
punctatus is therefore a genotypic concept, and is a speci-
fic case of genetic caste determination. A genetic analysis
suggests that some non-cheater lineages produce only wor-
kers and other non-cheater lineages can produce both wor-
kers and ergatoid queens (DOBATA & al. 2011). The latter
cases are most likely an account of phenotypic plasticity af-
fected by larval nutrition as seen in the caste differentia-
tion of most ants (DOBATA & al. 2011). Given the castes are
mostly environmentally determined in those non-cheater
lineages, we, however, do not rule out the possibility that
some non-cheater lineages have a propensity to produce er-
gatoid queens. This is because such weak cheating is re-
ported in some patrilines of a polyandrous Acromyrmex ant
(HUGHES & BOOMSMA 2008), but is yet to be seen in P.
punctatus. Interestingly, almost all adults of the cheater
lineage (98.8%) examined so far have three ocelli. In con-
trast, ergatoid queens in non-cheater lineages have no or
more or less vestigial ocelli that can be usually recognized
only by using strong light that passes through the ant's
head. Moreover, most of them have zero to two ocelli, and
only 11.2% had three ocelli that are also more or less de-
generated (DOBATA & al. 2011). Therefore, in practice, one
can label ergatoid queens with three distinct ocelli as chea-
ters.
The monophyly of cheaters was suggested by analyses
using microsatellite nuclear DNA and mitochondrial haplo-
types in our study population in Kihoku (DOBATA & al.
2009, 2011). The existence of another cheater lineage of
independent origin is inferred from mitochondrial DNA
data in a population in Takamatsu, western Japan (HASE-
GAWA & al. 2011). However, as the rare occurrence of sex-
ual reproduction in this species has been suggested (see
later), further studies incorporating nuclear genomic data
are needed. Cheaters of the identical multiloci genotype are
found in many colonies. This occurrence, as also suggested
by a more rigorous population genetic analysis (DOBATA
& al. 2011), implies the horizontal transmission of chea-
ters. In other words, cheaters migrate to other intact colo-
nies. Nothing is known about this process, however. Such
horizontal transmission of cheaters despite the presence
of strict nestmate discrimination is not surprising, because
many social-parasitic species can evade the host's discri-
mination behavior. A parallel phenomenon is known in the
Cape honey bee (Apis mellifera capensis), in which wor-
kers can reproduce by thelytokous parthenogenesis, as does
Pristomyrmex punctatus. Some parthenogenetic worker lin-
95
eages of the Cape honey bee have become social-parasitic
and migrated among captive colonies of the neighboring
subspecies A. m. scutellata, causing mass extinction of the
host colonies (NEUMANN & MORITZ 2002, DIETEMANN &
al. 2007). One can draw an analogy also to the transmissible
cancer cells that infect and kill the host, as found in some
mammals (e.g., MURGIA & al. 2006, PEARSE & SWIFT
2006). For example, a facial cancer transmitted among Tas-
manian devils (Sarcophilus harrisii) through biting now
poses a serious threat to the persistence of the species. By
this analogy, the parasitic Cape honey bee workers and the
P. punctatus cheaters are called social cancers (OLDROYD
2002, DOBATA & al. 2009; but see KORB & HEINZE 2004
for the case of Cape honeybee).
A question arises about the cause of the difference in
the long-term consequences between these two social can-
cers; one leads to mass extinction within a decade or so (the
Cape honeybee) the other persists much longer (Pristomyr-
mex punctatus). DOBATA & al. (2011) discussed that differ-
ence in migration ability of social cancers may account
for the differential consequences. In theory, it is well es-
tablished that limited migration of parasites can contribute
to the persistence of host-parasite systems by creating the
local extinction-recolonization process. The parasitic Cape
honey bee workers have wings and thus can migrate fur-
ther than the cheaters in P. punctatus that have no wings,
which might hinder the former to persist long. Future theo-
retical and empirical studies should test this idea.
Similar to Pristomyrmex punctatus, Cerapachys biroi
also shows a variation in body size and ovariole number
among wingless females (RAVARY & JAISSON 2002, 2004),
therefore some of these can be called ergatoid queens. More
recently, LECOUTEY & al. (2010) revealed that colony
demography and nutrition affects the production of erga-
toid queens in C. biroi. However, if cheaters also exist in
C. biroi or not is yet to be studied.
Parthenogenesis and rare sexual reproduction
ITOW & al. (1984) studied chromosomes in the ovaries of
pupae of Pristomyrmex punctatus and revealed that the first
meiosis occurs normally in developing oocytes. Micro-
satellite marker loci are often heterozygous (DOBATA & al.
2009). These results suggest that parthenogenesis in P.
punctatus is a central-fusion-type automixis.
Although reproduction of this species is considered to-
tally asexual, males are occasionally found. Males are ha-
ploid (n = 12; females have 2n = 24) and have seemingly
normal sperm (ITOW & al. 1984). As already mentioned,
workers have no spermatheca, but ergatoid queens with
three ocelli have a seemingly functional spermatheca (GO-
TOH & al. 2011). Therefore, ergatoid queens might occa-
sionally reproduce sexually, although we have found no
inseminated individuals despite having dissected more than
a thousand ergatoid queens with three ocelli (T. Sasaki &
K. Tsuji, unpubl.). In the Kihoku population, there is some
mismatching between the mitochondrial DNA-based phylo-
geny and the nuclear microsatellite-based phylogeny, sug-
gesting sexual reproduction in the past leading to genetic
introgression among lineages (DOBATA & al. 2011). How-
ever, we stress that the dominant mode of reproduction is
thelytokous parthenogenesis, which is indicated by several
population-genetic indices; for example, the observed re-
dundancy of the same multilocus genotypes due to distinct
sexual reproductive events has at most a probability of
0.8%, which indicates that this redundancy is derived main-
ly from thelytokous parthenogenesis (DOBATA & al. 2011).
Multilevel selection for the short-term dynamics of
cheater and non-cheater populations
Although we previously mentioned that the long-term co-
existence of cheaters and non-cheaters in Pristomyrmex
punctatus can be described as a local extinction and im-
migration dynamics, another approach might be possible
to understand their short-term dynamics. Ross Crozier was
the first to point out that multilevel or group selection can
be a useful framework to understand the maintenance of
cooperative societies in this ant (see pages 99 - 100 in
Discussion by ITOW & al. 1984 that was written by RC).
TSUJI (1995) also discussed how the coexistence of non-
cheaters and cheaters can be explained by multilevel selec-
tion. Individual selection favors cheaters, whereas colony-
level selection favors non-cheaters. A balance of these two
forces operating in opposition may lead to coexistence at
least in the short term. Note, however, that group selec-
tion and kin selection are not alternative mechanisms but
rather different descriptive models for the same phenome-
non of evolutionary dynamics (QUELLER 1992). In fact,
multilevel selection in P. punctatus can be transformed to
kin selection. Cheaters obtain a higher individual fitness
than non-cheaters (minus c) but harm the fitness of nest-
mates (minus b). Therefore they can increase in the (meta-)
population when relatedness is low: That is, a cheater is no
more likely than by chance to interact with cheaters in the
background metapopulation. In contrast, cheaters can de-
crease when relatedness is high: That is, a cheater is more
likely than by chance to interact with cheaters in the meta-
population, leading to mutual exploitation. We are conduct-
ing long-term research to monitor the microevolutionary
process of cheater-non-cheater dynamics in the field and
to test both group selection and kin selection models (see
TSUJI 1995 for the earliest study).
Intraspecific parasitism or parasitic species?
People often wonder whether cheaters and non-cheaters are
different species, in which case prey-predator or host-para-
site ecological dynamics could provide a more appropriate
description of the phenomenon than group or kin selection.
We consider this view to be wrong for three reasons: (1)
The biological species concept is not applicable to parthe-
nogenetic organisms, and thus we have to resort to other
criteria such as phylogenetic distance. (2) Although chea-
ters and non-cheaters form separate clades in the genetic
analysis of the Kihoku population (DOBATA & al. 2009,
2011), both are nested in a deeper clade of the morpholo-
gical species Pristomyrmex punctatus among other popula-
tions of Japan. Thus, cheaters and non-cheaters in Kihoku
are phylogenetically more closely related to each other than
to P. punctatus found in Okinawa. If cheaters and non-
cheaters were regarded as separate species, many cryptic
species should be discernable within the morphological spe-
cies currently called P. punctatus. This would not be a
practical decision. (3) A model of the biological dynamics
in P. punctatus that includes two parties – one parasitic, the
other non-parasitic – might be called a metapopulation host-
parasite ecological model if the two parties are regarded as
distinct species. Or it might be called a multilevel selec-
96
tion or family-structured kin-selection model if they are
regarded as the same species. However, mathematically,
both models are in principle the same with regard to pre-
dicting the relative abundance of the two parties when one
is exploiting the other. Based on these arguments, we con-
clude that the criticism claiming that the two parties might
be different species is semantic. Regardless of the taxono-
mic status of cheaters and non-cheaters, we believe that this
system provides an ideal opportunity to test models of eco-
logical and evolutionary dynamics.
The origin of cheaters
The body-size difference between workers and ergatoid
queens (with three ocelli) in Pristomyrmex punctatus cor-
responds almost exactly to that of congeneric species with
alate queens (DOBATA & TSUJI 2009). Furthermore, rudi-
mentary wings can be seen under the cuticle of the thorax
of these ergatoid queens. This evidence suggests that erga-
toid queens in P. punctatus are real queens with arrested
development.
However, we have to stress that there is an exceptional
characteristic of ergatoid queens in Pristomyrmex punc-
tatus and in Cerapachys biroi, in addition to their asexu-
ality. Ergatoid queens in these two species reproduce to-
gether with many workers, forming a striking contrast to
other cases in which reproductive division of labor between
reproductive ergatoid queens and sterile workers is conspi-
cuous.
The other congeneric species are all known to have
queen (either winged or ergatoid) and worker castes (WANG
2003). Furthermore, males are found in many of those spe-
cies (WANG 2003), suggesting their sexual reproduction.
Therefore, asexual reproduction by workers instead of a
winged queen in Pristomyrmex punctatus is likely a derived
condition. Interestingly, P. rigidus, which is presumably
the species most closely related to P. punctatus, exhibits
a conventional social system with winged queens (WANG
2003). From the above circumstantial evidence we set out
the hypothesis that cheaters in P. punctatus arose from a
mutation that reuses the hidden developmental trajectory
to a winged queen. In other words, although the ancestor of
P. punctatus suppressed the queen trajectory, the genes en-
coding the developmental pathway are retained, and there-
fore mutations in regulatory regions can restore the path-
way (except for full development of wings). Among such
putative mutations, the ones with strong effects gave rise to
cheaters in the Kuhoku population and the ones with weak
effects lead to lineages producing both workers and erga-
toid queens. Alternatively, the following scenario is also
possible. Wing morphology of ant queens is likely an evo-
lutionary labile trait (HEINZE & TSUJI 1995, MOLET & al.
2009, PERFILIEVA 2010). Indeed, a few species of Pristo-
myrmex, such as P. africanus and P. wheeleri, have both
winged queens and ergatoid queens (WANG 2003). These
intraspecific variation indicates winglessness of queens was
evolutionary attainable also in Pristomyrmex. The ability
of thelytokous parthenogenesis might have evolved in an
ancestral species, where ergatoid queens reproduced sexual-
ly as in some other species of Pristomyrmex (WANG 2003).
Then, parthenogenetic reproduction by ergatoid queens to-
gether with young workers prevailed. Later, in some popu-
lations, parthenogenetic queens became selected for, where-
as in other populations ergatoid queens were selected against.
A comparative study across populations and across related
species, with detailed descriptions of morphology and di-
vision of labor together with phylogenetic data, is needed
to test these hypotheses.
Concluding remarks
Although the above scenarios on the origin of the unusual
reproductive biology in Pristomyrmex punctatus are largely
hypothetical, the ideas provide an interesting model system
for future studies in developmental biology and in evolu-
tionary biology from genomics to ecology.
Acknowledgements
We thank T. Sasaki and C. Peeters for discussion. We also
thank two anonymous referees for their comments. This
work is supported by a JSPS Research Fellowship for
Young Scientists (S.D.), KAKENHI (No.18370012 and
21247006 to K.T) and Mitsui and Co., Ltd. Environment
Fund (08R-B047).
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... The inheritance of behavioral phenotypes this makes possible allows for a simplification in modeling reproductive competition mathematically, since differences in fitness impact survival directly. Moreover, parthenogenetic reproduction is common in nature, and has been observed in species ranging from aphids [32], ants [12,13,35], and bees [22] to zebra sharks [14] and Komodo dragons [41]. ...
... Biologically, the parameters r u and r v can be thought of as the relative growth rate of populations u and v, respectively, when each worker is contributing to the public good at rate c. It is reasonable, then, to assume that r u = r v in general, as workers and cheaters are often phenotypically distinct and therefore have potentially different rates of growth [13,35]. Without loss of generality, and for consistency with [13,35], we will assume that r u < r v . ...
... It is reasonable, then, to assume that r u = r v in general, as workers and cheaters are often phenotypically distinct and therefore have potentially different rates of growth [13,35]. Without loss of generality, and for consistency with [13,35], we will assume that r u < r v . Reversing this inequality does not change any of the qualitative behaviors described below, only the regions in parameter space in which they are observed. ...
Article
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Through the lens of game theory, cooperation is frequently considered an unsustainable strategy: if an entire population is cooperating, each indi- vidual can increase its overall fitness by choosing not to cooperate, thereby still receiving all the benefit of its cooperating neighbors while no longer expending its own energy. Observable cooperation in naturally-occurring public goods games is consequently of great interest, as such systems offer insight into both the emergence and sustainability of cooperation. Here we consider a population that obeys a public goods game on a network of discrete regions (that we call nests), between any two of which individuals are free to migrate. We construct a system of piecewise-smooth ordinary differential equations that couple the within-nest population dynamics and the between-nest migratory dynamics. Through a combination of analytical and numerical methods, we show that if the workers within the population migrate sufficiently fast relative to the cheaters, the network loses stability first through a Hopf bifurcation, then a torus bifurcation, after which one or more nests collapse. Our results indicate that fast moving cheaters can act to stabilize worker-cheater coexistence within network that would otherwise collapse. We end with a comparison of our results with the dynamics observed in colonies of the ant species Pristomyrmex punctatus and in those of the Cape honeybee Apis mellifera capensis, and argue that they qualitatively agree.
... However, some species exhibit a continuous range of sizes from workers to queens (Molet et al., 2012;Londe et al., 2015). Fig. 2 summarizes the most detailed available data on size and phenotype for ant workers, intercastes and queens (based on studies of Myrmica rubra, Mystrium rogeri, Pristomyrmex punctatus, Technomyrmex albipes and Temnothorax nylanderi) (Brian, 1955(Brian, , 1956Tsuji et al., 1991;Tsuji and Dobata, 2011;Okada et al., 2013). Note that Fig. 2 does not depict a developmental series, but a series of adult phenotypes at varying sizes. ...
... This is a hierarchical progression: within a species, individuals with queen-like ovarioles may have otherwise worker-like features, but individuals with queen-like wings also have queen-like eyes, ocelli and ovarioles. Some flexibility exists in this hierarchy: in P. punctatus and T. albipes, the smallest class of intercastes has additional ovarioles but no ocelli, while in M. rubra, the smallest class of intercastes has an additional ovariole and partially developed ocelli (Brian, 1956;Tsuji et al., 1991;Tsuji and Dobata, 2011). This flexibility is constrained, however: to our knowledge, within a species, smaller individuals on average never possess more queen-like traits than larger individuals. ...
... Intercaste Size is estimated by body mass and/or length. Phenotypic state is estimated by either the number or the presence/absence of ovarioles, eyes/ocelli and wings, and/or by measurements of abdomen, head and thorax width (Brian, 1955(Brian, , 1956Tsuji et al., 1991;Tsuji and Dobata, 2011;Okada et al., 2013). We assume that increased body mass correlates with increased body length, and that increased ovariole, eye/ocellus and wing development correlate with increased abdomen width, head width and thorax width, respectively. ...
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Female ants display a wide variety of morphological castes, including workers, soldiers, ergatoid (worker-like) queens and queens. Alternative caste development within a species arises from a variable array of genetic and environmental factors. Castes themselves are also variable across species and have been repeatedly gained and lost throughout the evolutionary history of ants. Here, we propose a simple theory of caste development and evolution.We propose that female morphology varies as a function of size, such that larger individuals possess more queen-like traits. Thus, the diverse mechanisms that influence caste development are simply mechanisms that affect size in ants. Each caste-associated trait has a unique relationship with size, producing a phenotypic space that permits some combinations of worker- and queen-like traits, but not others. We propose that castes are gained and lost by modifying the regions of this phenotypic space that are realized within a species. These modifications can result from changing the size- frequency distribution of individuals within a species, or by changing the association of tissue growth and size. We hope this synthesis will help unify the literature on caste in ants, and facilitate the discovery of molecular mechanisms underlying caste development and evolution. © 2017 Published by The Company of Biologists Ltd / Journal of Experimental Biology.
... Parasitic lineages are not unique to social bees. So far we know of one thelytokous ant with a parasitic lineage: Prystomyrmex punctatus (Dobata et al. 2009Tsuji and Dobata 2011). P. punctatus is completely parthenogenetic, contains no winged queen caste and all females contribute to worker reproduction . ...
... Perhaps confusingly for a queenless ant, some authors refer to these females as ergatoid queens . The reproductive behavior of the cheaters is costly to the colony because the production of ergatoids instead of workers lowers the overall output of the colony (Dobata et al. 2009Tsuji and Dobata 2011). These cheaters appear to have a single origin, as microsatellite data reveals that they originate from a single colony in Kihoku, central Japan Tsuji and Dobata 2011). ...
... The reproductive behavior of the cheaters is costly to the colony because the production of ergatoids instead of workers lowers the overall output of the colony (Dobata et al. 2009Tsuji and Dobata 2011). These cheaters appear to have a single origin, as microsatellite data reveals that they originate from a single colony in Kihoku, central Japan Tsuji and Dobata 2011). Cheaters with identical multi-locus genotypes have been found in other colonies, suggesting that similarly to A. m. capensis, cheating P. punctatus workers can enter neighboring nests and parasitize them (Dobata et al. 2009Tsuji and Dobata 2011). ...
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The notion that honeybee colonies are harmonious, isolated societies in which workers selflessly sacrifice their reproductive opportunities to serve their queen has long been debunked. Like any society, honeybee colonies contain selfish individuals that pursue their own interests, or cheat, at the expense of the colony, and these individuals need to be controlled. There are numerous studies detailing the myriad ways in which selfish workers may subvert the typical dominance hierarchy of a haplo-diploid insect society. Recent studies have focussed on thelytoky, the ability to produce diploid offspring without mating, as the most significant attribute of a successful reproductive parasite. However, we argue that thelytoky is not necessary for successful parasitism, and that even arrhenotokous societies contain specialized reproductive parasites. Using A. mellifera and A. cerana as examples, we show that the most important aspects of a would-be reproductive cheat’s success are an ability to escape policing and the timing of the reproductive attempt. Finally, we show that thelytoky, while not necessary for the evolution of successful reproductive parasites, can give rise to specialized parasitic lineages and that such lineages are likely to be far more common than previously assumed.
... Reproductive workers are rare when fertile queens are present; for example, less than 1% of honeybee workers lay eggs (Bourke, 2019 and references therein). Reproducing workers have been compared to cancerous, somatic cell lineages in multicellular organisms, which also selfishly replicate at catastrophic cost to the organism (Tsuji and Dobata, 2011;Teseo et al., 2013). In multicellular organisms, constant immunosurveillance by the immune system identifies and eliminates mutant cells before they develop into cancers via tumor-specific antigens present on malignant cells (Dunn et al., 2002;Pradeu, 2013;Corthay, 2014;Feng et al., 2018). ...
... They give rise to more parasitic workers (Martin et al., 2002) and too many can cause colony collapse. This is remarkably similar to transmissible cancers in organisms, such as the facial tumors of Tasmanian devils (Tsuji and Dobata, 2011;Teseo et al., 2013). In both cases, these parasites are an asexual lineage of somatic origin that has broken free from their natal (super)organism to infect other (super)organisms (Bourke, 2011). ...
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Social insect colonies can express adaptive, organism-like design. In some cases, colonies so resemble a unique, cohesive and integrated "individual" that they are termed superorganisms. The major evolutionary transitions framework explains, via inclusive fitness theory, how new levels of biological individuality, including genes into genomes within cells, cells into multicellular organisms and organisms into superorganisms can emerge. Importantly, it highlights how at each major transition similar challenges arose and why seemingly convergent solutions evolved. One challenge faced at each transition is exploitation, caused internally by social cheaters and externally by parasites and pathogens. To overcome the problem of exploitation transitions in biological individuality required novel immune systems to maintain the integrity of newly emerged individuals. Multicellular organisms evolved an immune system while social insect colonies evolved a social immune system. In this review, we take a major transitions perspective of immunity to highlight the interdependency between the evolution of immune systems and the emergence of biological individuality. We build on the notion that superorganisms have evolved an immune system to promote the fitness of the colony. We draw parallels between the evolution of the metazoan immune system and the social immune system, and their expression as cognitive networks. Moreover, we discuss how research on other group-living species, such as family based cooperative breeders, can inform our understanding of how social immune systems evolve. We conclude that superorganism immunity is an adaptive suite of organismal traits that evolves to maximize the fitness of advanced social insect colonies, fulfilling the same function as the immune system of Metazoa.
... All workers of these ants can produce female offspring from unfertilized eggs. This eventually results in an entirely clonal colony (Schilder et al. 1999a;Tsuji and Dobata 2011;Kellner and Heinze 2011;Kronauer et al. 2012), which allows the study of division of labor without confounding variation in genetically varying thresholds for particular tasks. In two thelytokous ants, Pristomyrmex punctatus and Cerapachys biroi, individual sterility appears to be absent. ...
... All young workers lay eggs and engage in tasks inside the nest, but they cease egg laying and begin to forage later in life (Tsuji 1990;Ravary and Jaisson 2004). This suggests a simple age-based division of reproductive and nonreproductive labor, even though the picture has become more complex through the observation of selfish, egglaying intercastes (Tsuji and Dobata 2011) and experienced-based specialization in particular tasks (Ravary et al. 2007). ...
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In many species of social insects, division of non-reproductive labor is to some extent affected by age, in that younger individuals engage in activities in the nest, whereas older individuals forage. While the link between age and task is less robust than originally thought, the transition from nursing to foraging is associated with large changes in gene expression, neuroanatomy, and physiology and therefore seems largely irreversible. Here, we investigate division of labor in the thelytokous ant Platythyrea punctata. Since it forms clonal colonies, it is an ideal model to investigate the behavioral flexibility of individuals and the proximate mechanisms underlying division of labor, while avoiding confounding factors, such as variation in genotype or morphology. We found that nurses and foragers of P. punctata differ in residual life span, fat content, fecundity, and the propensity to engage in dominance interactions. However, age-based division of labor appears to be flexible: foragers can revert to nursing and egg laying, even though they appear less fecund than original nurse workers. Interestingly, the transition from foraging to nursing seemed to slow down aging and senescence.
... However, each party should pay some costs to maintain the relationship (e.g., the investment in honeydew by ant-associated aphids or scale insects 27 and ant cost for caring them 28 ). Such "cooperative" relationships can be threatened by the invasions of cheaters, such as social parasites observed in social insects 29 . Invasions by cheaters are inevitable, as a free rider can exploit the costs paid by honest participants. ...
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Symbiotic relationships are widespread in nature, but the mechanisms maintaining these relationships remain to be elucidated because symbiosis incurs a maintenance cost to each participant, which lowers its reproductive rate. In host-parasite relationships, parasites are known to manipulate the host's behavior selfishly, and there is an arms race between them. Selfish manipulations also occur in symbiosis, but the effects of selfish manipulations on symbiosis are not fully understood. Here, we show that an ant-associated aphid manipulates attending ants to receive stronger protection. Aphid honeydew regurgitated by ants contains dopamine (DA). The ants showed low aggressiveness before contact with the aphids, but it rose after contact. Administration of DA to the ants increased ant aggressiveness as the concentration increased, while an antagonist of DA inhibited this effect. The other 3 amines showed no effect on aggressiveness. A previous study showed that attending ants selfishly manipulate aphids by increasing the reproductive rate of green morph to obtain high-quality honeydew. These results suggest that mutual selfish manipulation benefits both participants and is likely to strengthen symbiosis. The selfishness of each participant may contribute to sustaining this symbiosis because their selfishness increases their long-term fitness.
... biroi (Tsuji & Yamauchi, 1995) and Pristomyrmex punctatus (Tsuji & Dobata, 2011), in which all workers reproduce and help others. While we can only speculate with regards to the evolutionary forces responsible for this secondarily evolved egalitarian behavior, Pristomyrmex punctatus shows rather low fecundities (Tsuji, 1988) and their nomadic life history may suggest important variance in resources, which is in line with our model predictions. ...
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We surveyed the behavioral properties of unusual large workers in the parthenogenetic queenless ant, Pristomyrmex pungens. The majority of colonies mostly consist of monomorphic workers, which have two ovarioles (small workers). Large workers with four ovarioles are occasionally found in some colonies. We compared the behavior of small and large workers. Large workers performed brood care less frequently than small workers and almost never foraged. We set out three hypotheses of the adaptive significance of large workers: they are (1) reproductive castes, that is, functionally defined queens, (2) major workers, such as soldiers, and (3) of a socially parasitic lineage.
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Inclusive-fitness models have been critized because they give incorrect results for cases in which fitness components interact nonadditively. However, this failure is not due to anything intrinsic to the inclusive-fitness viewpoint. It stems from an essentially quantitative genetic feature of the model, an attempt to separate fitness terms from genetic terms. A general rule is provided for determining when such a separation is justified. This rule is used to show how Price's covariance equation is related to standard quantitative genetic results and to derive quantitative genetic equations for inclusive fitness and group selection. It also shows that the group-selection model is no more general than the inclusive-fitness viewpoint. These models serve a role that is different from, but not inferior to, population-genetics models. Although they are less exact under some conditions, like quantitative genetic models in general, they provide us with measurable parameters.
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