Boomsma JJ.. Beyond promiscuity: mate-choice commitments in social breeding. Philos T Roy Soc B 368: 20120050

Abstract

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female's, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.

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, 20120050, published 21 January 2013368 2013 Phil. Trans. R. Soc. B
Jacobus J. Boomsma
breeding
Beyond promiscuity: mate-choice commitments in social
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Review
Cite this article: Boomsma JJ. 2013 Beyond
promiscuity: mate-choice commitments in
social breeding. Phil Trans R Soc B 368:
20120050.
http://dx.doi.org/10.1098/rstb.2012.0050
One contribution of 14 to a Theme Issue ‘The
polyandry revolution’.
Subject Areas:
behaviour, ecology, evolution,
theoretical biology
Keywords:
commitment, conflict, cooperation, eusociality,
cooperative breeding, monogamy
Author for correspondence:
Jacobus J. Boomsma
e-mail: jjboomsma@bio.ku.dk
Beyond promiscuity: mate-choice
commitments in social breeding
Jacobus J. Boomsma
Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15,
2100 Copenhagen, Denmark
Obligate eusociality with distinct caste phenotypes has evolved from strictly
monogamous sub-social ancestors in ants, some bees, some wasps and some
termites. This implies that no lineage reached the most advanced form of
social breeding, unless helpers at the nest gained indirect fitness values
via siblings that were identical to direct fitness via offspring. The complete
lack of re-mating promiscuity equalizes sex-specific variances in reproductive
success. Later, evolutionary developments towards multiple queen-mating
retained lifetime commitment between sexual partners, but reduced male var-
iance in reproductive success relative to female’s, similar to the most advanced
vertebrate cooperative breeders. Here, I (i) discuss some of the unique and
highly peculiar mating system adaptations of eusocial insects; (ii) address
ambiguities that remained after earlier reviews and extend the monogamy
logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect
fitness benefits driving the dynamics of (in)vertebrate cooperative breeding,
while emphasizing the fundamental differences between obligate eusociality
and cooperative breeding; (iv) infer that lifetime commitment is a major
driver towards higher levels of organization in bodies, colonies and mutual-
isms. I argue that evolutionary informative definitions of social systems that
separate direct and indirect fitness benefits facilitate transparency when testing
inclusive fitness theory.
1. Introduction
Most plants and animals are promiscuous, which implies that mate choice can
be viewed as a fluid parentage market. Darwin [1] was the first to realize that
the dynamics of this market are ultimately driven by paternity interests, which
prevail or fail depending on male– male competition or female choice. About a
century later, seminal contributions by Parker, Trivers and Eberhard [2– 4]
initiated a neo-Darwinian synthesis of sexual selection studies. The massive
work that followed in the wake of these pioneering conceptual and empirical
studies has significantly advanced our understanding of the forces that shape
the diversity of mating systems. However, we are still short of a general explan-
ation of female promiscuity/polyandry, as novel insights into the direct
(resource-related) and indirect (good genes-related) benefits of female promis-
cuity have generated at least as many new questions as those that became
answered. We are left with the notion that there is a limited set of relevant prin-
ciples, but endless variation in how they combine into specific scenarios of
male–female cooperation and conflict, each with their own fitness rewards to
the sexes involved [5– 12].
The eusocial insects with true worker castes are exceptional in having much
less mating system variation, because they do not have re-mating promiscuity
[13–15]. This is a remarkable feat, because obligate eusociality evolved inde-
pendently in the ants, bees, wasps and termites, and yet all these lineages are
characterized by mating pairs that commit for life without exception, something
that is highly unusual in other organisms. Even more peculiar, mate-choice be-
haviour is not part of social life: it normally takes place after reproductives
(prospective queens and kings/drones) have left the colony in which they
hatched and it is completed before they found a new generation of colonies.
As it turns out, the simplest form of partner commitment, strict lifetime
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monogamy, appears to have been a universally necessary,
although not sufficient, condition for allowing the evolution
of differentiated eusocial worker castes [14–17]. A review
of polyandry in the eusocial insects thus has to take the
opposite of promiscuity as its starting point and explore evo-
lutionarily derived convergent elaborations of ancestral
sexual commitment for life.
Contrasts such as this tend to inhibit intellectual exchange
between fields, as they often result in semantic inconsisten-
cies that need to be made explicit before any synthesis is
possible. For example, the special nature of polyandry in
the eusocial insects has implied that some researchers are
reluctant to use the term and prefer the more passive ‘mul-
tiple queen-mating’, which does not carry the implicit
suggestion of re-mating promiscuity. Another terminology
issue worth noting is that direct and indirect benefits mean
different things in sexual selection and kin selection argu-
ments. Instead of emphasizing benefits that females receive
from mates (see first paragraph), social evolution uses
direct benefits when referring to gene copies in future gener-
ations obtained by personal reproduction, whereas indirect
benefits refer to gene copies that come about via the repro-
ductive success of relatives. Inclusive fitness is the sum of
these two components [18,19], but it remains essential to con-
sider them separately. This is because altruistic traits can
evolve only when indirect benefits are significant because
relatedness is positive, whereas mutualism characterizes
cooperation between non-relatives, i.e. between interactants
with zero relatedness [20– 26].
The absence of the usual dynamics of re-mating has the
advantage that sexual selection predictions in the eusocial
domain are easier to formulate from first principles and often
straightforward to test by comparing mating system character-
istics across lineages in which multiple queen-mating has
evolved. The concepts used are in many ways complementary
to the logic of inclusive fitness theory [18– 20,27] and sex
allocation theory [28–30], which also predict adaptive evo-
lutionary endpoints without explicitly considering short-term
dynamics or possible constraintsthat may need to be overcome
[31]. The simplicity emanating from lifetime commitment in
eusocial mating therefore offers interesting perspectives on
both sexual selection and social evolution, provided one can
get one’s head around the idea that eusocial polyandry does
not create paternity markets, but permanent chimaeras of
nestmates sharing maternal but not paternal genes.
An explicit focus on commitment makes it also transpar-
ent that reproductive conflicts are either about whether or not
to make a commitment (e.g. which egg and sperm combine
to become a zygote or which female and male end up breed-
ing together), or about monopolizing or biasing the results of
an irreversible commitment (e.g. imprinted genes affecting
offspring provisioning, maternally transmitted genes/sym-
bionts killing male offspring or dominant breeders coercing
helpers). Much research on eusocial Hymenoptera in recent
decades has used inclusive fitness theory to explain intracolo-
nial conflicts of the biasing kind [20,32– 40], whereas
simultaneous studies of vertebrate cooperative breeders con-
centrated primarily on dominant individuals of both sexes
competing for opportunities to breed while offering subordin-
ates opportunities to help [8,41– 47], i.e. on the kind of
breeding commitments to be made and for how long. My pres-
ent focus on constrained promiscuity in the most advanced
forms of social breeding emphasizes how the absence of conflict
over parental commitment conflict has helped to forge
harmonious cooperation between parents and offspring.
Eusociality has traditionally been defined as (sub-social)
cooperative brood care between a mother and her offspring
in nests where individuals belong to reproductive castes [48].
This restricted eusociality to the vespine wasps, corbiculate
bees, ants and (as we now know, foraging) termites, i.e. to
lineages where there is no intracolonial conflict over the breed-
er role [49], consistent with Wheeler’s [50, p. 23] original
definition, which he used to emphasize the striking analogies
between eusocial colonies and metazoan bodies [15,20,25].
The term eusociality was loosened up to include all forms of
cooperative division of labour that affect lifetime reproductive
success by Wilson [51], a trend that culminated in the idea of a
‘eusociality continuum’ where degree of eusociality was prag-
matically defined by reproductive skew ([52]; reviewed by
Costa & Fitzgerald [53]). This continuum approach was criti-
cized by Crespi & Yanega [54], who argued that the
definition of eusociality should be precise and evolutionarily
informative, and thus necessarily be based on the distinct lifetime
trajectories in behaviour and reproduction that accompany the
evolution of irreversible castes. Crespi and Yanega defined repro-
ductive totipotency (the default of solitary breeding) as the
potential to express the full behavioural repertoire needed to
independently (without helpers) produce offspring with the
same abilities, and divided eusocial systems into: (i) ‘facultatively
eusocial’ where the more reproductive caste has retained totipo-
tency and the less reproductive caste has not, and (ii) ‘obligatorily
eusocial’ where neither caste has retained totipotency so that
all individuals have irreversible complementary roles. Their
obligate and facultative eusociality terminology is largely con-
sistent with ‘advanced’ and ‘primitive’ eusociality [55] and
with ‘complex’ and ‘simple’ eusociality [20,56]. However, the
advanced/primitive classification becomes ambiguous in evo-
lutionarily-derived simplifications (e.g. various ponerine ants)
and renders the bumble-bees primitively eusocial in spite of
having lost all reproductively totipotent individuals [57]. The
complex/simple categorization, based on colony size driving
multiple aspects of social complexity, allows large epiponine
wasp societies to rank above small ant societies in spite of a
fundamental difference in caste commitment.
In earlier reviews [14,15], I have elaborated the conceptual
framework of Crespi and Yanega to underline that irrevers-
ible evolution of a worker caste is the defining hallmark of
obligate eusociality and that the acquisition of this state is
a major evolutionary transition into a domain of social breed-
ing that is distinct from solitary, cooperative and facultatively
eusocial breeding combined. In the same reviews, I connected
that transition to strict and lasting lifetime monogamy of
colony parents as that condition was apparently necessary
for the evolution of obligatorily eusocial and physically dif-
ferentiated workers [16]. This resolved the critique by
Beekman et al. [58], who argued that the Crespi & Yanega
definition failed to acknowledge that reproductive domin-
ance owing to permanent morphological caste differences is
fundamentally different from reversible behavioural dom-
inance. In the same reviews, I also used the term permanent
eusociality as a synonym to emphasize the need forall individ-
uals to adopt caste roles for life and for the last totipotent
individuals to disappear before any transition to obligate euso-
ciality was completed. The monogamy approach does not
logically require the complexity of eusociality to be correlated
with either reproductive skew or large colony size [20].
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To further illustrate the generality of merging the concept
of lifetime commitment with Crespi & Yanega’s [54] evo-
lutionary informative definition of eusociality, I will explore
three complementary angles in this review. First, I will
demonstrate how peculiar the independent, evolutionarily-
derived eusocial insect mating systems are in comparison
with what we normally find in animals. The bottom line of
this section will be that one cannot just consider eusocial
mating systems as endpoints of promiscuity gradients of
which the overall principles are already generally known
from theory and data obtained for other animals. Second, I
will update arguments on why strict lifetime monogamy is
so tightly connected to the evolution of sterile workers, and
I will develop an analogous general rationale for the evo-
lution of soldier castes in facultatively eusocial systems, the
fortress defenders sensu [59]. Third, I will review how
mating-commitment logic has allowed novel insights into
cooperatively breeding vertebrates, where promiscuity is ubi-
quitous but functions as a constraint for helpers at the nest to
obtain indirect fitness benefits. Fourth, I will explore some
implications of the commitment/promiscuity approach for
understanding more general principles of multicellular life
at different levels of organization and emphasize the general
need for evolutionary informed definitions of eusociality and
cooperative breeding. A glossary of the main terminology
that I use is provided in table 1.
2. Eusocial mating separates sex and society and
establishes unusual adaptive syndromes
The TV comedy-drama ‘Sex and the City’ aptly illustrates that
issues of mate choice in our own societies always overlap
with other social interactions. It is therefore intuitively
Table 1. Glossary of the main mating system and social evolution terminology used. Sources: Boomsma [14,15], Crespi & Yanega [54], Cockburn [44], Clutton-
Brock [45], Davies [60], Emlen [41], Russell [47] supplemented and updated by various Wikipedia articles.
promiscuity: having structured or casual sexual relationships with more than one other individual. The term is also used in non-sexual contexts, always
retaining a meaning related to non-random mixing of elements. Examples are predictable or haphazard horizontal gene transfer in micro-organisms and
the regular or occasional willingness and ability to absorb influences from multiple cultural backgrounds.
re-mating promiscuity: sexual promiscuity with serial mates, so that some but not all ejaculates may compete for immediate or later egg fertilizations after
storage. The emphasis on social insects in the present review makes it necessary to define this temporal variance component explicitly, because it is
absent when queens of eusocial Hymenoptera mate with multiple males in quick succession and store multiple ejaculates jointly in a specialized
‘spermatheca’ to never mate again later in life.
chimaerism: promiscuity without a temporal component resulting in the permanent coexistence of conspecific elements that normally occur alone. Examples
are individuals with more than a single genetic population of cells owing to mergers of two fertilized eggs, the fertilization of a single egg by multiple
sperm (strictly speaking a mosaic), the merger of sibling placentas, or the asexual merger of genetically different haplotypes.
polyandry: an animal mating system in which females typically mate with several or many males in the course of their lifetime. It almost always implies
re-mating promiscuity, but longer-term relationships between a single female and several specific male partners are known in some vertebrate and
human populations and, particularly, in the multiple-mating lineages of obligatorily eusocial Hymenoptera where queen-polyandry with a specific
number of mates lasts for life because re-mating promiscuity is lacking.
polygyny: an animal mating system where single males mate with several to many females, usually in direct competition with each other through displays
of physical strength or secondary sexually selected ornaments. Otherwise similar to polyandry, but virtually absent in the eusocial insects, where the
term is used for colonies that have multiple egg-laying queens.
polygynandry: an animal mating system characterized by recurrent sexual relationships between multiple males and multiple females. Both co-breeding
males and co-breeding females may be relatives, but inbreeding is rare. Sometimes referred to as communal breeding, or (together with polyandry and
polygyny) as polygamous breeding.
cooperative breeding: a breeding system characterized by dominant breeders and subordinate helpers providing alloparental care. Helpers are either older
siblings gaining indirect (kin-selected) fitness benefits, or unrelated adults who might earn direct fitness benefits by increasing their future probability
of breeding, either independently after dispersing or by inheriting the residential nest from a more dominant breeder.
facultatively eusocial breeding: a cooperative breeding system where reproductive and helping roles are lifelong determined for a substantial fraction of the
colony membership, but where a subset of offspring retains reproductive totipotency in spite of being part of a helper cohort, so they may later inherit
the nest as dominant breeder or disperse to become dominant elsewhere. Caste roles are mostly behavioural and characterized by minor and
overlapping distributions of body size and matedness, but some lifelong subordinates may belong to a physically distinct soldier caste. When a soldier
caste is absent, there is no sharp distinction between advanced cooperative and facultatively eusocial breeding, as both combine obligate colony life
with the retention of reproductive totipotency for some fraction of the subordinates.
obligatorily eusocial breeding: a breeding system in which all individuals are either designated breeders or unmated workers/soldiers for life, and where castes are
always physically distinct and differentially adapted to a specific subset of social tasks so that colony growth and reproduction always require the
complementary efforts of all castes. This implies that no caste has retained reproductive totipotency. The evolution of a specialized worker caste ofunmated
individuals is the ultimate defining character of obligate eusociality, no matter whether a worker caste evolves after (termites) or before (Hymenoptera) soldiers.
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easier to relate to animals where sex has a social context than
to imagine the lives of ants, bees, wasps and termites where
issues of mate choice and society-building are separated in
time and space. All clades that convergently entered the obli-
gatorily eusocial domain have absolute lifetime pair-bonding,
after a brief period of mate choice between dispersing from
the natal nest and founding a colony (or sometimes joining
one as a secondary evolutionary elaboration). It cannot be
emphasized enough how exceptional this form of monogamy
is: it is as strong as the commitment of a female and male
gamete to a zygote—it implies that once you find a partner
(s)he will be your only one and even death will not part
you. A lifetime-united founding pair of diploid higher (i.e.
foraging/mound-building) termites is thus analogous with
a tetraploid zygote, whereas a standard colony-founding
ant, bee or wasp queen is a triploid analogy, owing to the
sperm of the lifetime mate in her specialized storage organ
being a haploid clone rather than an ejaculate of haploid
sperm related by 0.5 because of meiosis (figure 1a; see also
[15]). Just like a sperm cell is unable to fertilize yet another
egg, and an egg lacks the capacity to team up with another
sperm after fertilization, so does the commitment of an ob-
ligatorily eusocial queen and king/drone preclude further
sexual activity forever. Where multicellular eukaryote
bodies produce clonal adhering cell copies and sequester
germ-lines to produce new gametes, the founding ‘royalty’
of an obligatorily eusocial colony assumes a comparable
role in taking the lion’s share of producing new cohorts of
dispersing reproductives (winged virgin queens and
drones) after their ‘somatic’ colony has grown to maturity
(figure 1a; see [15] for details on worker male production
that make the germ-line analogy only approximately valid).
Sister lineages of obligatorily eusocial clades either lack
this extreme single-zygote-like colony-founding or they
are unable to universally maintain that form of lifetime
commitment later in the colony life cycle (see §3).
(a) Eusociality equalizes sex-specific variances in
reproductive success and maximizes sperm quality
Outside the eusocial insects, strict lifetime monogamy
requires that a male physically merges with the body of a
female who then stops being receptive for life, which is
very unusual and only known or suspected from a few dispar-
ate lineages such as some of the angler fish [64] and parasitic
barnacles [65]. When such strict parental commitments induce
insect offspring to become altruistic helper castes rather than
independent breeders, their relatedness can be accurately pre-
dicted because they are either full-siblings or a chimaeric
combination of patrilines (table 1) that are half-sisters to each
other (figure 1b). This predictability has been the prime
reason for eusocial insects becoming excellent test systems
for inclusive fitness theory, because these relatednesses deter-
mine the later (potential and realized) biasing-type conflicts
between colony members about reproductive allocations
[20,37,59,66].
In non-social organisms, the open-market characteristics
of promiscuous mating are major drivers of evolutionary
innovation, but also involve considerable waste in a utilitar-
ian sense. This not only concerns the evolution of male
ornaments in species where males offer no other contri-
butions to breeding efforts than sperm [67], but also the
massive numerical overproduction of sperm relative to
eggs, combined with a suite of manipulative sperm traits
for outcompeting rival sperm (reviewed in Simmons [68])
and manipulating female physiology, e.g. [69]. The males of
eusocial insects universally lack ornamental traits, which
seems a paradox because they appear to contribute only
sperm, but lifetime partner commitment resolves this as it
implies that both sexes ‘put all their gametes in the same
basket’ after ultra-brief courtship [13]. This likely explains
why termites have tandem-running as their main if not sole
potential mechanism of premating sexual selection, a process
that will tend to assort couples according to general physical
condition, because the sexes have equal interests in avoiding
an inferiorly endowed partner [70,71]. How little room preda-
tion pressure will leave for termite partners to steer coupling
away from being purely random remains to be established
(but see [70]), but the same overall logic would explain that
most mate choice in ants, bees and wasps appears to be
based on flight stamina and male receptiveness to queen
pheromones [13,72], i.e. on indices of quality that cannot be
faked [73].
When lifetime partner commitment is based on stored
sperm obtained early in life, there must be strong selection
for high sperm viability, high sperm longevity in storage,
and prudent sperm use. While promiscuous mating systems
also have their limitations in sperm production [12,74],
male gametes always vastly outnumber female gametes.
However, lifetime monogamy equalizes sex-specific vari-
ances in reproductive success and fundamentally changes
the numbers of female and male gametes that circulate in a
population (figure 1a), even though every female remains
under selection to secure the best possible sperm on the
single day when she picks her lifetime mate as a young
virgin. All sperm that survive the brief mating window are
locked away in a permanently committed production unit
(termite king) or a specialized female storage organ (Hyme-
noptera) so that eggs continue to be fertilized with minimal
waste. When multiple queen-mating evolves as a secondary
elaboration, several males breeding with the same female
implies that male variance in reproductive success drops
below female variance in reproductive success, representing
another reversal of common sexual selection practice that is
also found among the vertebrate cooperative breeders with
the highest reproductive skew [8,75,76] (see also §4).
Both long-lived queens of Atta leaf-cutting ants and Apis
honeybees have males with high sperm viability and sperma-
thecal fluids that actively enhance sperm preservation [77,78],
and both use very few sperm to fertilize an average egg
[79,80]. Higher (mound-building) termites have a founding
queen and king living side by side in a lifetime monogamous
relationship based on the regular transfer of aflagellate sperm
that has lost the capacity to move independently [71]. It will
be interesting to see whether further studies will show more
variation in sperm morphology across termite lineages, but
the currently available data seem to offer compelling indirect
evidence for strict lifetime monogamy, as sperm lacking tails
could never have evolved, let alone go to fixation, as long as
even a very low probability of sperm competition would
have remained (as in many lower termites—see §3).
Termite queens are unable to test the quality of their
mate’s sperm when committing for life, but queens of euso-
cial Hymenoptera will normally have an extra round of
selection to work with, as their first mate-choice commit-
ment coincides with males depositing sperm in the female
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bursa copulatrix [71,77,78] from where it normally needs to
actively move towards final storage in the spermatheca.
There will thus be an unambiguous male fitness benefit
in delivering highly viable sperm with optimal motility and
a consistent queen fitness benefit in evolving chemical
gradients that make sperm run the gauntlet while being
underway to the final (lifetime) storage organ, so she
can retain the best possible fraction [13,78,79]. It would
therefore be virtually impossible for eusocial hymenopteran
sperm to lose tails as queens are expected to have evolved
means to discard the least motile sperm. The extent to
which such selection processes will make a difference
depends on factors such as the size of ejaculates relative to
spermathecal storage capacity, average viability of sperm
and the cost of sperm storage [13,78– 81]. Lifetime commit-
ment between paternal and maternal gametes is therefore not
multicellular body
eusocial insect colony
metazoan
zygote (2n)
lifetime committed
royal pair (3n or 4n)
(a)
(b)
germ line
germ-line analogue
few long-lived
female gametes;
many short-lived
male gametes
male gametes out-
number female
gametes only slightly
and can be long-lived
n or 2n
2n
metazoan body chimera
slime mould asexual chimer
a
eusocial insect colony
with two patrilines
Figure 1. Gametes, zygotes, bodies, chimaeras and colonies. (a) The somatic cells of metazoan bodies are clonal copies of a single zygote to which a female and
male gamete have committed for life upon fertilization (top left), whereas standard colonies of obligatorily eusocial insects are founded by a lifetime-committed
royal pair that contributes three haplotypes in the haplodiploid Hymenoptera and four in the diploid termites (top right; see [15] for details). Such colonies consist of
individuals rather than cells (symbolized by eyespots). Queen and worker castes develop from totipotent larvae, similar to somatic cells differentiating from
totipotent stem cells, after which both castes and somatic cells become irreversibly committed to their specialized complementary functions. The lifetime-committed
royal pair is analogous to a metazoan germ line, but lineages that practise obligate eusociality have remarkable (inversed) patterns of population-wide availability
and longevity of gametes (text boxes). The inset picture of the bumble-bee Bombus terrestris (photo credit: Matthias Fu¨rst) exemplifies an obligatorily eusocial
species with colonies that are always headed by a single, once-mated queen [61]. (b) Clonal metazoan bodies (left square with blue circles) only very rarely combine
multiple cell lineages derived from more than two parents in a chimaera (or mosaic when strictly of single zygote origin; blue and red circles) (table 1). However,
Dictyostelium slime moulds (photo credit Owen Gilbert) are characterized by non-trivial frequencies of chimaeras when they produce asexual fruiting bodies [62] and
eusocial insect colonies have repeatedly evolved chimaeric structures when queens became multiply mated. The inset picture of Lasius niger exemplifies an ant
species whose colonies are always headed by a single queen, but where some fraction mates with two or three males rather than with a single male [63], giving a
chimaeric colony kin-structure of full-sibling patrilines that are half-siblings to each other.
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decided at insemination or fertilization, but at the final sto-
rage of sperm, provided sperm is used randomly after
storage (see §2b).
(b) Three mating system syndromes, constrained sperm
competition and female control
In eusocial insects the distinction between pre- and post-
copulatory sexual selection is applicable only with significant
modification. There obviously is a pre-copulatory mate-
choice phase, but it involves a very restricted set of mate
quality cues (see §2a), and the entire process ends with a
monogamous commitment, in termites even well before the
first copulation takes place [70,71]. However, in the eusocial
Hymenoptera, there are two very distinct post-copulatory
phases, separated by sperms’ irreversible entry into the sper-
matheca. As long as lifetime monogamy prevails, there will be
no sexual selection in either of these, as sperm of haploid males
are clonal so that any differential storage can be based only on
non-genetic criteria [13,79]. Ejaculates of different males will
interact only in those hymenopteran lineages where multiple
queen-mating evolved as a secondary elaboration (cf. [16]). A
logical corollary of the monogamy hypothesis is, therefore,
that during the evolution of a lifetime-committed worker
caste there was never any mixing of sperm, so that all mechan-
isms of ejaculate conflict between insemination and final sperm
storage had to evolve de novo and independently after second-
ary switches to facultative or obligate multiple mating had
occurred [15].
The window for ejaculate competition is brief and very
distinct; so the null hypothesis to be rejected is that we
expect females to have evolved control over sperm compe-
tition. Once permanently stored, there will normally not be
opportunities for preferential sperm use during egg fertiliz-
ation many months or even years later, as such biasing
would either require empowering mechanisms for clones of
stored sperm derived from specific males (patrilines) or
female fitness incentives for allowing anything else than
‘fair raffle’ sperm use when fertilizing eggs [13,79,82]. Selfish
patrilines [83,84] might have evolved ways to overcome this
form of queen control, but otherwise one would expect to
see complete sperm mixing if queen fitness increases with
increasing genetic diversity of workers [85]. Thus, when
paternity differences across worker cohorts in the same
colony appear to occur, it is important to check whether
this might reflect differential larval growth rather than tem-
porary variable sperm use owing to incomplete sperm
mixing [82,83,86].
The increasingly convincing evidence for the secondary
nature of multiple queen-mating across the obligatority eu-
social Hymenoptera [16,85,87,88] also reinforced that
facultative and obligate multiple-mating appear to be
mutually exclusive lineage-specific syndromes forming chi-
maera colonies (table 1 and figure 1b). Each of these mating
systems tends to be typical for entire genera or higher-level
clades [85,87] rather than being shifting alternatives in some
mating-frequency continuum. Thus, ants, eusocial bees and
eusocial wasps tend to have either 100 per cent single
mating, or some mixture of colonies headed by a monandrous
or mildly polyandrous queen, or 100 per cent (usually high)
polyandry of queens [16,85,87] (figure 2). There is now reason-
able consensus about the evolution of obligate multiple mating
having been driven by benefits related to enhanced genetic
diversity among workers (proposed by [89,90] and reviewed
by [85,87,91–93]), but what has driven the convergent evol-
ution of facultative multiple mating has remained enigmatic.
It is tempting to speculate that this mating system evolved to
allow females to correct suboptimal first inseminations, but
considerable research effort will be required to unravel the
interaction between sperm transfer, mating plug efficiency
and female sperm storage responses, which seems a tall
order as almost no eusocial species with facultative multiple
mating are known to mate under laboratory conditions.
Because re-mating promiscuity (table 1) is absent, all
brood cohorts throughout a polyandrous queen’s life will
be fertilized by the same set of fathers that managed to get
their sperm stored on the single day that they mated with
her in quick succession. This implies that any competition
between ejaculates for storage would have to take place in
the provisional storage phase, as continued competition
after storage will affect lifetime fecundity of queens and
thus be selected against [13,94]. Recent work has shown
that seminal fluid proteins play a key role in hostile interactions
me
5
4
3
2
1
exclusive single mating:
ancestral mating system
maintained in most
extant lineages
facultative multiple
mating: both singly
and multiply mated
queens reproduce
successfully
obligate multiple mating:
only multiply mated
queens reproduce
successfully
Figure 2. An illustration of the categorical, rather than continuous, variation
in mating systems of facultatively and obligatorily eusocial insects. Most
extant species appear to have retained the ancestral exclusive single mating
habit [16,85,87,88]. Facultative and obligate multiple mating are distinct
secondary evolutionary endpoints that have convergently evolved in multiple
lineages (often entire genera or higher order clades) of ants, vespine wasps
and corbiculate bees, but apparently never in the termites. Frequency
distributions of the genetically effective number of matings (m
e
) across
species (the standard used by social insect researchers as it is inversely related
to nest-mate relatedness; [87]) are therefore not unimodal but trimodal
(illustrated by the non-overlapping ranges of red dots). Facultative multiple
mating is likely to represent a mixed evolutionarily stable strategy as both
singly and multiply mated queens can successfully found colonies and
reproduce. Obligate multiple mating implies that mature full-sibling colonies
are essentially never found, which must imply that directional selection
quickly took these lineages through an inevitable ancestral phase of
facultative multiple mating, presumably driven by genetic diversity benefits
[85,87]. The selection factors that stably maintain facultative multiple mating
are unknown. Obligate multiple mating is only found in the obligatorily
eusocial Hymenoptera, but facultative multiple mating occasionally occurs in
facultatively eusocial lineages, and re-evolved in a number of obligatorily
eusocial clades [16,85,87,88].
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between ejaculates during this phase [77,78,95], as accessory
gland secretions of monandrous fungus-growing ants and
bumble-bees were as supportive to own sperm and alien
sperm (as expected when ejaculates have no evolutionary his-
tory of ever interacting), whereas respective polyandrous sister
lineages of leaf-cutting ants and honeybees appear to have a
combination of generally supportive and specifically hostile
seminal fluid interactions with alien sperm [78].
As inseminated ejaculates are highly viable and new
inseminations become impossible soon after the first because
queens lose receptivity, eusocial sperm competition is
expected to be a closed endgame where males have little
power, and the queen decides both the number of ejaculate
participants at the start (when she stops mating) and the
completion of sperm admission into the spermatheca (when
she discards the remaining sperm). Queens thus provide a
bursa copulatrix arena to let a fixed number of ‘gladiator
ejaculate armies’ perform a self-thinning process before the
survivors are admitted to potential reproductive status in
her storage sanctuary. It thus seems almost unimaginable
that queens would not have close to 100 per cent control
over sperm competition, a situation that is highly unusual in
promiscuous mating systems where ejaculates enter serially.
In such cases, ejaculates can be adjusted by males depending
on the likely reproductive value of current versus future
matings, and accessory gland proteins can affect female physi-
ology in more selfish ways because males will not breed with
the same female again [69,96,97]. Given that eusocial poly-
andry evolved convergently in multiple lineages of ants,
corbiculate bees and vespine wasps [15,16,85], and each time
from strictly monogamous ancestors, it will be interesting to
see whether the molecular mechanisms that mediate seminal
fluid hostility in different genomic backgrounds also have
elements of functional convergence.
Once sperm of different males has become permanently
stored, all male manipulation is expected to cease, because
from now on the Monty Python ‘Meaning of Life’ logic that
‘every sperm is sacred’ will apply [13]. This is because
mother queens of mature colonies are more likely to be
sperm limited [94] in their total lifetime reproductive success
than egg limited, because they can continue to lay eggs as
long as they have workers to feed the hatching larvae, but
they cannot continue to fertilize eggs to replace short-lived
workers when their spermatheca is empty. Recent work has
shown that sperm-limited lifetime reproductive success
seems indeed likely for queens of Atta colombica leaf-cutting
ants [80] and that spermathecal fluid of these ants somehow
terminates hostile interactions between seminal fluid and
genetically different sperm, as expected when queens
‘consider’ permanently stored sperm as an invaluable com-
modity that is no longer to be depreciated by any form of
male–male competition [78]. This encouraging match
between expectations and first empirical analyses deserves
further testing in other polyandrous ants, bees and wasps
to see whether complications in the general logic of these
evolutionary inferences might emerge.
As internal fertilization is a universal trait in many ver-
tebrate and invertebrate lineages, there are many ways in
which sperm must have been selected to avoid being attacked
by the female immune system. As long as sperm tenure after
insemination is transient because females frequently re-mate,
one would expect female immune defences to contribute to
the gauntlet-running test-bed were that to enhance the
probability of the most suitable sperm reaching the eggs.
However, queens of the eusocial Hymenoptera, and long-
lived ant queens in particular, are lifetime pregnant with a
large clump of non-self sperm, and selection should thus
have ensured that not even a little harm is done to these
sperm cells once they have entered the spermatheca. It
would be interesting to know how the transcriptomes and
proteomes of known immune genes in spermathecal fluid
differ from those in control tissues. Termites could offer an
interesting parallel test, as their queens have sperm storage
organs that are regularly refilled by re-mating with the
same colony king so that storage remains brief [71] and
female immune genes could thus impose adaptive ejaculate
thinning before queens use sperm.
3. Lifetime monogamy as universal ancestral
state for obligate eusociality
In a previous review [14], I summarized the arguments for
strict lifetime monogamy being the most obvious general
factor to facilitate rare irreversible transitions to obligate eu-
sociality in a diagram that I reproduce here in a more precise
version (figure 3). The parsimony inference was that if the
establishment of irreversible caste phenotypes is most likely
to happen in a long and gradual evolutionary process of infin-
itesimally small steps, then there would be no better general
facilitating condition than the strict lifetime monogamy that
we know has remained the commonest form of family organ-
ization throughout extant clades of the obligatorily eusocial
insects (figure 2). Eusociality is favoured most effectively if
the product of the benefits of lifetime helping (b) and average
lifetime relatedness to nest-mates (r
n
) exceeds the product of
the lifetime costs of helping (c) and relatedness to offspring
(r
o
). Hamilton’s rule thus reduces to b/c.1 when both rela-
tednesses are always 0.5 on average, whereas the necessary
b/c-ratio threshold will always have to be higher when
parental promiscuity reduces sibling relatedness to values
below 0.5 on average. Hence, very slight efficiency benefits
will allow the transition to obligate eusociality under lifetime
monogamy as long as they are long-term consistent (which
will rarely be the case), but less so under even low degrees
of serial monogamy or promiscuity. The prediction has
now been formally substantiated by comparative data [16],
confirming that all known independent evolutionary develop-
ments towards obligate eusociality appear to have been
realized by ancestors going through a prolonged lifetime mon-
ogamy window (straight arrows in figure 3) and not by
crossing the white/grey diagonal elsewhere, even though
that would be allowed by Hamilton’s [18,19] rule (see also
[14]). However, facultative eusociality plays out along the
diagonal, but in separate regions depending on whether it
is derived from lifetime monogamy (possibly including
a soldier caste; §3b), or from advanced cooperative breeding
where colony life is based on recurrent turnover of dominant
female and male breeders (§4). The cooperative breeding tri-
angle is not formally distinct from the other white areas
towards the left as social systems move in and out of these
over evolutionary time.
Strict lifetime monogamy as a necessary condition for
making the transition to obligate eusociality with altruistic
(true) workers is fully consistent with defining obligate eu-
sociality based on all individuals having lost reproductive
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totipotency [14,54,58] (table 1). However, necessity does not
imply sufficiency. There are a number of animal lineages
with lifetime monogamy that never had life cycles or ecol-
ogies that would make the b/cratio in Hamilton’s rule
favourable for offspring to become sterile workers rather
than (at least potentially) independent breeders. What the
monogamy hypothesis posits is that those sub-social lineages
that have managed to make the transition had lost re-mating
promiscuity before any b/cbenefits could vector them over
into the obligatorily eusocial domain. This is consistent
with many primitively eusocial systems approaching mon-
ogamy (cf. [16]) but without having achieved this 100 per
cent, as for example the halictid bees maintaining low frequen-
cies of facultative multiple mating and replacement of founder
queens by daughters, the wood-dwelling lower termites being
unable to avoid colony mergers, and the paper wasps where
auxillary foundresses occur in many species (see §3a,b).
The monogamy hypothesis works the same way for haplo-
diploidy and diploidy, because 0.75 relatedness to diploid
supersisters and 0.25 relatedness to haploid brothers gives an
average relatedness of 0.5 similar to diploid full-sibling related-
ness under ancestral 50/50 sex allocation [14,15]. This is
convenient as Trivers & Hare [99] decisively refuted the
notion that haplodiploidy would have given the Hymenoptera
a higher likelihood of evolving eusociality just because of 0.75
relatedness to full sisters. Recent years have seen a renewed
interest in modelling the possible effects of haplodiploidy
without ignoring the compensating 0.25 relatedness to
brothers. The results have been mixed [100,101], so for now
it seems most reasonable to assume that haplodiploidy can
either be favourable or unfavourable for the evolution of
eusocial castes, depending on assumptions.
(a) Major transitions require irreversibly completed
developments: principle and examples
The monogamy hypothesis is incompatible with obligate
eusociality being the tail end of some eusociality continuum
[52]. Extant species are either obligatorily eusocial or they are
not in the original meaning of the term (truly social). If they
are, they have physically distinct queen and worker castes
with complementary social roles without which a colony
can never grow to reproduce [50,54,58], or they are derived
from ancestors that must have had such obligate castes (e.g.
workerless inquiline ants and ants with gamergate repro-
ductives, see §3a(ii)). Almost having made a transition to
obligate eusociality therefore means not having made it, as
a genetic trait that has not gone to fixation remains easily
reversible. To realize the transition, both lifetime monogamy
and (slight) b/cbenefits needed to be long-term consistent,
so that there was enough evolutionary time for gene com-
plexes which normally secure unrestricted expression of
reproductive totipotency to accumulate so many deleterious
mutations and deletions when expressed in a worker pheno-
type that reversal becomes a practical impossibility. This is
why becoming obligatorily eusocial is a major evolutionary
lifetime relatedness ratio (rn/ro)
varying degrees of re-mating promiscuity lifetime parental commitment without re-mating
lifetime benefit–cost ratio (b/c)
1
0.1
2
0.5
0.2
0.1 1 100.2 0.5 2 5
solitary/communal breeding cooperative breeding
inbreeding
mating
before/without
dispersal
mating
after
dispersal
obligate eusociality
eusocial inbreeding
low
parental
turnover
high
parental
turnover
Figure 3. The monogamy window (filled black circle in the centre) towards obligate eusociality in the parameter space provided by Hamilton’s [18,19] rule as
it plays out over the entire lives of altruistic helpers, with the log ratio of relatedness to nest-mates (r
n
) versus offspring (r
o
) on the y-axis and the log ratio of
benefits (b) versus costs (c) of helping on the x-axis. The grey triangle represents all parameter combinations where Hamilton’s condition for reproductive altruism
(br
n
.cr
o
; here plotted as log(r
n
/r
o
).2 log(b/c)) is fulfilled across the lifetime of offspring, so that permanent worker castes are expected to evolve and be
maintained. Breeding systems are written in the different parts of the diagram and the white/grey presence or absence of promiscuity is highlighted in the text
boxes at the top. Straight arrows illustrate that both inclusive fitness logic [14] and available evidence [16] indicate that transitions towards obligate eusociality
were achieved via the narrow monogamy window (black circle) in the centre of the diagram, and not by crossing the white/grey diagonal elsewhere. Bent arrows
illustrate that non-eusocial mating systems are expected to be solitary or communal when parental turnover is high and cooperatively breeding when parental
turnover is low. Similarly, mating before (possible) dispersal or after dispersal will determine whether a breeding system will be inbred or outbred, but no social
systems based on inbreeding are known to have produced obligate eusociality. The ellipse overlapping with the black circle approximates the combination of r
n
,b
and cvalues that likely apply in fortress defenders that have often evolved altruistic soldier morphs, but rarely true worker castes. Figure modified after Boomsma
[14] and Cornwallis et al. [98].
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transition, but living in societies or colonies is not [14,15].
The logic that an evolutionary transition completes a devel-
opment without being part of it is similar to, and
complements, Gardner & Grafen’s [102] argument that
there is a fundamental difference between group selection
and group adaptation, because adaptations for the exclusive
benefit of the group do not arise gradually, but only after
lower-level selection has all but disappeared. Defining euso-
ciality based on morphologically distinct castes [14,53,54,58]
(table 1) is thus more evolutionarily informative than using
pragmatic definitions.
(i) Polistine wasps: obligate eusociality remains to
be demonstrated
Recent studies have underlined the fundamental significance
of the distinction between eusociality and cooperative breed-
ing. Leadbeater et al. [103] confirmed (for a review of earlier
evidence, see [15]) that helpers of Polistes wasps do not
always irreversibly commit to their behavioural caste roles.
They may gain considerable indirect fitness benefits when
the dominant breeder is a relative, but females of the same
cohort in the same population may also help non-relatives,
because such nests offer a favourable probability of obtaining
direct fitness benefits by acquiring breeder status later in life.
These alternative tactics coexist side by side, showing on the
one hand that there are significant indirect fitness benefits for
the average helper in the population, and on the other hand
that many helpers are likely to obtain direct fitness benefits as
later breeders. The same study showed that a small minority
of offspring females opted out by mating and overwintering
early to join the pool of spring breeders rather than complet-
ing their life cycle in the same season, i.e. they continued to
behave as univoltine, reproductively totipotent solitary breed-
ers. Phenotypic plasticity of this kind is characteristic for
cooperative breeders, but inconsistent with hard-wired obli-
gate eusociality where worker-helpers will never obtain the
direct fitness of a dispersing breeder. It seems likely that
similar social dynamics apply in all Ropalidini and related
lineages of independent-founding paper wasps [104,105].
The Epiponini are the sister clade of the Polistini and have
from several to many mated and egg-laying females per nest,
considerable body size variation in some species, and colony
founding by swarming (reviewed by Hunt [105] and Jeanne
[106]). Although relatedness is high when female reproduct-
ives are produced [107,108], this complex type of sociality
seems to challenge the monogamy hypothesis, as this scen-
ario would require a clade ancestor with 100 per cent
colony founding by a single once-mated queen. However,
the enigma would disappear if it could be shown that epipon-
ine worker roles have remained reversible as a study by
Strassmann et al. [109] indicates (making them advanced
cooperative breeders similar to Polistes), or that the basal
branches of their phylogeny would have lifetime monog-
amous parents and solitary colony founding (which might
make them an independent transition to obligate eusociality
if worker castes in at least some species would prove to be
hard wired). The social evolution status of the crown group
of the vespid wasp phylogeny thus remains ambiguous. This
is not because lineages do not all have obligate colony life,
but because it remains to be proved that caste phenotypes out-
side the obligatorily eusocial vespine (yellowjacket) wasps are
distinct for all individuals, rather than phenotypically plastic
with reproductive totipotency always being one of the avail-
able options for some fraction of each cohort. Hunt [105]
provides an update review on our current knowledge of
wasp social biology, emphasizing various intriguing forms of
phenotypic plasticity in polistine wasps, but neglecting the
key question of whether anyof these wasps has become obliga-
torily eusocial in the sense of permanent caste commitment. As
long as some fraction of each cohort are ‘false workers’ in the
termite sense of remaining uncommitted as young adults, the
transition towards obligate eusociality has not been made,
and polistine wasps would thus remain cooperative breeders
or facultatively eusocial in the sense of [54].
(ii) Ants with cooperative breeder traits: distinct from
non-eusocial cooperative breeders
The ants are monophyletic and obligatorily eusocial through-
out [110,111], but some basal lineages seem to have reverted
to forms of cooperative breeding [49,112]. However, careful
inspection of the details shows that this is not really the
case in spite of a number of suggestive convergent analogies.
It appears that these ants are all derived elaborations of obli-
gate eusociality that emerged via secondary selection against
independent colony founding by winged, newly mated and
dispersing queens while favouring alternative modes of
reproduction based on the division of existing colonies
[113–115]. Such evolutionary developments have happened
in all subfamilies of ants [115] and normally start with
some form of coexistence between independent and depend-
ent colony founding where, respectively, queens mate
during dispersal or before/after colony division [113].
Further evolutionary change may then result in the complete
loss of the ancestral state so that obligate colony division
by fission or budding remains and lineages become fully
characterized by ergatoid queens lacking flight muscles and
wings [115].
In three subfamilies of ants (Amblyoponinae, Ponerinae,
Ectatomminae), selection against having only queens that dis-
perse on the wing occurred in species where the workers had
not irreversibly lost their spermathecae (i.e. they had retained
the potential to express spermatheca genes in a morpho-
logically distinct worker caste phenotype [116]). In some
species belonging to these lineages, the winged queen caste
was completely lost and replaced by gamergates (sexually
reproducing workers), consistent with the idea that once
selection for colony division as an alternative mode of repro-
duction starts, cheaper (i.e. smaller, leaner and non-flying)
female reproductives evolve as replacements [115]. These
derived lineages may ultimately restore single-female (mono-
gynous) breeding, even though the ancestors that initiated
the loss of flying queens could only do so by having multiple
gamergates per nest [114]. Gamergates are much less fecund
than ergatoid queens, so colonies headed by gamergates are
small, particularly in the most derived lineages that tend to
converge on a single gamergate breeder per colony [114].
A major general difference between ergatoid queens and
gamergates is that the former retain the exclusive caste-
specific monopoly of mating and reproduction, whereas in
gamergate species, the workers must establish dominance
hierarchies to regulate who ends up mating and laying eggs.
Gamergate societies have thus secondarily acquired the coop-
erative breeder trait that a single ant phenotype can change
caste role behaviourally by mating and advancing to breeder
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status. However, they never re-evolved other key traits
that characterize cooperative breeding, such as re-mating
promiscuity (vertebrates) and the ability to found colonies
alone after long distance dispersal (polistine wasps).
Gamergates can only change to breeder roles early in adult
life [115], whereas such changes tend to be associated with
later adulthood in vertebrate cooperative breeders. These evo-
lutionarily-derived eusocial breeders thus never regained
reproductive totipotency.
(iii) Ancestral versus derived inbreeding: termites, ambrosia
beetles and social spiders
Recent phylogenies suggest that there have likely been two or
three independent origins of true workers in the termites
and that these transitions were always associated with the
adoption of central place foraging from one-piece-nesting
(wood-dwelling) ancestors [117–119]. However, only one of
these lineages—the higher termites—realized a significant
radiation and ecological footprint, indicating that making
the transition to obligate eusociality does not always start a
major lineage development. Further work will be needed to
clarify the constraints that prevented the foraging Mastoter-
mitidae and Hodotermididae from carving out their own
major eusocial niche space comparable to the Termitidae.
That non-foraging lower termites are essentially coopera-
tive breeders (albeit with a differentiated soldier caste,
see §3b) has recently been underlined by evidence that
larvae and nymphs of several genera provide little indirect-
fitness-driven brood care, but rely on the likelihood of later
advancement to breeder status, either in the same nest or
after dispersal to find a mate and found a new colony
[120–122], not unlike the Polistes wasps discussed above.
Few species have been investigated, but it appears that
these lower termites still have some sperm motility, consist-
ent with experiencing a non-zero probability of promiscuity
later in life [71,123 – 125]. All this fits the term ‘false workers’
that some authors have used to characterize these, at best,
conditionally altruistic workers [126,127].
A further notion worth emphasizing is that association of
relatives, either as outbred siblings with recent co-ancestry or
as inbred offspring of a local group of parents, appears not to
have ever produced a single obligatorily eusocial lineage
(hence no straight arrow in the top left of figure 3; see also
[14]). Recent work on ambrosia beetles [128] has shown
that inbred offspring help, both as larvae and adults, but
(sib)mate and predominantly disperse to found new burrows,
illustrating that high sibling relatedness combined with mon-
ogamy does not have to produce eusociality. Although some
(dead wood) burrows of ambrosia beetles may last for two or
three generations, most deteriorate sooner, precluding in-
direct fitness gains for later offspring that would fail to
disperse after some variable period of helping—quite similar
to wood-dwelling lower termites running out of food. Tell-
ingly, the only known ambrosia beetle that has apparently
evolved true workers is diploid and digs its burrows in live
Eucalyptus trees, so they can last for many years [129].
Another African species of apparently outbred platypodine
ambrosia beetles is known to found colonies biparentally in
live trees and may represent earlier stages of eusociality
that can be compared with sympatric sister lineages living
in dead wood where burrows are shorter-lived [130,131].
Analogous arguments for inbred social spiders, which
never produced obligatorily eusocial lineages, have been
given by Boomsma [14] (see also [132] for a recent review
of their comparative biology). It thus appears that all
known obligatorily eusocial lineages have arisen sub-socially
from lifetime-committed outbred parents.
Both in the lower and the higher termites, sib-mating
offspring of founders may inherit nests or become the
reproductives of nest fragments that bud off [118,127,133].
However, it is important to note that such incestuous replace-
ment breeders do not violate the non-promiscuity rule, as no
fresh blood enters the colony, so they merely recombine the
genes of their lifetime monogamous colony-founding parents
[14,15]. The same is true when queen succession happens
by automictic parthenogenesis as is known to occur in
Reticulitermes (Rhinotermitidae) [134]. This underlines that
termites with true workers could apparently never evolve
secondary elaborations of obligate eusociality such as mul-
tiple mating and adoption of offspring queens mated to
unrelated males, as the eusocial Hymenoptera did. This
suggests that any form of genetic chimaerism to secondarily
diversify the founding tetraploid zygote analogue (table 1
and figure 1b) would likely have corrupted established
true worker pathways. This may well be because the termi-
tes lack pupal metamorphosis to developmentally (and
irreversibly) connect differential larval growth trajectories
with specific adult caste phenotypes (see also §3b). In ants,
obligate or predominant inbreeding only evolved in a few evo-
lutionarily-derived lineages [115]. In sum, inbreeding appears
to be a severe constraint for monogamous breeding systems
to evolve obligate eusociality (see also §3b), but it can evolve
as a derived condition once obligate eusociality has become
established. The upper part of the small ellipse through the
monogamy window and the arrow in the eusocial inbreeding
rectangle of figure 3 illustrate this distinction.
(iv) Swarming and the possibility of worker interference
during mating
As in the epiponine wasps discussed in §3a(i), swarming and
colony fission have also (convergently) evolved in obliga-
torily eusocial clades such as honeybees, stingless bees [57],
army ants [93] and a few other lineages of obligatorily eu-
social insects (reviewed by Cronin et al. [135]). These
developments are always derived, i.e. are elaborations on
already advanced forms of obligate eusocial life. They thus
represent secondary losses of the ability of single queens to
found colonies independently [113,115,136]—one of the hall-
marks characterizing the origin of obligate eusociality where
sex and society became separated. This makes these swarms
fundamentally different from the swarms in epiponine wasps
that always contain multiple egg layers [106]. Although the
later evolution of multiple mating and adoption of non-
sib-mated daughter queens (including the ergatoid and
gamergate elaborations of this type of colony kin structure)
did not restore re-mating promiscuity, so swarm-founding
did not remove the principle of queens mating alone and with-
out the interference of workers (e.g. honeybees and stingless
bees). The army ants are probably the exception that proves
the rule, as queens are permanently wingless and mate with
multiple unrelated males in their own nest, after the old
queen and approximately half of the workers have left the
colony [93,137]. This is fully comparable to honeybee colony fis-
sion and virgin-queen mating shortly thereafter, except that the
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mating swarm has been moved ‘indoors’ [93,138]. Attempts to
re-mate old queens later in life can be artificially induced, but
without leading to sperm transfer [137], confirming that lifetime
commitment between initial mating partners prevails.
The army ants are one of the few evolutionarily-derived
eusocial mating systems where society (i.e. workers) may
affect mating success of virgin queens [138], similar to
Cardiocondyla and some unicolonial ants [13,139]. However,
there is no evidence that workers do in fact actively and inde-
pendently interfere with their sisters’ mate choice. Tellingly,
the only known case of male-killing by workers affecting
sister mate-choice in Cardiocondyla ants needs chemical mark-
ing by rival males of the male victims to occur [140], which
makes the behaviour an extended phenotype of the compet-
ing males themselves. The separation of sex and society
that appears to be the leading principle of the obligatorily
eusocial domain would suggest that it is most likely that
the virgin army ant queen herself decides which of the avail-
able males she will mate with (i.e. that workers would not
prevent specific copulations), but that the worker collective
might function as a gauntlet-running matrix decreasing
the likelihood that less fit or too genetically similar males
may reach the virgin queen. Such a process would then be
reminiscent of female reproductive tracts providing physio-
logical hurdles for sperm on their way to eggs or storage
organs. It is a pity that the field biology of army ants
makes it very difficult to test hypotheses of this kind.
(v) Obligatorily eusocial bumble-bees and facultatively eusocial
halictids and allodapines
The recent literature on bees suggests that obligate eusociality
has evolved twice rather than once in the corbiculate bees
[57], with the honeybees and the bumble-bees plus stingless
bees representing separate origins. This is gratifying as it
reconciles many ambiguities (discussed in [57]) and also
clearly separates the clades in terms of mating systems,
with the honeybees having obligate multiple mating through-
out and the bumble-bees and stingless bees having single
mating or sometimes facultative multiple mating (figure 2;
[16,85]). While bee researchers tend to classify bumble-bees,
some halictid bees and some allodapine bees as primitively
eusocial [57,141], the evolutionarily informative definitions
advocated here (table 1) separate these clades, emphasizing
that the differences between bumble-bees and stingless bees
evolved in the obligatorily eusocial domain as they are both
derived from a single ancestor that passed through the mon-
ogamy window towards obligate eusociality, whereas none
of the halictine and allodapine bees has done so.
Some allodapine bees have morphological differentiation
reminiscent of queen and worker castes [142], but neither of
the two studied species has lost their last totipotent individu-
als, indicating that their sociality has remained facultative.
Their remarkable social systems evolved in dry habitats
where the lifespan of limiting nest sites came to exceed
individual lifespan, so that nest inheritance became a major
kin-selected force allowing offspring to become larger
replacement queens. The tendency towards facultative eusoci-
ality in halictid bees evolved ca 35 Ma ago [141], but sister
lineages often reversed to solitary breeding, as expected when
eusociality has not become obligate, similar to the most
advanced allodapine bees having sister species with simple
colonies [142]. This is very different in the bumble-bees that
only lost the worker caste in some lineages that secondarily
became social parasites—similar to the vespine wasps that are
always categorized as advanced (i.e. obligate) eusocial.
(b) The evolution of soldiers
Previous versions of the monogamy hypothesis [14,15] have
remained incomplete by hardly addressing the evolution of
soldier castes. This is not a serious omission in eusocial
clades such as ants where soldiers always arise as derived
additional worker castes and typically in lineages with
large colonies and substantial size dimorphism between
queens and standard-size workers [143 – 145]. Morphologi-
cally distinct soldier castes have not been documented for
any facultatively or obligatorily eusocial vespid wasps
[105,106], consistent with worker– queen dimorphism being
small; cf. [143]), and the only example in eusocial (stingless)
bees appears to be associated with defence against an unu-
sually effective robber-bee [146]. However, soldier castes in
termites have evolved before true workers [147], and a
number of other invertebrate lineages have in recent years
been singled out as eusocial based on the existence of altruistic
soldiers (figure 4). To be consistent with the monogamy
hypothesis, such soldier castes should have evolved in single
foundress families with, at least early in family life, maximal
relatedness among offspring, but in ecological settings that
will never select for true (foraging) workers (figure 4).
As outlined by previous authors [59,117,127,148,155,156],
nesting within an abundant food resource is a powerful pre-
dictor for the initiation of sociality outside the Hymenoptera.
No indication has been obtained that any of these fortress
defenders [59] would not have monogamous colony-found-
ing, and in the better studied species strict lifetime
monogamy (or clonality as in aphids and polyembryonic
wasps) appears to be upheld (see references in figure 4).
The question therefore is why most of these lineages have
not evolved true workers after evolving soldiers, and the
answer appears to be that there has never been selection
for specialized phenotypes operating outside the nest [156].
The aphids and thrips have nothing to gain from foraging
unless they can gain access to a neighbouring gall, which
would compromise genetic homogeneity and the inclusive
fitness of residents and thus solicit vicious defence. They
are also constrained in expanding their galls, so the number
of broods remains low [148,150], similar to the ambrosia bee-
tles nesting in dead wood [128]. Snapping shrimp obtain
their food from the sponge tissues around their nests or pas-
sively via water flowing through [157]. Food is therefore not a
limiting factor, so that foraging outside the nest never pays
off in any of these lineages. Similar logic would appear to
apply for the false worker castes in termites. Living inside
the food resource, referred to as ‘bonanzas’ by previous
reviews [156,158], implies that immatures can largely feed
themselves, so that prolonged provisioning of younger sib-
lings by older nest-mates may not be a major driver of
social evolution. This appears to be consistent with recent
findings that brood care is mostly focused on prophylactic
hygiene measures, both in lower termites [122] and in
wood-dwelling ambrosia beetles [128] where larval social be-
haviour appears focused on waste concentration, whereas
adults are waste disposers and defensive gallery blockers.
The basal termite lineages have strictly monogamous
colony founding, but face competition later in life from
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conspecific founding pairs colonizing the same log
[120,122,123]. As the full-sibling larvae of these founding
pairs start eating out cavities and gallery systems, colonies
are bound to meet and compete for feeding and nesting
resources. While this often allows adjusted coexistence in
nests that remain separate, colonies may also merge, which
will end with one of the breeding pairs being killed (usur-
pation) or one of each pair being eliminated, resulting in
re-mating promiscuity of the surviving breeders [125,126].
It is this higher than zero statistical likelihood of experienc-
ing unrelated (after having been usurped) or half-sibling
(after one surviving parent re-mates) nest-mates later in the
colony cycle that the monogamy hypothesis predicts to be a
non-starter for transition towards obligate eusociality with
a true worker caste. However, as strict monogamy is always
intact early in the colony cycle, there is no reason why
altruistic soldiers should not evolve and be maintained
by kin selection when pressure from natural enemies
is substantial. Phylogenetic data [119] are consistent with
the non-zero probability of re-mating promiscuity in lower
termites precluding that true workers could evolve until ter-
mites stopped living in their food, spaced out sufficiently to
avoid colony mergers, and thus secured continuing full-sib
relatedness [117,120,147].
Overall, it appears that the evolution of defence castes in
termites is generally compatible with the monogamy hypoth-
esis. Lower termite soldiers tend to be relatively few and be
produced early enough to maximize the likelihood that full-
siblings are protected when colonies are most vulnerable
because they are still small [120,126,127]. Soldiers have to
be sclerotized to be effective, which comes at the expense of
losing the ability to moult back into an uncommitted nym-
phal stage [120]. They thus represent irreversibly altruistic
individuals, but their social systems are not obligatorily eu-
social as long as the pool of large immatures remains false
workers, i.e. transient developmental phenotypes that can
be abandoned when conditions change [120]. Major ques-
tions that need to be addressed in termites are whether the
soldiers of lower termites are primarily meant to defend colo-
nies against predators or competing conspecifics in the same
log, and whether their production is mostly a function of
relatedness or the level of imminent threat.
The Synalpheus sponge-dwelling shrimps are yet another
invertebrate example of fortress colony defence (figure 4).
first soldiers appear last totipotent phenotypes disappear
wood-eating cockroaches
monogamy
biparental brood care
solitary relatives facultative eusociality obligate eusociality
alpheid shrimps
lifetime monogamy
clonal polyembryonic wasps
clonal gall-forming aphids
single gall-foundress
many clonal phenotypes
gall-forming thrips
single gall-foundress
full-sibling families
ambrosia beetles
single burrow-foundress
full-sibling families
wood-dwelling termites
lifetime committed soldiers
brood care less important?
snapping schrimps
all individuals have claws
clonal polyembryonic wasps
lifetime committed soldiers
spiteful to non-clone mates
social gall-forming aphids
lifetime committed soldiers
only in long-lasting galls
social gall-forming thrips
lifetime committed soldiers
reduced soldier fertility
ambrosia beetles
larvae and adults help before
dispersal; no soldiers needed
central place foraging termites
lifetime committed soldiers and workers
advanced nest building and brood care
has not evolved
no need for foraging outside sponge
has not evolved
ephemeral resource base
has not evolved
ephemeral resource base
has not evolved
ephemeral resource base
has not evolved
ephemeral resource base
Austroplatypus incompertus
lifetime committed workers?
predictable and lasting resource base
Figure 4. The evolution of defence altruism in invertebrate clades that live in their food and where fortress-defence requirements [59] have produced soldier
morphs, but only rarely true workers. The ambrosia beetles are either diploid or haplodiploid and may or may not be inbred [128]. Obligate eusociality was not
selected for, except in a single Australian species that nests in live wood and which represents an independent lineage not closely related to the cooperatively
breeding ambrosia beetles [128,129]. The fixed diameter of entrance tunnels would never select for soldier morphs because normal sized individuals can block
tunnels. In the haplodiploid gall-forming thrips soldiers appear to be irreversible phenotypes, but remain able to reproduce [148,149]. In the gall-forming aphids,
clonality makes direct/indirect fitness distinctions irrelevant, similar to germ-line and somatic cells in metazoan bodies having identical interests, and many
alternative phenotypes already exist in the non-social aphid lineages that have produced social species [150]. In the polyembryonic wasps, soldiers evolved to
eliminate offspring of unrelated cofoundresses and clonality ensures that their evolution was relatively unconstrained [151,152]. Snapping shrimp feed on the sponge
they live in or on food items carried by water currents, so there has never been selection for specialized foragers or nest builders [153,154]. The termites have
irreversible soldier phenotypes in the wood-dwelling lineages and lifetime-committed workers (in addition to soldiers) in derived lineages that no longer live in their
food [120,122].
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A recent study by Duffy & Macdonald [154] has shown that
the alpheid shrimp clade in which complex social family
structures evolved is monogamous throughout, but excep-
tional in having small body-size and non-dispersing larvae
that hatch directly into crawling juveniles, rather than into
swimming dispersers. Life-history and phylogeny data for
these shrimp are thus consistent with monogamy being a
necessary condition for transitions towards advanced social
organization. It is important to note, however, that the snap-
ping shrimp have no permanently differentiated castes, as all
individuals have fighting claws and the female breeders
merely tend to become the largest individuals in the
sponge as colonies grow [153], similar to naked mole rats
(see §4) and some allodapine bees [142]. As argued above,
there will never be selection for worker foragers leaving the
nest, so snapping shrimp will remain advanced cooperative
breeders for whom defence of nest sponges is essential but
where future research may show that there is little brood
care altruism similar to the lower termites so far investiga-
ted [120,122]. The social spiders (§3b(iii)) passively acquire
food similar to the snapping shrimp and they inbreed as
do some of the ambrosia beetles, but have never evolved
specialized castes for either defence or foraging [132].
A final example is found in the polyembryonic wasps,
where soldier morphs eliminate non- or lesser relatives to
secure the fitness gains that their mothers intended when
laying an egg in a host of fixed size [151,152]. These wasps
are particularly interesting because a modelling study [159]
has indicated that female soldiers (which tend to be the
majority) are primarily adaptive for mediating sex ratio con-
flicts, whereas male soldiers eliminate competing unrelated
individuals, suggesting that selection forces during the
origin and later elaboration of soldier morphs may have
been different.
The arguments of this section are mostly an update of
previous attempts to functionally classify categories of
social organization in insects and vertebrates [49,59,118],
but I believe that the monogamy criterion adds useful
insights into the most likely evolutionary pathways that
produced fortress defending life histories and constrained
their further social evolution. As illustrated by the ellipse
superimposed on the monogamy window in figure 3, most
fortress defenders have been unable to evolve away from
the log(r
n
/r
o
)¼2log(b/c) diagonal to irreversibly enter
the obligatorily eusocial domain in spite of monogamous
parents. The approach taken here makes it explicit that
‘fortress defenders’ and ‘life insurers’ (sensu [59]) almost
never share direct common ancestry. The comparative data
(figure 4) suggest that the termites are the only major excep-
tion to this rule, and even in this lineage the emergence of
obligate eusociality was a rare event with only a single
major radiation with true workers. It is tempting to speculate
that evolving obligate eusociality from fortress defending
ancestors was facilitated by the termites decomposing
wood and other organic matter (with the help of endosym-
bionts), so that the resources they could obtain outside their
fortresses were not too radically different from what the
walls of their fortresses used to provide. The other likely
exception is the platypodid ambrosia beetles that never
needed morphologically distinct soldiers to block their bur-
rows, but have likely progressed to obligate eusociality in
one, and possibly a few more, species that independently
specialized on exploiting live trees (figure 4).
4. Vertebrates were never monogamous enough
to have evolved obligatorily eusocial lineages
The monogamy hypothesis was developed from the idea that
promiscuous mating reduces, all else being equal, the indirect
fitness benefits that older siblings obtain from adopting roles
as helper at the nest. Following the first comparative analysis
by Griffin & West [160], this topic was briefly explored for
vertebrates in Boomsma [14], suggesting that cooperative
breeding should, all else being equal, be characterized by
lower degrees of parental re-mating promiscuity than solitary
breeding. Recent comparative analyses have shown that par-
ental re-mating indeed explains a large proportion of the
variation in cooperative and solitary breeding in birds and
mammals. Cornwallis et al. [98] assembled a dataset of 267
bird species with known breeding systems and showed that
the likelihood of cooperative breeding is higher when parents
are more monogamous, both across and within extant
species, and that the evolution of monogamy normally pre-
ceded the evolution of cooperative breeding, whereas the
loss of cooperative breeding followed rather than induced
higher parental promiscuity. Similar results were obtained
for mammals by Lukas & Clutton-Brock [161], analysing
comparative data from 57 species.
(a) Interpreting the comparative data
The consistent support for monogamy affecting the pro-
bability of cooperative breeding across the birds and
mammals is remarkable because mammalian helper roles
differ in many ways from those in birds. The analyses con-
firm that relatedness incentives are a crucial selection force
for cooperative breeding when all three Hamiltonian vari-
ables (r, b, c) vary continuously and can compensate each
other, in contrast to the obligatorily eusocial insects that
evolved from ancestors where average relatedness to siblings
was always 0.5, so that the r-term cancelled out of Hamilton’s
rule, i.e. stopped being a variable determining helper com-
mitment ( figure 5a; see also §2aand [14]). The results
obtained [98,161] reinforce that cooperative breeding is not
a distinct domain of social evolution by itself, as lineages
enter and leave this form of sociality over evolutionary time
(the bent arrows to and from the triangle in figure 3) and
some fraction of the helpers always retain reproductive
totipotency [15,54].
Monogamy in birds and mammals is never as absolute as
in the eusocial domain. At its vertebrate extreme, long-lasting
serial monogamy without cuckoldry all but eliminates prom-
iscuity in the sense of sperm competition, but yet maintains
some long-term unpredictability of parenthood at established
nests. While obligate eusociality arose in insects that die with
the only sexual partner with which they ever mate on a single
day early in life, serial monogamy implies that individuals
will have some likelihood of producing half-sibling families
over their lifetime rather than only full-sibling families. This
difference between strict and serial monogamy explains that
no bird or mammal lineage has ever crossed the white –
grey diagonal towards the obligate eusocial domain in
figure 3 or the gap between the red ellipse and the black
dot in figure 5a. The continued presence of some degree of
promiscuity will retain the standard market dynamics of
mate choice that the eusocial domain has principally aban-
doned and replaced by lifetime commitment (even when
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polyandry evolved later). Thus, the Hamiltonian condition
for helping is not completely fulfilled for even the most
advanced cooperative breeders, as there will always be
some initially subordinate individuals who will change
reproductive roles during their lives to become dominant
breeders that are themselves dependent on helpers. This
implies that part of the red ellipse of figure 5aalways remains
below the diagonal, precluding that individuals become
b/c
solitary
breeding
strict lifetime
monogamy
communal and
cooperative
breeding
eusocial
breeding
maximal
skew
minimal
skew
r
n
/r
o
125
1.00
0.50
(a)
(b)
0.20
fortress defenders
advanced cooperative breeding and facultative eusociality
obligate eusocial breeding
Figure 5. The fundamentally different Hamiltonian parameter space in which cooperative breeding, facultative eusociality and obligate eusociality operate. (a)As
before (the present figure amplifies the bottom right of figure 3), the axes represent the ratios of lifetime relatednesses to younger nest-mates (r
n
) versus offspring
(r
o
) and the efficiency benefits (b) and costs (c) associated with offspring staying to help parents reproduce. Advanced cooperative and facultatively eusocial breeders
have condition-dependent helping for a substantial fraction of subordinates. They remain close to the diagonal and cannot move beyond this line as their breeding
populations retain a number of subordinate individuals whose ability to become dominant breeders later on (i.e. moving back to the other side of the diagonal) is
actively maintained by selection (red ellipse). The origin of the insect clades that evolved obligate eusociality after passing through the strict monogamy window
(figure 3) is now represented by the filled black circle at the top left. In practice, this circle does not overlap with the red ellipse because a lasting transition from
minimal promiscuity by serial monogamy to strict lifetime monogamy is very difficult to make and thus is not part of continuous variation over ecological time (see
text). As in figure 3, the fortress defenders of figure 4 (note this panel only covers the outbred ones) can be conceptualized as a small black ellipse extending
downwards along the diagonal. The obligatorily eusocial insects have evolved irreversibly ‘rewired’ developmental pathways for at least two distinct caste trajectories.
In this process, they lost the last reproductively totipotent individuals while retaining relatedness ratios (r
n
/r
o
) of exactly unity so they could slowly consolidate the
benefits of eusocial life (i.e. the b/cratio becoming larger as illustrated by the blue ellipse). Once no single individual no longer had the possibility to change caste
later in life (i.e. all individuals had become lifetime committed to a single caste), secondary elaborations such as polyandry (multiple queen-mating) and polygyny
(adopting newly mated daughter queens back in the nest) could, but often did not, evolve to further increase the b/cratio. This reduced the relatedness ratio, but
without there being an obvious overall correlation between relatedness and b/cratios (blue arrows). Measuring b/cratios is impossible in the obligatorily eusocial
domain, because there is no longer a joint currency of independent personal reproduction, as there is in the cooperative and facultatively eusocial breeders who
remain under selection to continuously evaluate the Hamiltonian inequality and adjust their individual commitment decisions accordingly [103,162,163]. (b) Possible
variation in reproductive skew when evolution proceeds from solitary to cooperative breeding and vice versa, and in some lineages to eusocial breeding as an
irreversible transition. Colours are as in figure 5a, but now given below the x-axis. Reproductive skew is maximal (¼1) per definition both in solitary breeders and
during the origin of obligate eusociality. This implies that lower degrees of reproductive skew (the grey space between the curve and the maximal skew ¼1 line) in
the obligatorily eusocial and cooperative breeding domains have evolved in fundamentally different social contexts (with and without sterile workers; without and
with promiscuity; without and with the option for long distance dispersal when fitness options in other groups are superior) and thus cannot be directly compared
(see text for details).
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permanent members of castes that behaviourally and
morphologically cement reproductive division of labour
instead of keeping it plastic. In a companion paper,
Lukas & Clutton-Brock [164] show that mammalian mon-
ogamy has led only to kin-selected cooperative breeding
when there was a realistic possibility for increasing litter
size of the dominant breeding female. This is an interesting
finding as studies of Seychelles warblers that normally lay a
single egg per clutch have shown that helpers rely primarily
on direct rather than indirect fitness benefits [165].
Both Cornwallis et al. [98] and Lukas & Clutton-Brock
[161] explicitly excluded communal and other forms of
social breeding (table 1) that either do not offer indirect fit-
ness benefits to helpers at the nest or make such benefits
ambiguous because alternative direct fitness interpretations
are possible. This indicates that traditional broad definitions
of cooperative breeding are at best partly evolutionarily
informative, similar to pragmatic definitions of eusociality,
and that clarity would be gained by considering vertebrate
communal and polygamous breeding systems (polyandry,
polygyny, polygynandry; table 1) separately when they lack
indirect fitness incentives for offspring to stay as helpers at
the nest. The comparative studies by Lukas & Clutton-Brock
[161,164] further emphasize that cooperative breeding in
mammals always involves a single dominant female and
that transitions towards cooperative breeding have never
occurred in lineages where groups of multiple females breed
communally, often with a single dominant male. Communal
(polygynandrous) breeding tends to create positive matrifilial
relatedness, because males disperse and compete for access to
multigenerational groups of females. However, this mating
system needs continuous reinforcement by the promiscuity
market forces of sexual selection and will inevitably imply
that subsequent offspring of a focal female are at least partly
half-siblings rather than full-siblings. Cooperative breeding
in mammals being based on commitment between a single
dominant female and her mate(s) is gratifying as it offers a
conceptual connection across the dividing line between the
cooperative and eusocial breeders in figure 3, and across the
gap between the red ellipse and the black dot in figure 5a—
but only as long as one realizes that the transition from
serial- to lifetime monogamy is very difficult to make.
(b) Inbreeding, reproductive skew, domain comparisons
and modelling
The bird and mammal data seem to provide little support for
inbreeding having been an important driving factor in ver-
tebrate social evolution, suggesting that the most social of
all mammals, the naked mole rat, is a special rather than a
generally representative case. Its ecology has similarities
with the fortress defenders living in their food [59,156]
(figure 4), suggesting that inbreeding is a derived trait to
secure nest inheritance for some generations, rather than a
precursor of further social evolution, consistent with the
Damaraland mole rat having independently evolved outbred
cooperative breeding but with smaller colonies [166]. Cat-
egorizing the naked mole rat as a specialized (obligate)
cooperative breeder is consistent with a scheme proposed
by Clutton-Brock [45]. The mole rats and other specialized
cooperative breeders such as the Kalahari meerkats would
also fit my definition of facultative eusociality (table 1), but
that is merely a semantic issue as facultative eusociality and
advanced cooperative breeding are both part of an evolution-
ary continuum (the white areas in figure 3). The most
cooperative edge of that continuum is characterized by coop-
erative breeding being obligate (i.e. no reproductive success
can be realized by individuals that are not part of a social
group), but that is fundamentally different from all individu-
als having distinct lifetime caste roles. The crucial point is
that the mole rats are not obligatorily eusocial, just like the
Polistes wasps where obligate colony life has not allowed
the evolution of permanent individual caste fates either.
Both for caste/helper roles and for inbreeding, we thus see
coherent general patterns emerge. Across the vertebrates
and the invertebrates, there is a fundamental distinction
between variably committed ‘helpers’ (cooperative and facul-
tatively eusocial breeding) and the lifetime-committed
‘workers’ that allow further caste evolution beyond adult
phenotypic plasticity (obligate eusociality only). Similarly,
we know of no examples, in either vertebrates or invert-
ebrates, of inbreeding (often combined with female biased
sex allocation) having vectored lineages across the point of
no return towards obligate eusociality with true workers
(figure 4), independently of there being inbreeding
depression or outbreeding depression [132,167–169].
Reproductive skew is a useful measure of biased repro-
ductive allocation in communal/cooperative and eusocial
breeders [170,171], but the ways in which skews are achieved
in these two domains are fundamentally different, because
there was maximal skew per definition in the monogamy
window separating them (figure 5b). This underlines once
more that attempts to capture all variation in a eusociality
continuum [52] cannot be conceptually defended. It is inter-
esting to note that advanced vertebrate cooperative breeders
with high reproductive skew may have more than a single
male breeding with the dominant female [8,75], which
implies that the overall variance in reproductive success
among females may become higher than among males, simi-
lar to what happens when queens of eusocial Hymenoptera
evolve multiple mating (§2).
Separating obligate eusociality, on the one hand, and soli-
tary, communal, cooperative and facultatively eusocial
breeding, on the other hand, makes it easier to see both the
commonalities and the fundamental differences between
these domains, which Costa & Fitzgerald [53] refer to as
merely ‘eusocial’ and ‘social’. The crucial difference is that
the former have irreversibly evolved away from the diagonals
in figure 3 and figure 5a, and the latter have not because they
retained some fraction of reproductively totipotent indi-
viduals. The obligate eusocial domain offers interesting
questions about skew in paternity [172] and maternity
(reviewed in [170,171]), but options to leave the nest to
become an independent breeder are absent, while they
remain possible in cooperative breeding and facultative euso-
ciality. Acknowledging these domain differences appears
more fundamental than clade-specific differences within
domains. For example, cooperative breeding in vertebrates
is rare outside the mammals and birds, but the fishes offer
some exceptions of which the cooperatively breeding cichlids
are best studied. Helping in cichlids is driven by defence
against predators and by a fluid combination of direct and
indirect fitness benefits [173–175]. It is straightforward to
acknowledge the breeder/helper similarities with Polistes
wasps or fairy wrens that can help at parental and alien
nests [103,176] while taking into account that cichlid
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predation risks are exceptionally high. However, similar com-
parisons with queens of ants or workers of honeybees,
stingless bees or bumble-bees are less meaningful because
reproductive totipotency no longer applies.
Only few explicit attempts have been made to formally
model the idea that monogamy enhances social evolution,
either in the form of eusocial workers or as facultative helpers
at the nest. The first such model was produced by Charnov
[177] and specifically addressed the likelihood of male help-
ers. More recently, Nonacs [178] suggested that the effect of
monogamy was at best minor and could also easily be oppos-
ite, i.e. promiscuity favouring the evolution of helping, even
suggesting that inclusive fitness logic is inadequate for
making predictions about the origin of eusociality. However,
a model by Gardner et al. [101] confirmed the importance of
monogamy and a combination of inclusive fitness, and indi-
vidual-based modelling by Leggett et al. [17] was also
generally supportive, similar to a model by Fromhage &
Kokko [100]. These somewhat mixed results are not surpris-
ing as the assumptions of the models matter, consistent
with the idea that monogamy is a necessary but not sufficient
condition for the evolution of altruistic helping [14,15]. For
example, it would seem essential that models consider con-
ditions that would favour altruistic helping to become
fixed, as the complete loss of totipotency is decisive for
making the transition towards obligate eusociality, not the
frequency of helping genes in a socially polymorphic popu-
lation. Furthermore, nest inheritance should either be
excluded or allowed to be lost, as this direct fitness benefit
does not apply during the hypothetical monogamy window
towards obligate eusociality and only re-evolved in some
lineages as a later elaboration of obligate eusociality.
5. Promiscuity across the domains of
social evolution
The monogamy hypothesis makes an explicit connection
between paternity uncertainty of fathers and the probability
of indirect fitness for offspring. Its logic and the tests current-
ly available explain that: (i) major evolutionary transitions
towards obligate eusociality could be made only when
there was no paternity uncertainty at all, (ii) the eusocial
domain has a number of very peculiar adaptations that
make sense only in the light of re-mating promiscuity
having been completely abandoned, (iii) the frequency of
re-mating promiscuity is an important driver for cooperative
breeding outside the obligate eusocial domain, determining in
considerable measure the position of species in a continuum
between solitary (including communal and polygamous)
breeding and advanced cooperative breeding or facultative
eusociality (see table 1 for definitions). The former tends to
generate little or no indirect fitness benefits from social inter-
actions, whereas the latter normally has such indirect fitness
benefits but without precluding the realization of substantial
direct fitness benefits later in life and (iv) provisioning castes
(workers) that collectively and irreversibly forego mating to
express morphologically specialized phenotypes are restrict-
ed to the separate, obligatorily eusocial domain, because
the presence of this caste is the defining trait for obligate
eusociality (table 1) [14,50,54,58].
The evolutionarily informative definition of eusociality
used here allows a direct and explicit connection between
lifetime commitment of mating partners and the evolution of
eukaryote multicellularity from single zygotes [15,20,25,50,
179], a type of conceptual coherence that pragmatic definitions
of eusociality lack. Drawing this analogy emphasizes that there
are only a handful of independent major adaptive radiations
for each of these transition categories (plants, animals, fungi
and two lineages of algae versus ants, higher termites, vespine
wasps and two lineages of corbiculate bees), but considerably
higher numbers of sister lineages that have remained ‘faculta-
tive’ [15,180]. Facultative and obligate eusociality belonging
to different domains of social evolution captures this funda-
mental difference, whereas implicit [51] and explicit [52]
definitions based on reproductive skew do not. The approach
pursued here follows Bourke [20] in acknowledging that
processes of social evolution have origins (formations), elabor-
ations (maintenance) and transitions (transformations) to
higher levels of integration, but differs in emphasizing the
irreversibility (sensu [181]) of known transitions towards eu-
sociality and eukaryote multicellularity from the moment
that these states became obligate.
Using commitment criteria helps to generalize social evo-
lution theory building on the major transition groundwork
laid by Buss [182], Maynard Smith & Szathma
´ry [183] and
Queller [25,184]. The major transitions approach emphasizes
that there are clearly separated domains of social evolu-
tion, where the same inclusive fitness principles apply [20]
but where the outcomes are different. In this view, major tran-
sitions are singularities [14], i.e. significant discontinuities in
the omnipresentgradients inwhich life manifests itself. Suchdis-
continuities give different meaning to established processes, and
promiscuity isan example case in point: it isabout unpredictable
parentage in eukaryotes, about horizontal gene flow in prokar-
yotes, mostly about gene– culture interactions in humans, and
it is absent in the obligatorily eusocial domain (table 1). Singular-
ities also reconcile apparent contradictions: at the dawn of
eukaryote multicellularity, the sequestering of germ-lines can
both be interpreted as enforced [182] and altruistic [25], but clon-
ality makes these mechanisms two sides of the same coin. At the
origin of obligate eusociality, the evolution of worker castes may
be interpreted as parental manipulation or altruism, but lifetime
monogamy makes these explanations equivalent [136,185].
Extensions towards obligate mutualistic cooperation
between species appear to follow suit. They are egalitarian
transitions [25,184] and the most successful and irreversible
ones appear to be based on lifetime commitment between
the minimal possible number of lineages required for a
specific symbiosis (see also [23,24,182]). We see this in multi-
cellular eukaryotes having a single lineage of mitochondria
and plasmids, and in the most conflict-free ectosymbioses
being based on rearing single clones of symbionts per host
or host compartment, in spite of ample population-wide
genetic variation. An illustrative example concerns fungus
farming by insect societies, where colonies of attine ants
acquire their fungal symbiont by vertical transmission and
actively protect it against secondary competition with similar
but not identical clones [186–188]. Colonies of fungus-grow-
ing termites (except for a few derived exceptions with vertical
transmission) acquire their lifetime association with a single
fungus-garden clone via horizontal transmission and positive
frequency-dependent propagation of strains inside colonies
so that only one of them prevails and becomes impossible
to invade [189]. These convergent farming mutualisms have
lifetime commitment in common, not transmission mode,
rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120050
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type of promiscuity threats or evolutionary history. Also in
mutualistic interactions, it might therefore be useful to dis-
tinguish between systems where lifetime commitment
happens without exception and with considerable comple-
mentarity of function after the mutual loss of reproductive
totipotency (analogous to the black dot and blue ellipse in
figure 5a) and a separate gradient of other commitments
(reminiscent of the red ellipse in figure 5aand thus varying
in promiscuity and mutual benefits). Frank [190], Sachs
et al. [191], Foster & Wenseleers [21], Leigh [24] and
Scheuring & Yu [192] offer general reviews and models to
address the stability of the latter types of mutualism.
Perhaps not surprisingly, the emphasis on commitment
rather than promiscuity reinforces an explicitly ‘female’ per-
spective on the propagation of life with an egg committing
to a single sperm, a queen committing to a single mate,
and insect colonies hosting single clones of particular sym-
bionts. All of these are principally life-long symbioses
between unrelated genetic elements that create complex
chimaeric (super)organisms. The committed unions are egali-
tarian in the sense of Queller [184], but driven by ‘female’
enforcement of exclusive ‘male’ commitments so that inter-
ests become joined and symmetrical. In all cases, a larger
number of possible ‘male’ elements compete for becoming
part of such commitment: many sperm per egg, multiple
males per female, several fungal clones per social insect
colony. The ultimate success criterion of commitment is the
absolute exclusion of other ‘male’ elements from the symbi-
osis—a process with which we are familiar when thinking
about sexual selection, but much less so when considering
polyspermy [193] or host– symbiont conflict over symbiont
mixing [194–196]. The exclusion of promiscuity is almost uni-
versally successful in fertilization, but only partially so across
interspecific symbioses, and rarely in mating systems. Here,
promiscuity normally prevails so that individuals operate in
fluid markets [197], where commitments last only until
‘male’ elements are displaced by competitors or ‘females/
hosts’ can pick better alternatives.
Lifetime commitment or promiscuous lack thereof is also
of relevance when considering the extent to which social con-
structions can be considered to have (super)organismal
properties. In a recent review, Queller & Strassmann [198]
arranged a representative selection of widely varying forms
of sociality along two axes, one representing the extent of
cooperation and the other the degree of conflict, to identify
which of these are most organismal, i.e. combine high
degrees of cooperation with low conflict. It is interesting
to see that their organismal quadrats for multicellular
individuals and symbioses mostly contain examples of life-
time-committed partnership, whereas their respective
‘society’ quadrats of high cooperation combined with high
conflict tend to coincide with cooperative or advanced
communal breeders and promiscuous symbioses. Their com-
parative approach exposes some of the inconsistencies in the
way the field has traditionally used terms such as ‘society’
and ‘superorganism’, but the correspondence of their results
with the lifetime commitment approach advocated here is
encouraging. It confirms that a productive way to conceptu-
alize colonies of obligatorily eusocial species is to
acknowledge that they are ‘organismal’ per definition and
underway to ‘full’ or ‘super’ organismality as possible end-
point (see also [20,23,66]). It would seem a logical general
hypothesis to expect that promiscuity, either in mating or in
symbiont acquisition, will preclude two-partner interactions
from crossing an organismality threshold when hosts have
unitary growth (metazoans), but that hosts offering modular
compartments for symbiont colonization might realize
lifetime-committed chimaeras with multiple lineages of the
same symbiont without jeopardizing overall organismal
integrity [199–202].
I thank Boris Baer, Peter Biedermann, Susanne den Boer, Andrew
Bourke, Tim Clutton-Brock, Charlie Cornwallis, Andy Gardner, Ju
¨rgen
Heinze,Judith Korb, Christian Peeters, Tommaso Pizzari, Dustin Ruben-
stein, Michael Schwarz, Shannon Smith, Michael Taborsky and Stu West
for discussion and comments on earlier versions of the manuscript, and
the Danish National Research Foundation for funding.
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