Ecological Drivers of Non-kin Cooperation in the Hymenoptera

Abstract

Despite the prominence of kin selection as a framework for understanding the evolution of sociality, many animal groups are comprised of unrelated individuals. These non-kin systems provide valuable models that can illuminate drivers of social evolution beyond indirect fitness benefits. Within the Hymenoptera, whose highly related eusocial groups have long been cornerstones of kin selection theory, groups may form even when indirect fitness benefits for helpers are low or absent. These non-kin groups are widespread and abundant, yet have received relatively little attention. We review the diversity and organization of non-kin sociality across the Hymenoptera, particularly among the communal bees and polygynous ants and wasps. Further, we discuss common drivers of sociality across these groups, with a particular focus on ecological factors. Ecological contexts that favor non-kin sociality include those dominated by resource scarcity or competition, climatic stressors, predation and parasitism, and/or physiological constraints associated with reproduction and resource exploitation. Finally, we situate Hymenopteran non-kin sociality within a broader biological context by extending insights from these systems across diverse taxa, especially the social vertebrates. Non-kin social groups thus provide unique demonstrations of the importance of ecological factors in mediating the evolutionary transition from solitary to group living.

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REVIEW
published: 09 February 2022
doi: 10.3389/fevo.2022.768392
Edited by:
Floria M. K. Uy,
University of Rochester, United States
Reviewed by:
Heikki Helanterä,
University of Oulu, Finland
Alessandro Cini,
University College London,
United Kingdom
*Correspondence:
Madeleine M. Ostwald
ostwald.madeleine@gmail.com
Specialty section:
This article was submitted to
Social Evolution,
a section of the journal
Frontiers in Ecology and Evolution
Received: 31 August 2021
Accepted: 05 January 2022
Published: 09 February 2022
Citation:
Ostwald MM, Haney BR and
Fewell JH (2022) Ecological Drivers
of Non-kin Cooperation
in the Hymenoptera.
Front. Ecol. Evol. 10:768392.
doi: 10.3389/fevo.2022.768392
Ecological Drivers of Non-kin
Cooperation in the Hymenoptera
Madeleine M. Ostwald1*, Brian R. Haney2and Jennifer H. Fewell1
1School of Life Sciences, Arizona State University, Tempe, AZ, United States, 2Division of Natural Sciences, College
of Mount Saint Vincent, Riverdale, NY, United States
Despite the prominence of kin selection as a framework for understanding the
evolution of sociality, many animal groups are comprised of unrelated individuals.
These non-kin systems provide valuable models that can illuminate drivers of social
evolution beyond indirect fitness benefits. Within the Hymenoptera, whose highly related
eusocial groups have long been cornerstones of kin selection theory, groups may
form even when indirect fitness benefits for helpers are low or absent. These non-
kin groups are widespread and abundant, yet have received relatively little attention.
We review the diversity and organization of non-kin sociality across the Hymenoptera,
particularly among the communal bees and polygynous ants and wasps. Further,
we discuss common drivers of sociality across these groups, with a particular
focus on ecological factors. Ecological contexts that favor non-kin sociality include
those dominated by resource scarcity or competition, climatic stressors, predation
and parasitism, and/or physiological constraints associated with reproduction and
resource exploitation. Finally, we situate Hymenopteran non-kin sociality within a
broader biological context by extending insights from these systems across diverse
taxa, especially the social vertebrates. Non-kin social groups thus provide unique
demonstrations of the importance of ecological factors in mediating the evolutionary
transition from solitary to group living.
Keywords: social evolution, relatedness, kinship, wasps, bees, ants
INTRODUCTION
Social animals represent some of the most ubiquitous and ecologically dominant organisms globally
(Hölldobler and Wilson, 1990;Krause and Ruxton, 2002;Ward and Webster, 2016). To date,
our understanding of how social groups emerge has been rooted overwhelmingly in the study
of family groups. From these groups have emerged useful theoretical frameworks for explaining
cooperation in nature, especially kin selection theory, which posits that indirect fitness benefits
of helping kin can compensate for direct fitness costs (Hamilton, 1964;West-Eberhard, 1975;
Trivers and Hare, 1976;Abbot et al., 2011;Bourke, 2014). Nevertheless, many animals form
groups with non-relatives, and in these societies direct fitness gains are generally the major
component of inclusive fitness (Clements and Stephens, 1995;Dugatkin, 2002;Goodnight, 2005;
Clutton-Brock, 2009;Queller, 2011). These social groups, which exist across diverse animal taxa
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Ostwald et al. Non-kin Cooperation in the Hymenoptera
(Bernasconi and Strassmann, 1999;Clutton-Brock, 2009;Riehl,
2013;Wilkinson et al., 2016;Brask et al., 2019;Suarez and
Goodisman, 2021), demonstrate the value of examining the
diversity of selection contexts for understanding the evolution
of sociality, and provide useful models for examining ecological
drivers of social evolution.
Kin selection has proven critically valuable for understanding
the evolution of eusociality, especially within the highly related
colonies of the social insects (West-Eberhard, 1975;Queller
and Strassmann, 1998;Hughes et al., 2008;Abbot et al.,
2011;Bourke, 2011;Linksvayer and Wade, 2011). However,
eusociality is rare; even among the Hymenoptera; other forms
of group living are considerably more common (Heinze et al.,
2017;Hunt and Toth, 2017;Wcislo and Fewell, 2017;Fewell
and Abbot, 2018). Perhaps due to the prominence of kin
selection as a framework for understanding insect sociality, non-
kin groups in insects have received relatively little attention,
despite advances in our understanding of non-kin vertebrate
groups (Clutton-Brock, 2009;Riehl, 2013;Wilkinson et al., 2016;
Brask et al., 2019). Departures from a kin-centric framework
for understanding insect social evolution may enable valuable
connections to other animal groups, contributing to a broader
body of evolutionary theory. Further, these systems may be
neglected because interactions among non-kin rarely (if ever)
constitute altruism—that is, behavior that reduces the fitness of
the actor and increases the fitness of the group—which has been
a major focus of social evolutionary research in the eusocial
Hymenoptera (Hamilton, 1972;Simon, 1990;Foster et al., 2006;
Kennedy et al., 2018). Rather, non-kin associations provide
examples of cooperation based on mutual benefits of grouping,
with or without reproductive division of labor.
We review advances in our understanding of non-kin social
groups in the Hymenoptera, with a focus on patterns of diversity
in social structure and ecological context. We characterize
variation in the organization of these groups and describe
the distribution of non-kin sociality across the bees, ants,
and wasps. Across these groups, we then highlight common
ecological drivers of non-kin sociality, particularly environmental
challenges and intra- and inter-specific interactions. Finally, we
synthesize insights from the current body of research on non-kin
sociality and highlight promising directions for future research.
In doing so, we emphasize the role of ecological context in
shaping sociality at its evolutionary origins.
NON-KIN COOPERATION IN THE
HYMENOPTERA
Non-kin sociality is found broadly among the social ants, wasps,
and bees, and ranges in complexity from simple, facultative
nest sharing in primarily solitary populations to cooperative
founding of eusocial colonies (Figure 1). For the purposes of
this review, we define sociality as any long-term association
between conspecifics characterized by mutual tolerance and/or
cooperation within shared nesting space (Costa, 2006;Fewell
and Abbot, 2018). By “long-term,” we refer to an extended or
significant portion of an individual’s lifespan, as opposed to more
transient interactions like mating. Further, we emphasize mutual
tolerance as a minimum requirement in our definition of sociality
for the sake of including even groups characterized by limited
cooperative behavior. Mutual tolerance serves as a preadaptation
for the evolution of cooperation, by enabling individuals to share
nest space and providing opportunities for more complex social
interactions (Michener, 1974, 1990a).
Specifically, we examine social interactions in the context
of breeding and offspring care, because behavioral decisions in
these contexts have important fitness impacts. We emphasize
nest sharing to exclude from our definition of sociality those
animals living within aggregations of spatially clustered nests,
but otherwise living solitarily. Though some Hymenoptera (such
as army ants) are non-nesting, nests are used predominantly
by this taxon as an essential physical site for the prolonged
interactions intrinsic to social living. Additionally, we define
sociality as distinct from intraspecific social parasitism, and
therefore exclude from our discussion those systems in which
non-kin relationships arise through parasitic behavior (Beekman
and Oldroyd, 2008), including adoption of unrelated offspring
(Klahn, 1988;Nonacs and Reeve, 1993) and cleptoparasitism
(Michener, 1974;Rozen, 1991).
Non-kin associations vary considerably in the degree of
cooperation, and thus serve as an important counterpoint to
vertebrate sociality. However, discussions of cooperation for
social insects and social vertebrates have historically been treated
separately. For example, cooperation in the social insects is
often studied in the context of task allocation and division of
labor (Hölldobler and Wilson, 1990;Seeley, 1996;Beshers and
Fewell, 2001), while social vertebrate sociality is more often
discussed in terms of the costs and benefits of cooperative
interactions (Hamilton, 1964;Dugatkin, 2002;Clutton-Brock,
2009). Defining cooperation itself has also presented challenges,
with debate surrounding the questions of whether cooperative
interactions may incur differential costs for actor and recipient,
and whether cooperative sociality can be maintained under such
conditions without indirect fitness gains (Lehmann and Keller,
2006;West et al., 2006, 2007;Bergmüller et al., 2009). Within
such discussions, however, has emerged a central theme that
cooperation broadly entails behaviors that benefit the social
group (Clutton-Brock, 2009).
Social Evolution in the Hymenoptera
The evolution of cooperative behaviors is shaped by ecological
context and by the phylogenetic pathway that group has taken
to sociality. The task of categorizing the various forms of
sociality and their evolutionary histories has been the subject of
considerable debate (Wilson, 1971;Michener, 1974;Crespi and
Yanega, 1995;Toth et al., 2016;Boomsma and Gawne, 2018;
Richards, 2019). A well-established hypothesis has proposed
a stepwise evolutionary progression from simple forms of
sociality to complex eusociality (Evans, 1956;Wilson, 1971;
Evans and West-Eberhard, 1973;Rehan and Toth, 2015). Recent,
renewed discussion of this topic has challenged the theoretical
presumption of a “social ladder” in which less complex social
forms represent intermediate “levels” along an evolutionary
trajectory toward eusociality (Linksvayer and Johnson, 2019;
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FIGURE 1 | Examples of non-kin sociality are widespread across hymenopteran taxa. In the ants, unrelated foundresses may cooperate to rear eusocial colonies, as
in the harvester ant Pogonomyrmex californicus (top left; photo by Elizabeth Cash). Similarly, foundresses of some wasp species, like the paper wasp Polistes
dominula (bottom; photo by Meagan Simons), may cooperatively found eusocial nests with non-relatives. Non-kin associations are also found among the communal
bees, such as the sweat bee Agapostemon virescens (top right; photo by Nicholas Dorian), which shares nest-entrance guarding duties with unrelated nestmates.
Holland and Bloch, 2020). Accordingly, we consider the diversity
of cooperative systems in the social insects not as transitional
forms in the evolution of sociality, but instead in terms of their
shared cooperative behavioral repertoires that are adaptive in a
given ecological context.
One of the simplest forms of sociality, known as communal
living, refers to societies in which multiple same-generation
females (often unrelated) share nesting space but independently
forage and provision their own offspring (Michener, 1974).
Communal groups are characteristically casteless: group
members are not distinguished behaviorally or morphologically
by their capacity for reproduction. Only a subset of tasks—
typically nest construction and nest defense—are shared
cooperatively. Communal groups often exist among otherwise
solitary populations of bees and wasps, and are characterized
by behavioral repertoires similar to those of solitary females:
they mass-provision brood at the egg stage, and do not engage
in further direct parental care (Wcislo and Tierney, 2009;
Wcislo and Fewell, 2017). In contrast, other social insects,
including ants, wasps, and some bee taxa, perform direct parental
care in which larvae are fed progressively (Field, 2005). The
cooperative repertoire of these groups is similarly expanded.
These associations occur when related or unrelated females
found nests cooperatively (pleometrosis) by sharing or dividing
such tasks as provisioning, nest construction, and defense (Ross
and Matthews, 1991;Heinze et al., 2017).
Social Diversity in the Hymenoptera
Here we describe the diversity of non-kin sociality defined as
long-term adult nest sharing, with groups often characterized
by cooperative behaviors and task sharing. Because relatedness
is a relative attribute (Pamilo, 1989), we do not strictly
define kin vs. non-kin, but rather focus on groups in which
individuals may be no more related to their nestmates than
they are to non-nestmates. For some of the systems we discuss,
non-kinship in social groups has been evaluated with high
confidence by inferring relatedness from molecular markers.
In many other cases, the presence of non-relatives in social
groups has been inferred from observations of nest-joining
behavior, often by individuals from distant nests (in bees and
wasps), or of cooperative nest founding by presumed unrelated
foundresses (in wasps and ants). Though these observations
cannot confirm the degree of relatedness between joiners
and their nestmates, they provide suggestions of potential
flexibility in tolerance toward unrelated conspecifics. Because
the data on kinship in these groups is so incomplete, we
highlight these uncertain cases as promising avenues for future
genetic investigation.
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Within the Hymenoptera, we explore non-kin groups among
wasps, bees, and ants, finding limited evidence for true sociality
among the sawflies (Hymenoptera: Symphyta), which have short
adult lifespans and are non-nesting (Kudo et al., 1998). For
each group, we describe patterns and diversity of non-kin
social systems. We do not present an exhaustive review of
all known non-kin groups in the Hymenoptera, but instead
highlight common patterns of social organization across the
major suborders.
Wasps: Communal Societies and
Foundress Associations
The wasps (Hymenoptera: Apocrita) comprise more than
37 families, among which only three (Aculeata: Pompilidae,
Sphecidae, and Vespidae) contain social species (Hunt and
Toth, 2017). Non-kin groups are found within all three
of these families (Table 1). Communal nesting has been
described for several species, and among these, nest-joining
by non-relatives is possible, though unconfirmed, for the
spider wasp Auplopus semialatus (Pompilidae: Pepsinae); (Wcislo
et al., 1988), the digger wasp Crabro cribrellifer (Crabronidae:
Crabroninae); (Wcislo et al., 1985), and the pollen wasp
Trimeria howardii (Vespidae: Masarinae); (Zucchi et al., 1976).
Facultative nest sharing is likewise known among the hover wasps
(Vespidae: Stenogastrinae), where unrelated females can join
established foundresses (Strassmann et al., 1994;Turillazzi, 2012).
Similarly, among the primitively eusocial paper wasps (Vespidae:
Polistinae), foundress associations often form among sisters or
other close relatives (West-Eberhard, 1969;Ross and Matthews,
1991), but in many cases may be comprised of non-kin (Queller
et al., 2000;Hunt, 2007;Mora-Kepfer, 2014). For the paper
wasp Polistes dominula, 15–35% of foundress associations consist
of unrelated females (Queller et al., 2000;Zanette and Field,
2008;Leadbeater et al., 2011). Co-founding by non-relatives is
also known, but uncommon, in Polistes fuscatus (Klahn, 1979)
and Polistes exclamans (MacCormack, 1982). Unlike communal
groups, these societies are characterized by high reproductive
skew, so unrelated joiners often become subordinate helpers
with limited reproductive opportunities (Queller et al., 2000;
Leadbeater et al., 2010;Mora-Kepfer, 2014).
Bees: Communal and Parasocial
Societies
Communal nesting occurs across all six major bee families
(Wcislo, 1993;Kukuk et al., 2005), and many of these communal
groups are known or expected to consist of non-kin. This
social strategy is perhaps best known among the sweat bees
(Halictidae), which are known for their incredible diversity of
social behaviors (Michener, 1974, 1990b,2007;Brady et al.,
2006). Halictid communal nesting has been described within the
subfamilies Halictinae and Nomiinae; for most of these species,
relatedness among communal nestmates is unknown (Michener,
1969;Wcislo, 1993;Vogel and Kukuk, 1994;Wcislo and Engel,
1996), but may be inferred to be low through observations
of nest-joining behavior (Michener and Lange, 1958;Abrams
and Eickwort, 1981;Richards et al., 2003). Kukuk and Sage
analyzed two polymorphic genetic loci among colonies of the
sweat bee Lasioglossum hemichalceum (Halictidae: Halictinae)
and found relatedness within reproductively active nests to
be indistinguishable from zero (1994). Communal nesting is
present but less common among the Colletid bees (Sakagami
and Zucchi, 1978), with low relatedness (r= 0.26) confirmed
among nestmates of Amphylaeus morosus (Colletidae: Hylaeinae)
(Spessa et al., 2000). Similarly, non-kin nesting is possible
among the communal Andrenidae (Danforth, 1991;Paxton et al.,
1999), and has been confirmed for two species: Andrena scotica
(formerly jacobi); (Andrenidae: Andreninae) (Paxton et al.,
1996) and Macrotera (formerly Perdita)texana (Andrenidae:
Panurginae) (Danforth et al., 1996).
In other cases, the social organization of some non-kin bee
groups is more aptly described by the umbrella term “parasocial,”
which includes all associations of same-generation adults, which
may be cooperative or non-cooperative, and which may exhibit
high or low reproductive skew (Michener, 1974). This is the
case for many bees of the family Apidae, which includes both
solitary and highly social species. For example, bees in the genus
Exomalopsis (Apidae: Apinae) form multi-female nests, which
may be characterized by cooperative provisioning (Michener,
1966) and even reproductive skew (Raw, 1977). Relatedness
in this genus has not been formally investigated, but is likely
to be low for many species, considering the high number of
females per nest (884 in one nest of E. aureopilosa;Rozen, 1984).
Non-kin associations could also be found among pleometrotic
foundresses of eusocial colonies, though this is rare within the
bees. Low relatedness has been described for co-foundresses of
the primitively eusocial sweat bee Halictus ligatus, likely arising
from chance encounters among females emerging from their
winter hibernacula (Richards and Packer, 1998).
An interesting case of non-kin sociality exists among the large
carpenter bees in the genus Xylocopa (Apidae: Xylocopinae).
Nest-joining behavior has been observed in several species, in
many cases by unrelated bees (Gerling, 1982;Gerling et al., 1983;
Velthuis, 1987;Michener, 1990a;Hogendoorn and Leys, 1993;
Peso and Richards, 2011). However, low relatedness in social
groups has only been demonstrated with molecular evidence
for two species, X. sonorina and X. virginica (Ostwald et al.,
2021a, this issue; Vickruck and Richards, 2021, this issue).
Sociality in these groups is not easily classified, given variation
and ambiguity in helping behavior, reproductive skew, and
generational overlap (Gerling et al., 1989;Michener, 1990a;
Hogendoorn and Velthuis, 1993). In most cases, a single
dominant female per social nest will monopolize egg laying and
provisioning behavior, with nestmates potentially contributing
to nest guarding (Gerling et al., 1983, 1989;Hogendoorn and
Velthuis, 1999;Buchmann and Minckley, 2019).
Ants: Foundress Associations and
Primary Polygyny
In the ants, non-kin sociality through pleometrosis is relatively
commonplace in incipient colonies, but usually ends with a queen
culling event triggered by worker emergence (Bernasconi and
Strassmann, 1999). However, permanent non-kin social groups
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TABLE 1 | Hymenopteran species with the strongest evidence for non-kin associations.
Taxon Social
organization
Evidence for
non-kin sociality
Within-group rReferences
Wasps Vespidae
Stenogastrinae
Liostenogaster flavolineata Primitively
eusocial
Allozyme analysis Not reported for
foundresses
Strassmann et al., 1994
Polistinae
Mischocyttarus mexicanus Primitively
eusocial
Behavioral
observations
NA Mora-Kepfer, 2014
Polistes exclamans Primitively
eusocial
Behavioral
observations
NA MacCormack, 1982
Polistes fuscatus Primitively
eusocial
Behavioral
observations
NA Klahn, 1979
Polistes dominula Primitively
eusocial
Microsatellite
analysis
∼0.1 (for 15% of
population)
Queller et al., 2000;Zanette
and Field, 2008
Bees Andrenidae
Panurginae
Macrotera texana Communal DNA fingerprinting 0.008 Danforth et al., 1996
Andreninae
Andrena scotica Communal Microsatellite
analysis
∼0Paxton et al., 1996
Halictidae
Halictinae
Lasioglossum hemichalceum Communal Allozyme analysis 0.07 Kukuk and Sage, 1994
Halictus sexcinctus Communal or
primitively
eusocial
Behavioral
observations
NA Richards et al., 2003
Halictus ligatus Primitively
eusocial
Allozyme analysis −0.18 Richards and Packer, 1998
Agapostemon virescens Communal Behavioral
observations
NA Abrams and Eickwort, 1981
Pseudagapostemon divaricatus Communal Behavioral
observations
NA Michener and Lange, 1958
Colletidae
Hylaeinae
Amphylaeus morosus Communal Allozyme analysis 0.26 Spessa et al., 2000
Apidae
Xylocopinae
Xylocopa virginica Parasocial Microsatellite
analysis
0.09–0.30 Vickruck and Richards,
2021, this issue
Xylocopa sonorina Parasocial Microsatellite
analysis
−0.09–0.35 Ostwald et al., 2021a, this
issue
Xylocopa sulcatipes Parasocial or
semisocial
Behavioral
observations
NA Velthuis, 1987
Xylocopa pubescens Parasocial or
semisocial
Behavioral
observations
NA Gerling et al., 1983;
Hogendoorn and Leys,
1993
Ants Formicidae
Myrmecinae
Atta texana Eusocial Behavioral
observations
NA Moser and Lewis, 1981
Acromyrmex versicolor Eusocial Allozyme analysis −0.12 Rissing et al., 1989
Acromyrmex heyeri Eusocial Isozyme analysis Not reported Diehl et al., 2001
Acromyrmex striati Eusocial Isozyme analysis Not reported Diehl et al., 2001
Myrmica gallienii Eusocial Isozyme analysis 0.01 Seppä, 1996
Pogonomyrmex californicus Eusocial Microsatellite
analysis
0.059 Overson et al., 2016
(Continued)
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TABLE 1 | (Continued)
Taxon Social
organization
Evidence for
non-kin sociality
Within-group rReferences
Messor pergandei Eusocial Microsatellite
analysis
∼0Helms and Helms Cahan,
2012
Camponotus ligniperdus Eusocial Microsatellite
analysis; DNA
fingerprinting
Not reported Gadau et al., 1998
Formicinae
Myrmecocystus mimicus Eusocial Microsatellite
analysis
0.053 Eriksson et al., 2019
Formica podzolica Eusocial Microsatellite
analysis
0.156 DeHeer and Herbers, 2004
Oecophylla smaragdina Eusocial Microsatellite
analysis
0.08 Schlüns et al., 2009
Ponerinae
Neoponera inversa Eusocial Microsatellite
analysis
−0.036 (2007) Heinze et al., 2001;Kolmer
et al., 2002;Kellner et al.,
2007
Neoponera villosa Eusocial Microsatellite
analysis
0.024 Kellner et al., 2007
Myrmeciinae
Myrmicia pilosula Eusocial Microsatellite
analysis
0.088 Qian et al., 2012
Myrmicia rubra Eusocial Microsatellite
analysis; Isozyme
analysis
0.041 (1982) Pearson, 1982, 1983;
Seppä and Walin, 1996
Dolichonderinae
Iridomyrmex purpureus Eusocial mtDNA analysis Not reported Carew et al., 1997
Where available, we report r-values for comparisons among adult female nestmates, often foundresses.
can form when a pleometrotic queen association extends past
worker emergence and into colony maturity. This results in
primary polygyny, a group of unrelated worker lineages that
share a nest, colony resources, and colony tasks. Importantly,
workers in polygynous colonies may be close kin if they were
produced by the same queen. Nevertheless, overall worker
nestmate relatedness is often low in polygynous colonies (DeHeer
and Herbers, 2004;Kellner et al., 2007). More importantly, the
queens themselves represent prominent examples of non-kin
cooperative behavior, analogous to cooperative breeders in other
taxa, regardless of offspring group relatedness. Primary polygyny
is generally found interspersed between monogynous colonies or
as the majority structure in discrete populations, but has never
been documented as the only social structure of an ant species.
Primary polygyny is represented in several ant subfamilies
but is especially well documented in the Myrmicinae. Moser
and Lewis (1981) first observed multiple unrelated queens
in mature colonies of the Texas leaf-cutter ant Atta texana.
Mintzer and Vinson subsequently found that these cooperative
associations are stable and beneficial to A. texana queen survival
in the lab (Mintzer and Vinson, 1985;Mintzer, 1987). Shortly
afterward, Rissing et al. (1989) utilized allozyme markers to
directly show that cohabiting Acromyrmex versicolor queens
were not related and also reared stable multi-queen colonies
in the lab. There is also genetic evidence, using isoenzymes,
that two South American Acromyrmex species practice primary
polygyny, A. striatus and A. heyeri (Diehl et al., 2001). Multiple,
unrelated queens were also found in colonies of Myrmica gallienii
using enzyme electrophoresis (Seppä, 1996), however colony
age was not reported in this study. Primary polygyny may
also occur in the fungus growing ant species, Cyphomyrmex
transversus. Multiple queens were found in 37.7% of colonies
examined by Ramos-Lacau et al. (2012) but it is unknown
if these queens were related. Within the Myrmicinae, there
are also several harvester ant species that practice primary
polygyny. Pogonomyrmex californicus displays primary polygyny
in southern California, as confirmed with field observation
(Johnson, 2004), laboratory colonies (Clark and Fewell, 2014;
Overson et al., 2014), and microsatellite analysis (Overson
et al., 2016). Primary polygyny also occurs in a California
population of the seed harvester Veromessor pergandei, also
confirmed using microsatellites (Helms and Helms Cahan, 2012).
Queens of another species in the same genus, Messor barbarous,
can be induced into stable cooperative associations in the
lab, but no polygynous colonies have been found in the field
(Provost and Cerdan, 1990).
Within the subfamily Formicinae, the honeypot ant
Myrmecosystus mimicus also practices primary polygyny in
an Arizona population as confirmed by microsatellite analysis
by Hölldobler et al. (2011). The mound building ant Formica
podzolica exhibits primary polygyny in Colorado, as suggested by
field excavation (Deslippe and Savolainen, 1995) and confirmed
through microsatellite analysis (DeHeer and Herbers, 2004).
Finally, multiple unrelated queens have been found in mature
colonies of the pleometrotic weaver ant Oecophylla smaragdina,
strongly suggesting primary polygyny (Schlüns et al., 2009).
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Some of the most detailed genetic and behavioral research has
been performed on species in the Ponerinae subfamily. Primary
polygyny has been confirmed in Neoponera inversa through
behavioral observation in the field and lab (D’Ettorre et al.,
2005) as well as with multiple microsatellite analyses (Heinze
et al., 2001;Kolmer et al., 2002). In a closely related species,
Neoponera villosa, queen cooperation has been demonstrated
in the lab (Trunzer et al., 1998) and unrelated queens have
been documented in field colonies (Kellner et al., 2007), strongly
suggesting primary polygyny. Mature Neoponera striata Smith
colonies have also been found with multiple queens, but more
work is needed on queen relatedness to confirm primary
polygyny (Rodrigues et al., 2011). The arboreal trap jaw ant
Odontomachus hastatus has been found in colonies containing
several queens and workers, but it is unknown if these queens are
related (Oliveira et al., 2011).
Primary polygyny has also been confirmed via microsatellite
analysis in two species of the Myrmeciinae: the Australian jumper
ant Myrmicia pilosula (Qian et al., 2012) and the red ant Myrmicia
rubra (Pearson, 1982, 1983;Seppä and Walin, 1996).
Finally, in the Dolichoderinae subfamily, Hölldobler and
Carlin (1985) found that the Australian meat ant Iridomyrmex
purpureus is oligogynous, i.e., multiple queens share a nest but do
not tolerate each other and relegate themselves to different areas
of the nest. Further genetic analysis confirmed that oligogynous
I. purpureus queens are unrelated and share a workforce (Carew
et al., 1997). Oligogyny has also been documented in the
subfamily Formicidae (Camponotus ligniperdus, Gadau et al.,
1998;Camponotus herculeanus,Seppä and Gertsch, 1996).
ECOLOGICAL DRIVERS OF NON-KIN
SOCIALITY
Group living may have its evolutionary origins across a
particular set of ecological conditions that favor nest sharing
and/or cooperation (Arnold and Owens, 1997;Krause and
Ruxton, 2002;Rubenstein and Abbot, 2017). For non-kin
groups especially, local ecology may be a prominent driver
of group formation in the absence of strong indirect fitness
benefits. Below, we discuss evidence for the evolution of non-kin
sociality in the Hymenoptera as driven by five major ecological
conditions/constraints: (1) predator and parasite pressures,
(2) intraspecific competition, (3) physiological constraints, (4)
productivity constraints, and (5) climatic stressors. Importantly,
the distinctions we make between these five factors do not
represent mutually exclusive conditions; rather, they are highly
interactive and may even represent flip sides of the same
environmental selective pressures (e.g., productivity constraints
that arise from intense intraspecific competition). Together, these
conditions may give rise to fitness differentials between solitary
and social individuals when benefits of group living outweigh
intrinsic costs of resource sharing.
Predator and Parasite Pressures
The need for communal defense represents one prominent
benefit of nesting with non-kin. In particular, social defensive
strategies often arise in contexts where brood is vulnerable to
predation or parasitism (Alexander, 1974;Krause and Ruxton,
2002;Ward and Webster, 2016). Importantly, social nest defense
can be a passive, emergent property of shared nesting rather
than actively cooperative behavior. The presence of multiple
females (or even males; Kukuk and Schwarz, 1988) in the nest
can deter invaders by decreasing the daily time window in
which the nest is unattended (Lin and Michener, 1972;Wcislo
and Tierney, 2009). In other cases, labor may be divided such
that guarding is a functional role of certain group members,
often subordinates (Hogendoorn and Velthuis, 1995;Dunn and
Richards, 2003). Indeed, task specialization on guarding can
even emerge spontaneously among forced, unrelated associations
of normally solitary individuals, suggesting that improved nest
defense can arise in in communal nests from existing behavioral
repertoires (Jeanson et al., 2005;Holbrook et al., 2009, 2013).
Although predator/parasite pressures have been broadly
implicated in social evolutionary transitions (Michener and
Lange, 1958;Lin and Michener, 1972;Krause and Ruxton,
2002;Wilson and Hölldobler, 2005), empirical demonstrations
of the effectiveness of group defense in non-kin systems
are sparse. For the sweat bee Agapostemon virescens,Abrams
and Eickwort (1981) found that communal nests were more
effectively defended against the cleptoparasite Nomada articulata
than were solitary nests. Indeed, Lin and Michener (1972)
consider parasite/predator pressures to be the major driver of
sociality in the Halictidae (see also Michener and Lange, 1958).
Similarly, co-founding wasps may experience reduced predation
from birds and mammals relative to solitary foundresses, likely
due to more continuous nest guarding (Strassman et al., 1988;
Tindo et al., 2008). For other non-kin groups, guarding may
function to repel conspecific intruders, but may not be an
effective defense against predation and parasitism. For the
facultatively social bees Xylocopa virginica and Halictus ligatus,
rates of brood parasitism by Bombyliid flies were found to be
no different between solitary and social nests, despite increased
guard presence in social nests (Richards and Packer, 1998;Prager,
2014). Similarly, though multiple Polistes wasp foundresses
may provide effective protection against intraspecific usurpation
(Gamboa, 1978;Gamboa et al., 1978;Klahn, 1988), they may
be no more effective in guarding against predators (Gamboa,
1978;Gamboa et al., 1978;Gibo, 1978) and parasites (Gamboa
et al., 1978) than solitary foundresses, despite more continuous
guard presence (Gamboa et al., 1978). However, co-founding
may provide important benefits during recovery from predation
attempts (Gibo, 1978;Strassman et al., 1988).
Intraspecific Competition and Resource
Limitation
Grouping may arise as a response to limiting resources, especially
nesting sites and food (Emlen, 1982;Hatchwell and Komdeur,
2000). Environments characterized by strong intraspecific
competition may favor cooperative strategies that allow groups
to exploit resources. In many cases grouping occurs in densely
populated or saturated environments. Indeed, pleometrosis
and primary polygyny in ants have been associated in several
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species with high population density (Tschinkel and Howard,
1983;Rissing and Pollock, 1986, 1991;Bennet, 1987;Trunzer
et al., 1998). Likewise, for the facultatively polygynous harvester
ant, Pogonomyrmex californicus, sites dominated by polygyny
have higher colony density than primarily monogynous
sites (Haney and Fewell, 2018). Further, colonies in the
polygynous population have lower reproductive output than
colonies from the monogynous population. Experimental food
supplementation increased reproductive output of polygynous
colonies to that of colonies from the monogynous population,
suggesting that competitive, food-scarce conditions drive
cooperation in this species (Haney and Fewell, 2018). Similarly,
bees may adopt non-kin social strategies under food-scarce
conditions, even in the absence of productivity benefits of group
living. For the facultatively social carpenter bee X. pubescens,
solitary nests typically outperform social nests in terms of
reproductive output, due to brood mortality that results from
dominance competitions in social nests (Hogendoorn, 1991,
1996). However, under conditions of food scarcity, social
nesting can provide an important safeguard against pollen
robbery, outweighing costs of nest sharing (Hogendoorn, 1991;
Hogendoorn and Velthuis, 1993).
Nest sites can also be major limiting resources, favoring social
strategies that enable nest sharing and/or increase the likelihood
of nest inheritance. Carpenter bees are strongly limited by access
to nest sites, creating intense competition for constructed nests
that results in frequent supersedure and usurpation (Gerling
et al., 1989;Buchmann and Minckley, 2019). Social nesting
could feasibly provide an important defense against the threat
of nest invasion, but empirical studies have demonstrated
that guards of X. pubescens, though potentially valuable in
preventing pollen robbery, do not effectively defend the nest
from usurpers (Hogendoorn and Velthuis, 1993, 1995). Instead,
subordinate joiners are likely hopeful reproductives that queue
for reproductive opportunities upon the death of the dominant
bee and subsequent nest inheritance (Hogendoorn and Velthuis,
1995;Richards and Course, 2015;Vickruck and Richards, 2018).
Nest inheritance is likewise important for co-founding wasps
(Reeve, 1991;Leadbeater et al., 2011), especially for species that
reuse old nests (Queller and Strassmann, 1988). Similarly, for
many communal bees, group living enables shared exploitation
of valuable nest sites (Michener, 1974). In all these cases,
intraspecific competition for nests promotes group living and
interacts with other ecological constraints, especially energetic
and labor constraints on nest construction.
Energetic and Physiological Constraints
Non-kin groups may also form in contexts that impose steep
physiological costs on independent breeders. For example,
animals that invest in energetically costly nest building behaviors
may experience selection for strategies that reduce founding
costs, such as cooperative building and/or nest inheritance
(Hansell, 1987). Cooperative nest building has been documented
broadly across Hymenopteran non-kin groups (West-Eberhard,
1969;Bartz and Hölldobler, 1982;Tschinkel and Howard,
1983;Rissing and Pollock, 1986;Peeters and Andersen, 1989;
Danforth, 1991;Bernasconi and Strassmann, 1999;Hunt and
Toth, 2017). In some cases, these benefits have been linked to
ecological conditions and energetic constraints. The ground-
nesting communal bee Perdita portalis excavates nests through
a dense, clay layer of soil, prompting Danforth (1991) to propose
energetic costs of nest construction as a major driver of sociality
in this environment. Challenging excavation through hard soil
may likewise favor cooperative nest construction strategies in
the communal bee Macrotera texana (Danforth et al., 1996).
Carpenter bees may also face particularly high energetic costs of
nest building, due to the tendency of many Xylocopa species to
nest in dense wood substrate. For the carpenter bee X. sonorina,
the energetic cost of new nest construction is higher on average
than the cost of nest inheritance, even accounting for the
potential cost of renovating overused tunnels (Ostwald et al.,
2021b). In this group, and more broadly, high costs of nest
building can underlie intraspecific competition for existing nests.
These costs may incentivize social strategies such as reproductive
queuing or communal nesting, even at the expense of uncertain
reproductive opportunities.
Beyond energetic costs, nest building behavior can
impose physiological wear and damage. In arid habitats, nest
construction behaviors could be constrained more by desiccation
risk than by energetic costs. For many desert ants, nest excavation
causes cuticular abrasion that increases water loss rates (Johnson,
2000), exacerbating desiccation risk, which is a major cause
of foundress mortality (Johnson, 1998). Cooperative nest
excavation during founding poses an important possible solution
to this challenge. However, the physiological costs of excavation
may not be shared equally among co-foundresses (Fewell and
Page, 1999). Cahan and Fewell (2004) measured excavation
task specialization in experimental pairs of the facultatively
polygynous Pogonomyrmex californicus, with foundresses
collected either from a typically group-founding or typically
solitary-founding population. For both populations, more than
half of foundress pairs divided excavation labor asymmetrically,
with one foundress emerging as an excavation specialist.
However, pairs from the group-founding population showed
smaller asymmetries in excavation performance (Cahan and
Fewell, 2004). These findings suggest that while some foundresses
may experience disproportionate costs of excavation, cooperative
strategies overall can reduce physiological costs of excavation
for a significant portion of the population. Cooperative nest
excavation and maintenance may likewise be important for some
ground-nesting social bees (Danforth, 1991), but the extent to
which nest excavation behavior is physiologically constrained in
these groups is still unclear.
Productivity Constraints
Cooperation among non-kin can also improve productivity
under harsh or competitive conditions. In particular, cooperative
founding may provide competitive advantages in conditions that
favor rapid nest establishment via worker production. Group
founding in ants has been associated both with faster initial
worker production and accelerated colony growth (Tschinkel
and Howard, 1983;Rissing and Pollock, 1987;Deslippe and
Savolainen, 1995;Eriksson et al., 2019;Ostwald et al., 2021c).
Rapid production of a large workforce may beneficially accelerate
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incipient groups through the vulnerable founding period,
providing a critical survival advantage for cooperatively founded
colonies (Clark and Fewell, 2013;Ostwald et al., 2021c). These
advantages may be especially important for colonies vulnerable
to intraspecific brood raiding. Cooperative founding has been
shown to improve colony survival and success during brood
raiding, likely due to the protective effect of larger colony sizes
(Bartz and Hölldobler, 1982;Rissing and Pollock, 1987, 1991;
Eriksson et al., 2019). Increased colony size in multi-foundress
nests is also associated with reduced colony failure rates for
the paper wasp Polistes dominula (Tibbetts and Reeve, 2003).
Importantly, cooperative foundresses may experience enhanced
colony growth without increasing costly individual investment in
sterile worker production. Multi-queen colonies of the harvester
ant P. californicus experience faster colony growth than single
queen colonies, but lower per-queen worker production (Ostwald
et al., 2021c). The ability to assemble a large workforce while
minimizing individual investment in non-reproductive offspring
may represent an important physiological benefit of cooperation
with non-relatives.
Specifically, individuals may face productivity constraints
associated with resource exploitation. For example, the
communal bee Macrotera texana faces severe reproductive
time constraints due to its foraging dependence on Opuntia
flowers that bloom for only 2–3 weeks per year (Danforth et al.,
1996). Cooperative nest excavation likely enables females to
exploit this time-limited resource by accelerating nest founding
(Danforth et al., 1996). Similarly, increased colony activity levels
in polygynous P. californicus colonies suggests both increased
worker production and corresponding enhanced efforts to
capitalize upon limiting food resources (Haney and Fewell,
2018). In this way, productivity constraints interact strongly with
resource limitation and intraspecific competition.
Importantly, worker production benefits may not translate
to enhanced production of reproductives. For P. californicus
as well as for the sweat bee, Halictus ligatus, group-founding
nests produce more workers but fewer reproductive offspring
than solitary-foundress nests (Richards and Packer, 1998;Haney
and Fewell, 2018). Polistes foundress associations are likewise
associated with reduced per-capita reproductive output (Queller
and Strassmann, 1988;Reeve, 1991), despite increased worker
production in some species (Tibbetts and Reeve, 2003). These
cases suggest that cooperation often functions not as a means to
enhance reproductive output under ideal conditions, but rather
as a strategy to minimize losses under constraining or challenging
environmental conditions.
Climatic Stressors
Climatic factors represent fundamental ecological drivers of
group living across animal taxa. In particular, cooperation may be
favored in harsh or stochastic climates (Arnold and Owens, 1997;
Jetz and Rubenstein, 2011;Rubenstein, 2011;Griesser et al., 2017;
Lukas and Clutton-Brock, 2017;Kennedy et al., 2018). In insects,
climate likewise mediates the expression of social behavior,
especially through impacts on development time and seasonal
activity windows, which affect the available time for rearing
workers and therefore the potential for colony life to emerge
(Eickwort et al., 1996;Hunt and Amdam, 2005;Hirata and
Higashi, 2008;Fucini et al., 2009). These factors may be important
in the evolution of eusociality by promoting generation overlap
in the nest. For non-kin groups, however, that arise from stable
cooperative relationships between unrelated individuals, the
effects of climate on group formation are relatively unexplored.
Nevertheless, several studies point to prominent roles for
climatic conditions, especially environmental temperatures, in
facilitating non-kin cooperation. Among Polistes paper wasps,
which can found nests with non-relatives, cooperative nest
founding is associated with high temperature variability, perhaps
due to buffering cooperation of sociality in unpredictable
environments (Sheehan et al., 2015). Polygyny in ants has
also been associated with harsh thermal environments (Heinze,
1993;Heinze and Hölldobler, 1994;Heinze and Rüppel, 2014)
and with success of invasive species in their introduced
environments (Holway et al., 2002;Tsutsui and Suarez, 2003).
Future work should clarify mechanisms underlying this link
between cooperation and success in harsh, variable, or novel
thermal environments.
Precipitation can also influence the relative costs and benefits
of grouping. Arid environments and drought conditions can
increase soil hardness, potentially increasing excavation costs
and exacerbating nest limitation for ground nesting bees, ants,
and wasps (Wcislo, 1997;Michener, 2007;Purcell, 2011). Under
drought conditions, Bohart and Youssef (1976) found that
30% of nests of the normally solitary sweat bee Lasioglossum
galpinsiae were provisioned by multiple females. In desert
ants, group founding may be a by-product of the tendency to
seek refuge from desiccating conditions in shared belowground
spaces (Pfennig, 1995). Under desiccating conditions, group-
founding by the desert seed-harvester ant Veromessor pergandei
enhanced queen survival and water content relative to solitary
queens, though the mechanism for this advantage is unclear
(Johnson, 2021). Shared foraging duties could feasibly reduce
risk of desiccation in desert habitats. Cahan and Fewell (2004)
suggest that a group-founding population of the harvester ant
P. californicus occupies a habitat with lower and less predictable
summer precipitation than sites occupied by solitary founding
populations, suggesting possible desiccation constraints. In
less arid habitats, extended periods of rain can cause nest
failure for ground-nesting species. For the sweat bee Halictus
ligatus, foundress cooperation may provide protection against
rain-induced nest failure through enhanced nest maintenance
(Richards and Packer, 1998). As such, like environmental
temperature, precipitation can alternately promote or constrain
cooperative behavior among non-relatives.
DISCUSSION
Sociality can be understood as an adaptive response to ecological
conditions. Non-kin groups present valuable test cases for
hypotheses about the ecological drivers of group formation, in
particular, because communal and co-founding strategies are
nearly always facultative at the individual or population level
(Ross and Matthews, 1991;Michener, 2007;Heinze et al., 2017).
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Studying non-kin groups usefully controls for indirect fitness
benefits, thus enhancing our understanding of other, relatively
neglected drivers of group formation. These systems have yielded
important intraspecific demonstrations of the role of ecology
in determining the adaptive value of grouping behavior. Here,
we have explored five central ecological factors expected to
interact with the expression of social behavior: interspecific
pressures from predators and parasites, intraspecific pressures
over limited resources, environmental constraints on individual
physiology and productivity, and stressors associated with
climate. Evidence from across Hymenopteran systems indicates
that these conditions play a pivotal role in shaping non-kin
social strategies.
Importantly, these ecological drivers of sociality are highly
interactive. Efforts to understand sociality across a single
environmental axis are limiting and often yield contradictory
results (e.g., sociality alternately increasing and decreasing
with latitude; Purcell, 2011). Instead, integrative approaches
that accommodate these interactions can provide important
insights into the complex conditions underlying grouping
responses. Studies in Hymenopteran systems have emphasized
interactions among intraspecific, interspecific, and abiotic
selective pressures. For example, sociality can be a response
to intraspecific competition for access to nests (Gerling et al.,
1989;Leadbeater et al., 2011). This competition is often a
direct product of physiological constraints associated with nest
construction behavior (Johnson, 2000;Ostwald et al., 2021b),
which can be exacerbated by climatic stressors such as low
precipitation (Wcislo, 1997;Purcell, 2011). This particular
nexus of challenges is an important driver of group formation
among the communal and parasocial bees and polygynous
ants (Danforth, 1991;Danforth et al., 1996;Cahan and
Fewell, 2004). Highly competitive environments can also give
rise to cooperative strategies that mitigate worker production
constraints experienced by solitary foundresses. Accelerated
worker production is a major benefit of cooperation among ant
foundresses vulnerable to brood raiding in contexts dominated
by intraspecific competition (Bartz and Hölldobler, 1982;Rissing
and Pollock, 1987, 1991;Eriksson et al., 2019). Productivity
constraints may also be important drivers of grouping in
environments dominated by predation pressures; for group-
founding wasps, increased colony sizes can provide essential
resilience following predation attempts (Strassman et al., 1988).
Together, these examples suggest shared sets of ecological
conditions that favor cooperative behavior even when relatedness
is low or absent among group members. Importantly, these
conditions are not restricted geographically but instead occur
at intersections of particular selective pressures that can occur
across a wide variety of habitat types.
These findings in non-kin groups of ants, bees, and
wasps parallel known drivers of social evolution in non-insect
social systems, both kin and non-kin. Ecological constraints
are prominent, known drivers of cooperative breeding in
birds and mammals (Emlen, 1982, 1984;Arnold and Owens,
1997;Hatchwell and Komdeur, 2000;Shen et al., 2017).
Inheritance tactics in nest-limiting environments may favor
delayed dispersal and nest joining (Woolfenden and Fitzpatrick,
1978;Emlen, 1984). As with the ground-nesting ants and
bees, nesting constraints may be physiological, and can be
exacerbated by climatic conditions: nest excavation costs in arid
conditions have been proposed as a major driver of sociality
in the African mole-rats (Jarvis et al., 1994;Faulkes et al.,
1997;Hansell, 2005). More broadly, low and unpredictable
rainfall has been associated with the global biogeography of
cooperatively breeding mammals (Lukas and Clutton-Brock,
2017). Environmental stochasticity has also been implicated in
the global distribution of cooperative breeding in birds (Jetz
and Rubenstein, 2011), suggesting important links between
cooperation and environmental uncertainty that parallel trends
described in Polistes foundress associations (Sheehan et al., 2015).
Strengthening the conceptual links among Hymenopteran
and vertebrate sociality has great potential for the development
of broader evolutionary frameworks explaining non-kin
cooperation. Vertebrate research has benefited from a more
comprehensive understanding of the taxonomic distribution of
kin and non-kin sociality, especially among the cooperatively
breeding birds. This knowledge base has enabled valuable
phylogenetic studies highlighting the roles of environmental and
life history factors in shaping social organization (Riehl, 2013;
Downing et al., 2015, 2020;Cornwallis et al., 2017). The social
Hymenoptera likewise present special opportunities to study
non-kin sociality because it occurs frequently across closely
related lineages. To our knowledge, this comparative approach
has not yet been applied to the Hymenoptera in the context of
kin vs. non-kin social evolution, but may be feasible for those
taxa in which non-kin sociality is better documented, especially
the polygynous ants.
Beyond this comparative framework, the literature on
vertebrate social systems can provide social insect researchers
with valuable approaches for studying direct benefits of
cooperation. The social vertebrate literature is rich in
explorations of the costs and benefits of well-defined cooperative
behaviors, from hunting and defending food (Packer and Ruttan,
1988;Lucas and Brodeur, 2001) to detecting and repelling
predators (Hamilton, 1971;Foster and Treherne, 1981) or
successfully rearing offspring (Ebensperger et al., 2007;Hodge
et al., 2009). Likewise, studies should investigate direct benefits of
cooperative behaviors in Hymenopteran societies, for example,
the effectiveness of nest defense in social vs. solitary bee nests
(as in Hogendoorn and Velthuis, 1993;Prager, 2014), or
the consequences of shared foraging duties in ant and wasp
foundress associations (Cahan and Fewell, 2004). Importantly,
the exchange of theories and ideas between vertebrate and
invertebrate sociality research should be bi-directional. Insights
from Hymenopteran systems have the potential to overcome
many of the limitations of work with vertebrate systems.
Especially given their short generation times and experimental
tractability in lab settings, insect systems have the potential to fill
gaps in our broader understanding of the long-term direct fitness
outcomes of cooperation over multiple generations.
Current understanding of social evolution among unrelated
individuals is constrained by limited knowledge of the full
diversity of Hymenopteran taxa that form non-kin groups.
The incidence of non-kin cooperation is likely to be greatly
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Ostwald et al. Non-kin Cooperation in the Hymenoptera
underestimated due to the tendency of non-kin groups to occur
within otherwise solitary populations (Ross and Matthews, 1991;
Michener, 2007;Heinze et al., 2017), and due to limitations
associated with quantifying relatedness in some species. This
knowledge gap can be addressed with simple behavioral
techniques (e.g., mark-recapture or observations of nest joining;
Abrams and Eickwort, 1981;Peso and Richards, 2011) and
inexpensive genotyping methods (e.g., microsatellites; Moore and
Kukuk, 2002). Other techniques, like radio-frequency tracking
(Sumner et al., 2007;Kissling et al., 2014), have the potential to
reveal nest switching patterns that maintain low relatedness in
some insect groups. A first priority in future research on non-kin
sociality should be to expand our understanding of the diversity
of non-kin systems via integrated behavioral and molecular
research. Many of the species highlighted in Table 1 currently
possess incomplete evidence for non-kin sociality, especially
among the wasps and bees. It is likely that non-kin groups form
among many other, related species for which kinship has not yet
been quantified. The same may be true for similarly structured
social groups outside the Hymenoptera, especially among the
termites, which can form polygynous colonies through colony
fusion (DeHeer and Vargo, 2004,Deheer and Vargo, 2008;Korb
and Roux, 2012).
Beyond characterizing the organization and formation of these
groups, studies that relate social founding strategies to ecological
conditions or compare social and solitary strategies in sympatry
represent promising directions for future research. Particularly
illuminating would be controlled experimental studies relating
social condition to ecological conditions and, especially, to fitness
outcomes. The abundance of facultatively social non-kin groups
provides diverse, experimentally tractable systems in which social
condition can be observed and even manipulated within a single
species, thus avoiding the pitfalls of comparisons across species
with very different evolutionary histories. Manipulative studies
such as these could rigorously test hypotheses about proposed
drivers of sociality, providing insights into the ecological
conditions at the origins of group living.
CONCLUSION
The ecological drivers of non-kin cooperation represent a
highly overlapping suite of conditions that interact to constrain
solitary reproductive opportunities. Integrative research that
accommodates these interactions has the potential to reveal
common principles underlying social evolution broadly across
animal taxa and across kin and non-kin groups. Our current
understanding of the full diversity of non-kin sociality in the
Hymenoptera is highly limited, but existing analyses suggest
that groups containing non-relatives are more widespread
than previously acknowledged. Future work should quantify
relatedness across a diversity of species, and leverage these
systems as models for evaluating the ecological conditions that
favor group formation. Studies of known non-kin groups in the
Hymenoptera have emphasized the role of harsh, competitive
environments in selecting for cooperative strategies even in
the absence of indirect fitness benefits. These findings parallel
patterns more broadly across animal groups that indicate
a major role for ecological constraints in shaping diverse
forms of sociality.
AUTHOR CONTRIBUTIONS
MO wrote the main manuscript. BH wrote the section on ant
sociality. All authors contributed to manuscript editing and
developing the concept for the review.
FUNDING
This research was supported by an NSF Graduate Research
Fellowship to MO and a Momental Foundation Mistletoe
Research Fellowship to MO.
ACKNOWLEDGMENTS
We thank Andrew Suarez and Michael Goodisman for their
helpful feedback on a draft of the manuscript. We also thank
Elizabeth Cash, Nicholas Dorian, and Meagan Simons for their
photographs. Finally, we thank two reviewers whose comments
improved the manuscript, as well as the editors of this special
issue for useful feedback.
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