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Metrics of colony growth and survival during the first ten months post-founding in colonies initiated by one, two, or four queens, including: (A) Colony size (worker number), (B) per-queen worker production estimated as the mean worker number divided by the number of queens, (C) survival probability of individual queens, and (D) survival probability of colonies, where colony survival is defined as the survival of at least one queen. Points and bars represent means and standard errors, and the dashed vertical line marks the week in which the majority of colonies experienced first-worker emergence.
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The fitness consequences of cooperation can vary across an organism’s lifespan. For non-kin groups, especially, social advantages must balance intrinsic costs of cooperating with non-relatives. In this study, we asked how challenging life history stages can promote stable, long-term alliances among unrelated ant queens. We reared single- and multi-...
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... It remains unclear how the two effects-lower brood metabolic rate and increased worker brood-tending behaviour due to the presence of brood-interact to quantitatively affect colony metabolic rate when the amount of brood in the colony varies. In harvester ant colonies, the relative allocation of workers to the task of brood care tends to decline as colonies grow beyond early stages of development [28,29], reflecting a potential pattern in social insect colonies of more intense focus on brood production at smaller sizes [30]. Similarly, larger Temnothorax rugatulus ant colonies have lower brood : worker ratios [7], and in Florida harvester ants (Picipes badius) colonies, the colony-level brood : worker ratio declined from an average of 1.4 in incipient colonies to 0.33 in colonies of 6000 workers [31]. ...
In animals, metabolic rates during ontogeny often scale differently from the way they do in cross-species or population comparisons, with near-isometric scaling patterns more often observed during juvenile growth. In multiple social insect taxa, colony metabolic rate scales hypometrically across species or populations at the same developmental stage, but metabolic patterns during ontogeny have not been examined for any social insect species. We performed the first ontogenetic study of social metabolic scaling in harvester ant colonies (Pogonomyrmex californicus) over 3.5 years as they grew from 52 ± 12 to 767 ± 380 workers. Our data reveal iso- and hypermetric metabolic scaling during the first 20 months of growth, transitioning to hypometric scaling (scaling exponent = 0.93) thereafter. We discovered that the fraction of colony as brood has dual effects on colonial metabolic rate. A higher fraction of the colony that is brood decreases colonial metabolic rate because brood has approximately half the mass-specific metabolic rates of adult ants. Conversely, metabolic rate and activity of adult ants increase as this fraction increases. We further developed a nonlinear composition model, which shows that the maximal colony metabolic rate occurs when 29% of the colony mass is brood, suggesting that demographic changes and colony size may interact to drive the metabolic scaling.
... The propensity to cooperate in P. californicus queens is genetically based and shows population-level variation (Helmkampf et al. 2016;Overson et al. 2016). Queens from several localized populations in southern California form non-kin social groups during colony initiation (pleometrosis) that persist throughout the lifespan of the colony (primary polygyny; Rissing et al. 2000;Johnson 2004;Helms Cahan and Fewell 2004;Overson et al. 2016;Haney and Fewell 2018;Ostwald et al. 2021;Haney et al. 2023). Colonies from polygynous populations contain an average of 2.6 queens (range of 2-6), and all queens within a colony contribute to production of workers, gynes, and males (Haney et al. 2023). ...
... In P. californicus, populations with high incidences of polygyny tend to have greater population densities and may occur in more resource-limited areas (Haney and Fewell 2018). These lead to more intense intraspecific competition and favor multiqueen groups that can progress more quickly through the earliest and most vulnerable stages of nest initiation, at the cost of giving up the opportunity to eventually be the sole reproductive individual in the colony (Haney and Fewell 2018; Ostwald et al. 2021). ...
... Nest initiation by ant queens has extremely high mortality risks (> 99% failure; Cole 2009) and requires substantial use of body lipid and protein stores (Wheeler and Buck 1996;Hahn et al. 2004;Helms 2018;Matte and Billen 2021), so energetic costs or savings associated with grouping could be important to fitness Cole 1995, 2003;Johnson 2004;Cole 2009;Clark and Fewell 2014a, b). During nest initiation, ant queens must perform all the tasks needed to start a new colony and rear offspring, until the first workers emerge (Hölldobler and Wilson 1990;Ostwald et al. 2021). To establish pleometrotic associations, newly mated P. californicus queens must walk around to find other queens. ...
Cooperative behavior by nonrelatives is an evolutionary puzzle, because costs of cooperation are often strong while selective factors favoring cooperative groups remain unclear. In some populations of the seed harvester ant Pogonomyrmex californicus, unrelated queens form groups at colony founding (pleometrosis), whereas in other populations, colonies are initiated by single queens (haplometrosis). We tested the hypothesis that energetic savings of grouping contribute a benefit that may enhance queen success during colony founding and early growth for pleometrotic colonies. We measured metabolic rates and locomotor activity of individuals or pairs of freshly collected, newly mated P. californicus queens from pleometrotic and haplometrotic populations. Population source did not significantly affect metabolic rates, but paired queens from both populations had mass-specific metabolic rates only 86% of those of individual queens. The metabolic effect of grouping was not explained by differences in locomotion. To test whether this degree of energetic saving could be biologically significant, we assessed metabolic rate, body mass, and egg production for pleometrotic pairs at four time points of colony founding and compared the energetic content of stored lipid to energy use up to the point of worker emergence. Metabolic rates dropped over time for queens, as did body mass, and gas exchange switched from continuous to discontinuous, suggestive of metabolic suppression. Total joules required for queens to reach the worker emergence stage were 1.5 times the energy content of stored lipids, consistent with the need for foraging for these queens, and supporting the hypothesis that energetic savings of grouping can be beneficial by extending energetic stores and reducing the need for risky foraging.
... Our finding that foundations with workers survive and grow better than those without workers parallels the higher survival and growth of colonies founded by several queens (pleometrosis) compared to those founded by a solitary queen (haplometrosis) in some ant species displaying a polymorphism in this respect (Tschinkel and Howard 1983;Rissing and Pollock 1991;Ostwald et al. 2021). In both cases, the larger initial group size is the determinant of the higher growth rate, and larger foundations outgrow and outcompete smaller ones through scramble competition for resources or through aggressive behaviours such as territoriality or brood raiding depending on species' biology. ...
Dispersal and establishment strategies are highly variable. Each strategy is associated with specific costs and benefits, and understanding which factors favour or disfavour a strategy is a key issue in ecology and evolution. Ants exhibit several strategies of establishment, i.e. of colony foundation. Some species rely on winged queens that found new colonies alone when others found with accompanying workers (colony fission). The benefits conferred by these workers have been little studied and quantified, because comparing the costs and benefits of solitary foundation vs. colony fission is difficult when comparing different species. We investigated this using the ant Myrmecina graminicola, one of the few species that use both strategies. Young mated queens were allowed to found new colonies in the laboratory, with either zero (solitarily), two or four workers (colony fission). The presence of workers increased both survival and growth of the foundations over the first year, with more workers yielding higher growth. Few workers (as little as two workers) were sufficient to provide benefits, suggesting that in M. graminicola the strategy of colony fission may not dramatically decrease the number of new colonies produced compared to solitary foundation. Because queens performing solitary foundation or colony fission differ in dispersal (by flight vs. on foot), our results support the hypothesis that these two strategies of foundation coexist along a competition–colonization trade-off, where solitary foundation offers a colonization advantage, while colony fission has a competitive advantage.
... Polygyny in both P. californicus and Polistes spp. leads to increased colony size, conferring group augmentation benefits such as increased foraging activity (85,87) and survival (86,87). Thus, group augmentation benefits may also drive the evolution of reproductive sharing in invertebrate societies with complex social structure, particularly those living in unpredictable environments where, like vertebrates, such species are most common (87). ...
... Polygyny in both P. californicus and Polistes spp. leads to increased colony size, conferring group augmentation benefits such as increased foraging activity (85,87) and survival (86,87). Thus, group augmentation benefits may also drive the evolution of reproductive sharing in invertebrate societies with complex social structure, particularly those living in unpredictable environments where, like vertebrates, such species are most common (87). ...
... leads to increased colony size, conferring group augmentation benefits such as increased foraging activity (85,87) and survival (86,87). Thus, group augmentation benefits may also drive the evolution of reproductive sharing in invertebrate societies with complex social structure, particularly those living in unpredictable environments where, like vertebrates, such species are most common (87). ...
Although kin selection is assumed to underlie the evolution of sociality, many vertebrates-including nearly half of all cooperatively breeding birds-form groups that also include unrelated individuals. Theory predicts that despite reducing kin structure, immigration of unrelated individuals into groups can provide direct, group augmentation benefits, particularly when offspring recruitment is insufficient for group persistence. Using population dynamic modeling and analysis of long-term data, we provide clear empirical evidence of group augmentation benefits favoring the evolution and maintenance of complex societies with low kin structure and multiple reproductives. We show that in the superb starling (Lamprotornis superbus)-a plural cooperative breeder that forms large groups with multiple breeding pairs, and related and unrelated nonbreeders of both sexes-offspring recruitment alone cannot prevent group extinction, especially in smaller groups. Further, smaller groups, which stand to benefit more from immigration, exhibit lower reproductive skew for immigrants, suggesting that reproductive opportunities as joining incentives lead to plural breeding. Yet, despite a greater likelihood of becoming a breeder in smaller groups, immigrants are more likely to join larger groups where they experience increased survivorship and greater reproductive success as breeders. Moreover, immigrants form additional breeding pairs, increasing future offspring recruitment into the group and guarding against complete reproductive failure in the face of environmental instability and high nest predation. Thus, plural breeding likely evolves because the benefits of group augmentation by immigrants generate a positive feedback loop that maintains societies with low and mixed kinship, large group sizes, and multiple reproductives.
... The temporal factor consideration could be variable in function of the number of dealate queens initially taking part in colony foundation [20]. The cooperation of more queens to develop a colony is predictive of a significant fluctuation in the average period taken to establish a colony from embryonic stage towards a final stable juncture [70,71]. Incipient polygynous colonies reach maturity much earlier than monogynous colonies since the former may produce a far more abundant work force and broods [20,13,16]. ...
The Asian weaver ant (Oecophylla smaragdina) is a natural enemy, generalist predator of diverse major pest species (i.e. the highly destructive oriental fruit fly Bactrocera dorsalis) in economically strategic agricultural landscapes in Australia and Southeast Asia countries. For effective implementation of the weaver ant for biological control of the invasive bagworms Metisa plana, the dominant pest in the oil palm plantation, its distribution was investigated in Malaysia. From 2018-2022, censuses were first carried out to record Oecophylla colonies presence. Oecophylla colonies’ occupation patterns were monitored on 8 selected plantations. To distinguish between brood and barracks nests, 26 captured nests were evaluated to define the main predictor variable for its practical visual identification. More than 11000 palms with 10821 nests for over 500 colonies were sampled in this study. Results showed that O. smaragdina colonies distribution pattern exhibited three-dimensional ubiquitous occupation dominance. We also found that by observing the colony’s dense population spatial arrangements, it demonstrates them as spreading by waves featuring interconnected irregular geometrical patches shaped for each colony. The height to the ground nest location in palm canopies was the significant visual discriminant factor between Brood and barrack nests. Moreover, polydomous arboreal nesting behavior occupation occurred irrespective of palms or associated host plants sizes (≥ 3 m), throughout the year. However, colony nesting behaviors were polydomous and monodomous on shorter plants (≥ 2 m), while being strictly monodomous on small plants (≤ 1.5 m). Colonies occupied an average 3 to 4 palms yearly beginning from the newly founding phase up to the stable mature phase (3 to 4 years). Furthermore, we found that matured stable colonies (3 ≥ age ≥13) occupied 10-12 palms on average, on 800 m2 to 2500 m2 area delimited by a minimum average 20 m2 of “no ants land” zone between each colony. Our results suggest that a sustained agriculture system in this area would be possible with the presence of matured colonies nests exploitation which could provide an efficient biological control ecosystem service.
... Known as pleometrosis, this phenomenon has been documented in ants (Sommer and Hoelldobler, 1995;Choe and Crespi, 1997;Bernasconi and Strassmann, 1999;Johnson, 2004;Izzo et al., 2009;Offenberg et al., 2012;Eriksson et al., 2019), bees (Schwarz et al., 1998), wasps (Rau, 1931;Itô, 1986), termites (Hacker et al., 2005;Chiu et al., 2017), mites (Saito, 2009), aphids (MillerIII, 1998a;Miller, 1998b;Michaud and Belliure, 2000), and thrips Gilbert and Simpson, 2013). When cooperation persists throughout the life of the colony, it is called primary polygyny-as in the case described in this paper (Ostwald et al., 2021). ...
... In our study, foundress number influenced survival-with foundresses in social groups surviving longer than solitary foundresses, regardless of group size. In several earlier studies of this population, a similar survival advantage was reported for groups of between two and six queens (Johnson, 2004;Clark and Fewell, 2014;Shaffer et al., 2016;Ostwald et al., 2021), along with some suggestions that larger group sizes can facilitate enhanced survival rates. By founding in groups, queens may enhance their own survival by sharing the work of colony foundation, which can involve costly and dangerous tasks and includes excavation, brood care, and foraging (Bernasconi and Strassmann, 1999). ...
... Young colonies must likely contend with both predation from mature colonies as well as competition with other natal colonies. Our study captured only a narrow window at the beginning of the life of these colonies, but other work has demonstrated that the benefits of cooperative nest founding extend months into the early life of a colony, perhaps explaining why in addition to being pleometrotic, this population maintains primary polygyny in mature colonies, (Ostwald et al., 2021). In such contexts, a multilevel selection approach may be helpful in understanding the evolution of pleometrosis and related phenomena in social insect colonies (Rissing et al., 1989;Tsuji, 1995;Muir, 1996;Korb and Heinze, 2004;Reeve and Hölldobler, 2007;Dobata and Tsuji, 2013;Shaffer et al., 2016). ...
Cooperation in nature is usually between relatives, but unrelated individuals can also cooperate, requiring significant benefits to outweigh the costs of helping non-kin. Unrelated queens of the ant, Pogonomyrmex californicus, work together to found a new colony, a phenomenon known as pleometrosis. While previous studies have shown that pleometrosis improves queen survival and worker production, little is known of the behavioral interactions within nests that explain these advantages. We aimed to determine how the optimal group size for a small, simple social group is related to group productivity and the organization of work. Collecting queens from a known pleometrotic population, we established nests with either one, three, six, or nine foundresses and observed the resulting nascent colonies for 50 days. We found that queens in social founding groups survived longer and had higher productivity. While all social groups were equally successful in producing workers, intermediate-sized groups were most successful in terms of per capita production. Inactivity increased with group size. In addition, the proportion of essential colony growth tasks performed (such as foraging and brood care) was lowest in both solitary-founded groups and in groups of nine queens. As a result, intermediate sized groups outperformed both solitary queens and groups of nine in the efficiency with which they converted eggs into workers. These results emphasize the benefits of cooperation and the ways in which group size can influence fitness and the allocation of labor in social groups.
... Surprisingly, eusocial insects sometimes engage in non-kin cooperative behaviors (Jackson, 2007;Helantera et al., 2009;Leniaud et al., 2009;Lehmann and Rousset, 2010;Moffett, 2012;Boomsma and d'Ettorre, 2013;Hakala et al., 2020;Ostwald et al., 2021). Such actions are unexpected because eusocial insects are the paradigm of kin cooperative actions. ...
... There are a number of benefits to pleometrotic associations (Bernasconi and Strassmann, 1999;Ostwald et al., 2021;Teggers et al., 2021), notably the ability to produce workers more quickly than through haplometrosis. Many species that form pleometrotic associations are highly territorial, and workers from established colonies may destroy or raid incipient colonies in their immediate vicinity. ...
Eusociality represents an extreme form of social behavior characterized by a reproductive division of labor. Eusociality necessarily evolved through kin selection, which requires interactions among related individuals. However, many eusocial taxa also show cooperation between non-kin groups, challenging the idea that cooperative actions should only occur among relatives. This review explores the causes and consequences of non-kin cooperation in ants. Ants display a diversity of behaviors that lead to non-kin cooperation within and between species. These interactions occur among both reproductive and non-reproductive individuals. The proximate and ultimate mechanisms leading to non-kin cooperative interactions differ substantially depending on the biotic and abiotic environment. We end this review with directions for future research and suggest that the investigation of non-kin cooperative actions provides insight into processes leading to social evolution.
In ants, which are all eusocial, social polymorphism exists in the form of a variable number of queens. The occurrence of colonies with a single queen (monogynous) or multiple queens (polygynous) within a species is found in about 15% of ant species, offering various model systems to assess the life-history differences between the two social forms. Polygynous colonies are assumed to be better competitors due to larger colony size and higher colony growth, whereas monogynous colonies are supposed to rely on a colonizer strategy as they are founded solitarily by larger winged queens that disperse by flight. The ant Myrmecina graminicola harbors a social polymorphism associated with a wing polymorphism in queens, both being determined by a different supergene with monogynous queens being mostly winged and polygynous queens being always apterous. By comparing colonies sampled in the same population, we showed that polygynous colonies with apterous queens and monogynous colonies with winged queens did not differ in the number of workers and larvae at the time of collection. Accordingly, once reared in the laboratory, these colonies produced a similar number of pupae and adults (workers or sexual individuals), probably from the larvae already present at the time of collection. However, polygynous colonies produced more eggs and new larvae in the laboratory than their monogynous counterparts. We discuss why this larger brood production of polygynous colonies was not reflected by a larger colony size in the field, and what the consequences of similar colony growth and productivity between the social forms would mean for the maintenance of genetic polymorphisms.
With their unique colony structure, competition between ants (Hymenoptera: Formicidae) can be particularly intense, with colonies potentially willing to sacrifice large number of individuals to obtain resources or territory under the right circumstances. In this review, we cover circumstances in which ant competition escalates into combat, battle strategies and tactics, and analysis methods for these battles. The trends for when colonies choose to fight can vary greatly dependent on the species and situation, which we review in detail. Because of their large group sizes, ant conflicts can follow different patterns than many other species, with a variety of specialist adaptations and battle strategies, such as specialized worker classes and the need to rapidly recruit large number of compatriots. These same large group sizes also can make ant fighting amenable to mathematical analysis, particularly in the context of Lanchester’s laws that consider how total numbers influence the outcome of a confrontation. Yet, dynamic behavior can often disrupt idealized mathematical predictions in real-world scenarios, even though these can still shed light on the explanations for such behavior. We also systematically cover the literature on battles between groups of ants, presenting several other interesting studies on species with unique colony organization, such as army ants and leafcutter ants.
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.
