Unrelated Helpers in a Primitively Eusocial Wasp: Is Helping Tailored Towards Direct Fitness?

Leadbeater, Ellouise; Carruthers, Jonathan M.; Green, Jonathan P.; Heusden, Jasper van; Field, Jeremy

doi:10.1371/journal.pone.0011997

Cited by 32 publications

(56 citation statements)

References 34 publications

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“…Most paradoxically, fertile unrelated wasps join (and are allowed to join) groups with no differential treatment (49,50). Relatedness has no predictive role in establishing aggression patterns or dominance hierarchies on nests (48,50).…”

Section: Discussionmentioning

confidence: 99%

Kinship, greenbeards, and runaway social selection in the evolution of social insect cooperation

Nonacs

2011

Proc. Natl. Acad. Sci. U.S.A.

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Social Hymenoptera have played a leading role in development and testing of kin selection theory. Inclusive fitness models, following from Hamilton's rule, successfully predict major life history characteristics, such as biased sex investment ratios and conflict over parentage of male offspring. However, kin selection models poorly predict patterns of caste-biasing nepotism and reproductive skew within groups unless kin recognition constraints or grouplevel selection is also invoked. These successes and failures mirror the underlying kin recognition mechanisms. With reliable environmental cues, such as the sex of offspring or the origin of male eggs, predictions are supported. When only genetic recognition cues are potentially available, predictions are not supported. Mathematical simulations demonstrate that these differing mechanisms for determining kinship produce very different patterns of behavior. Decisions based on environmental cues for relatedness result in a robust mixture of cooperation and noncooperation depending on whether or not Hamilton's rule is met. In contrast, cooperation evolves under a wider range of conditions and to higher frequencies with genetic kin recognition as shared greenbeard traits. This "excess of niceness" matches the existing patterns in caste bias and reproductive skew; individuals often help others at an apparent cost to their inclusive fitness. The results further imply a potential for greenbeardtype kin recognition to create arbitrary runaway social selection for shared genetic traits. Suggestive examples in social evolution may be alloparental care and unicoloniality in ants. Differences in kin recognition mechanisms also can have consequences for maintenance of advantageous genetic diversity within populations.kin nepotism | phenotypic matching | social heterosis S eemingly overtly altruistic behavior, such as individuals accepting sterility, has puzzled evolutionary biologists since the time of Darwin. The first truly predictive framework for how reducing one's own reproduction could be adaptive came from the seminal work of W. D. Hamilton (1). His key insight was that fitness is "inclusive" of both an individual's direct reproduction and indirect gains arising through help provided to genetic relatives. Gains in indirect fitness, often labeled as "kin selection," recast altruism as an ultimately selfish act. Help relatives if the benefit provided (b), prorated by the genetic relatedness of the recipient (r), exceeds the cost to self (c). This is Hamilton's rule: Helping is adaptive if br > c.More than any other taxonomic group, social Hymenoptera (ants, bees, and wasps) sit at an apparent peak of kin selection, with many species having morphologically sterile workers. Kin selection and applications of Hamilton's rule, however, extend far the beyond the evolution of sterile castes to examine many aspects of cooperative (and noncooperative) behavior (2). Thus, social insects have had a pivotal role in the development of kin selection theory and its elevation to being the...

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Section: Discussionmentioning

confidence: 99%

Kinship, greenbeards, and runaway social selection in the evolution of social insect cooperation

Nonacs

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…However, mean relatedness is much lower (0.13-0.53) in other species such as P. aurifer [11] and P. dominula [12][13][14][15][16]. In these species, completely unrelated pairs of co-foundresses are common, with 15% (Spain) or 35% (Italy) of foundresses being unrelated in populations of P. dominula [13,15] (figure 2). In the Spanish populations, more than 80% of co-foundress groups contain at least one foundress that is unrelated or only distantly related to other group members [16].…”

Section: Unrelated Co-foundresses In Polistesmentioning

confidence: 99%

“…The latter context is useful because it can lead to serious, escalated fights between the original dominant and the rank 2, fights of a kind rarely seen otherwise [26]. Leadbeater et al [13] also tested whether unrelated subordinates tend to occupy higher inheritance ranks, as expected if they behave strategically to maximize their direct fitness.…”

Section: Behavioural Differences Between Unrelated Subordinates and Rmentioning

confidence: 99%

“…A first analysis of these behavioural data suggested that unrelated subordinates behave no differently to relatives of the dominant [13]: they forage as much, are no less aggressive in nest defence, and no more aggressive when the opportunity to inherit arises or when an experimentally removed dominant returns to the nest. Furthermore, unrelated subordinates occupy no higher inheritance ranks than relatives of the dominant.…”

Section: Behavioural Differences Between Unrelated Subordinates and Rmentioning

confidence: 99%

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Cooperation between non-relatives in a primitively eusocial paper wasp,Polistes dominula

Field

Leadbeater

2016

Phil. Trans. R. Soc. B

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One contribution of 18 to a theme issue 'The evolution of cooperation based on direct fitness benefits'. In cooperatively breeding vertebrates, the existence of individuals that help to raise the offspring of non-relatives is well established, but unrelated helpers are less well known in the social insects. Eusocial insect groups overwhelmingly consist of close relatives, so populations where unrelated helpers are common are intriguing. Here, we focus on Polistes dominula-the best-studied primitively eusocial wasp, and a species in which nesting with non-relatives is not only present but frequent. We address two major questions: why individuals should choose to nest with non-relatives, and why such individuals participate in the costly rearing of unrelated offspring. Polistes dominula foundresses produce more offspring of their own as subordinates than when they nest independently, providing a potential explanation for co-founding by non-relatives. There is some evidence that unrelated subordinates tailor their behaviour towards direct fitness, while the role of recognition errors in generating unrelated co-foundresses is less clear. Remarkably, the remote but potentially highly rewarding chance of inheriting the dominant position appears to strongly influence behaviour, suggesting that primitively eusocial insects may have much more in common with their social vertebrate counterparts than has commonly been thought.

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“…Among vertebrates, evidence for the importance of indirect fitness benefits exists for some bird species, for example, Seychelles warblers 5 , Long-tailed tits 6,7 and Bell miners 8,9 . However, several studies did not find kinship effects on helping behaviour as predicted by kin-selection theory (in mammals 10 ; fish 11 ; birds 12 ; insects 13 ) and substantial help is sometimes shown by unrelated individuals 9,[14][15][16] . Furthermore, unrelated helpers exist in all aforementioned systems.…”

mentioning

confidence: 97%

Kinship reduces alloparental care in cooperative cichlids where helpers pay-to-stay

et al. 2013

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Alloparental brood care, where individuals help raising the offspring of others, is generally believed to be favoured by high degrees of relatedness between helpers and recipients. Here we show that in cooperatively breeding cichlids, unrelated subordinate females provide more alloparental care than related ones when kinship between dominant and subordinate group members is experimentally manipulated. In addition, unrelated helpers increased alloparental care after we simulated egg cannibalism by helpers, an effect not shown by related helpers. By supporting predictions of pay-to-stay theory, these results suggest that in Neolamprologus pulcher, reciprocal commodity trading is important for the decision of subordinates to invest in care of the dominants' offspring.

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Unrelated Helpers in a Primitively Eusocial Wasp: Is Helping Tailored Towards Direct Fitness?

Cited by 32 publications

References 34 publications

Kinship, greenbeards, and runaway social selection in the evolution of social insect cooperation

Kinship, greenbeards, and runaway social selection in the evolution of social insect cooperation

Cooperation between non-relatives in a primitively eusocial paper wasp,Polistes dominula

Kinship reduces alloparental care in cooperative cichlids where helpers pay-to-stay

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