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Kinship, Greenbeards, and Runaway Social Selection in the Evolution of Social Insect Cooperation

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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 Peter Nonacs1 Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095 Edited by John C. Avise, University of California, Irvine, CA, and approved May 19, 2011 (received for review February 10, 2011) Social Hymenoptera have played a leading role in development tion than by nepotism toward kin (5). Finally, the status of social and testing of kin selection theory. Inclusive fitness models, fol- insects as being a paramount example of kin selection has been lowing from Hamilton’s rule, successfully predict major life history questioned, with kin selection relegated to being a dissolutive characteristics, such as biased sex investment ratios and conflict force that primarily selects against cooperation and sociality (6). over parentage of male offspring. However, kin selection models The response to these criticisms from defenders of inclusive fitness poorly predict patterns of caste-biasing nepotism and reproductive modeling and kin selection has been simultaneously vigorous and skew within groups unless kin recognition constraints or group- dismissive (3, 7–12). level selection is also invoked. These successes and failures mirror The current conceptual maelstrom offers an opportunity for a the underlying kin recognition mechanisms. With reliable environ- critical appraisal of the effects of kin selection in the social Hy- mental cues, such as the sex of offspring or the origin of male eggs, menoptera. Considering a model or hypothesis as either a failure or predictions are supported. When only genetic recognition cues are success is highly subjective. No single model can be expected to be potentially available, predictions are not supported. Mathematical 100% accurate for all taxonomic groups and in all situations. It is simulations demonstrate that these differing mechanisms for de- nevertheless fair to categorize a model as failing when a strong termining kinship produce very different patterns of behavior. Deci- majority of studies reject its predictions. Conversely, models that sions based on environmental cues for relatedness result in a robust are consistently supported by data are valued for accurately mixture of cooperation and noncooperation depending on whether tracking evolutionary outcomes. By such standards, and contrary or not Hamilton’s rule is met. In contrast, cooperation evolves under to its critics, kin selection theory has had major successes. However, a wider range of conditions and to higher frequencies with genetic contrary to its apologists, kin selection theory also has had some kin recognition as shared greenbeard traits. This “excess of nice- major failures. I will briefly review within the social Hymenoptera ness” matches the existing patterns in caste bias and reproductive two successes, (i) sex investment ratios and (ii) conflict over re- skew; individuals often help others at an apparent cost to their in- production by workers (i.e., worker policing), and two failures, (i) clusive fitness. The results further imply a potential for greenbeard- caste-biasing nepotism and (ii) reproductive skew theory. I will type kin recognition to create arbitrary runaway social selection for thereafter consider the mechanism for how kin are recognized as shared genetic traits. Suggestive examples in social evolution may the driving force for the observed pattern of success and failure. be alloparental care and unicoloniality in ants. Differences in kin These four topics are chosen because I believe the underlying recognition mechanisms also can have consequences for mainte- theory for the kin selective predictions is sound and that the nance of advantageous genetic diversity within populations. possibility for kin nepotism to evolve is at least potentially pres- ent. This differs from two other cases, where kin selection pre- kin nepotism | phenotypic matching | social heterosis dictions are suggested to have failed: the haplodiplody and monogamy hypotheses (4). First, cooperative breeding has re- eemingly overtly altruistic behavior, such as individuals ac- peatedly evolved in the haplodiploid Hymenoptera. Haplodiplody Scepting sterility, has puzzled evolutionary biologists since the creates a genetic asymmetry, such that a female is more related time of Darwin. The first truly predictive framework for how to her full sister (r = 0.75) than she is to her own offspring (r = reducing one’s own reproduction could be adaptive came from 0.5). Therefore, if a singly mated mother produces a female- the seminal work of W. D. Hamilton (1). His key insight was that biased offspring sex ratio, it is genetically more advantageous fitness is “inclusive” of both an individual’s direct reproduction for a daughter to help her mother raise more sisters. However, and indirect gains arising through help provided to genetic rel- the balance of evidence from existing species where cooperative fi atives. Gains in indirect fitness, often labeled as “kin selection,” breeding is facultative nds that such species are not monoga- recast altruism as an ultimately selfish act. Help relatives if the mous, do not predictably bias sex ratios toward females, or both benefit provided (b), prorated by the genetic relatedness of the (2). Hence, the haplodiploidy hypothesis is not a robust test of kin recipient (r), exceeds the cost to self (c). This is Hamilton’s rule: selection because the required patterns of genetic relatedness br > c likely did not exist in the putative ancestors of eusocial species Helping is adaptive if . “ ” More than any other taxonomic group, social Hymenoptera (13). The second example is the monogamy hypothesis, where (ants, bees, and wasps) sit at an apparent peak of kin selection, cooperative breeding is predicted to be more likely to evolve in with many species having morphologically sterile workers. Kin species where family groups are full siblings because of monog- 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, This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “In the Light of Evolution V: Cooperation and Conflict,” held January 7–8, 2011, social insects have had a pivotal role in the development of kin at the Arnold and Mabel Beckman Center of the National Academies of Sciences and selection theory and its elevation to being the dominant evolu- Engineering in Irvine, CA. The complete program and audio files of most presentations tionary paradigm for the study of cooperation and conflict. To are available on the NAS Web site at www.nasonline.org/SACKLER_cooperation. date, there have been hundreds of tests of kin selection pre- P.N. designed research, performed research, analyzed data, and wrote the paper. dictions in social insects (3). However, despite this track record The author declares no conflict of interest. of remarkable utility, kin selection theory has recently become This article is a PNAS Direct Submission. embroiled in controversy. The mathematics of inclusive fitness 1E-mail: [email protected]. modeling have been directly challenged (4). The evolution of This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. cooperation is argued as better explained by group-level selec- 1073/pnas.1100297108/-/DCSupplemental. 10808–10815 | PNAS | June 28, 2011 | vol. 108 | suppl. 2 www.pnas.org/cgi/doi/10.1073/pnas.1100297108 Downloaded by guest on October 2, 2021 amy (14). However, a gene-based model for the evolution of nieces (if queens are sisters) to totally unrelated. Therefore, any cooperation found that helping actually often tended to spread worker cohort that manages to have its full sisters preferentially more rapidly through populations with polygamy (15). This may be raised as the future reproductives should significantly increase its an instance where the underlying kin selection model actually fitness. Careful observation, however, has yet to find any signif- produces erroneous predictions [as postulated by Nowak et al. (4)]. icant conflict or favoritism over care giving under a wide range of scenarios. Honey bees (Apis mellifera), whose queens mate with Successes: Biased Sex Investment Ratios and Parentage of many males, have been studied most extensively for evidence of Males Through Worker Policing queen-rearing nepotism, but none has been conclusively dem- Another genetic consequence of the asymmetrical relatedness onstrated (22, 27). Similar studies in other social Hymenoptera patterns attributable to haplodiploidy is that with one singly have also failed to find nepotism in colonies with multiply mated mated queen (i.e., monogynous with monandry), workers are females or multiple queens (28, 29). more closely related to full sisters than to their brothers. This If facultatively cooperative groups are more productive than preference should drive female investment bias to the point the expected cumulative output of all their individual members, where it is exactly offset by the relative mating advantage of the it is possible for reproduction to be shared so that all individuals rare male sex (16). Thus, if workers control sex investment ratios, have higher fitness through cooperation (30). A fitness-maximizing a 3:1 female-to-male investment bias should result. Over 3 dec- division of the reproduction (i.e., the reproductive skew within ades of evidence has solidly
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