Multiple paternity or multiple queens: two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera
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Abstract Understanding the evolution of multiple mating by females (polyandry) is an important question in behavioural ecology. Most leading explanations for polyandry by social insect queens are based upon a postulated fitness benefit from increased intracolonial genetic diversity, which also arises when colonies are headed by multiple queens (polygyny). An indirect test of the genetic diversity hypotheses is therefore provided by the relationship between polyandry and polygyny across species, which should be negative if the genetic diversity hypotheses are correct. Here, we conduct a powerful comparative investigation of the relationship between polyandry and polygyny for 241 species of eusocial Hymenoptera (ants, bees and wasps). We find a clear and significant negative relationship between polyandry and polygyny after controlling for phylogeny. These results strongly suggest that fitness benefits resulting from increased intracolonial genetic diversity have played an important role in the evolution of polyandry, and possibly polygyny, in social insects.Keywords:
Eusociality
Polygyny
Inclusive fitness
One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation.
Eusociality
Inclusive fitness
Altruism
Social Evolution
Kin selection
Kin recognition
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The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene. Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness. Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false. Contrary to their claims, genetic relatedness is important and causal, workers are agents that can evolve to be in conflict with the queen, and eusociality is not so difficult to evolve. The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values. For example, all of their models implicitly assumed high relatedness, but modifying the model to allow lower relatedness shows that relatedness is essential and causal in the evolution of eusociality. Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection. This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.
Eusociality
Inclusive fitness
Kin selection
Social Evolution
Altruism
Fitness landscape
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Eusociality
Polygyny
Queen (butterfly)
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The hypothesis that obligate eusociality always evolved from ancestral states of strict lifetime monogamy implies that (1) facultatively eusocial lineages had to abandon multifemale breeding to achieve permanent morphologically differentiated castes, and (2) lineages of obligatorily eusocial insects had to independently re-evolve multifemale breeding when that served the inclusive fitness interests of nursing workers. Multiqueen nesting (eusocial polygyny) is known to be common across the ants, but rare in the corbiculate (eusocial) bees, the vespine wasps and the higher termites, but we show that this difference is mostly due to cases of obligate polygyny being restricted to the ants. This pattern is remarkably similar to the distribution of inquiline social parasites that use stealth rather than aggression to invade host colonies, which also repeatedly evolved in ants only. We explore the lineage-specific selection forces that have allowed or constrained de novo evolution of stable eusocial polygyny in Hamiltonian inclusive fitness terms. We argue that perennial life histories, male survival as stored sperm rather than as lifetime mates, and sib competition are possibly sufficient to explain the general prevalence of secondary polygyny across the obligatorily eusocial insects. We infer that obligate polygyny compromises eusocial 'soma' and 'germ-line' segregation in ways known to decrease developmental stability in metazoans, and we briefly evaluate the selection forces that reduce queen life span in highly, but probably not facultatively, polygynous species. We conclude that secondary polygyny in its obligate (ant) form resembles cooperative breeding with multiple 'tragedy of the commons' aspects, but in a peculiar manner because breeding females are selected to exploit the services of unmated workers rather than each other's. This breeding system has likely been maintained in ants because it allows modular extensions of colonies in directly adjacent habitat of similar quality without the re-emergence of sexual conflicts or unproductive local competition with kin.
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Obligate
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Haplodiploidy
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Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.
Inclusive fitness
Eusociality
Kin selection
Social Evolution
Altruism
Selfishness
Haplodiploidy
Group Selection
Reproductive value
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Polygyny
Eusociality
Swarming (honey bee)
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Abstract Understanding the evolution of multiple mating by females (polyandry) is an important question in behavioural ecology. Most leading explanations for polyandry by social insect queens are based upon a postulated fitness benefit from increased intracolonial genetic diversity, which also arises when colonies are headed by multiple queens (polygyny). An indirect test of the genetic diversity hypotheses is therefore provided by the relationship between polyandry and polygyny across species, which should be negative if the genetic diversity hypotheses are correct. Here, we conduct a powerful comparative investigation of the relationship between polyandry and polygyny for 241 species of eusocial Hymenoptera (ants, bees and wasps). We find a clear and significant negative relationship between polyandry and polygyny after controlling for phylogeny. These results strongly suggest that fitness benefits resulting from increased intracolonial genetic diversity have played an important role in the evolution of polyandry, and possibly polygyny, in social insects.
Eusociality
Polygyny
Inclusive fitness
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Polygyny
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When helping behaviour is costly, Hamiltonian logic implies that animals need to direct helpful acts towards kin, so that indirect fitness benefits justify the costs. We revisit inferences about nepotism and aggression in Hamilton's 1964 paper to argue that he overestimated the general significance of nepotism, but that other issues that he raised continue to suggest novel research agendas today. We now know that nepotism in eusocial insects is rare, because variation in genetic recognition cues is insufficient. A lower proportion of individuals breeding and larger clutch sizes selecting for a more uniform colony odour may explain this. Irreversible worker sterility can induce both the fiercest possible aggression and the highest likelihood of helping random distant kin, but these Hamiltonian contentions still await large-scale testing in social animals.
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Nepotism
Inclusive fitness
Kin selection
Kin recognition
Social Evolution
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Abstract Variation in the number of queens in colonies of social insects has become a subject of growing interest among sociobiologists. The increased concern with colony queen number is partly due to the discovery that multiple queen (polygynous) colonies are more common than previously recognized, especially among ants, in which polygyny may be the predominant social structure (Buschinger 1974; Rissing and Pollock 1988; Frumhoff and Ward 1992). More importantly, the mounting interest in polygyny stems from the realization that the origin and subsequent evolution of polygynous colonies from their presumed single-queen (monogynous) ancestors is an evolutionary enigma (Holldobler and Wilson 1977; Nonacs 1988), presenting many of the same theoretical challenges as does the origin and maintenance of eusociality (see Ross 1988a, 1989). For this reason, Rosengren and Pamila (1983) referred to the evolution of polygynous societies from monogynous ancestors as ‘sociality evolving a second time’. Thus research into the origin and evolution of polygyny and eusociality are highly complementary, with insights gained into one situation likely to shed light on the other.
Polygyny
Eusociality
Sociality
Social Evolution
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