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Polygyny and Poliandry

Two were the main biological features of wasp social life that puzzled Hamilton and that made their social systems an anomaly for his theory: polygyny, say the presence at nest foundation of multiple egg-laying and potentially unrelated females (Hamilton 1964b), and polyandry or multiple mating, say the fact that the reproductive individuals mate multiple times (Hamilton 1964b). Both polyandry and polygyny lower the degree of relatedness in colonies. Yet, the haplodiploidy hypothesis suggested that the frequent evolution of sterile workers in Hymenoptera might be the result of the unusually high relatedness of hymenoptera sisters due to male hap- loidy. Therefore, both polyandry and polygyny posed important challenges to Hamilton’s explanations of the evolution of social life.

Poliandry is common in Hymenoptera, and especially prevalent in wasps. In the Application to the Darwin Fellowship, after talking about his intention to work on wasps, Hamilton wrote that one of the main reasons for him to go to Brazil and spend time in the lab of the famous entomologist W.E. Kerr was: . to learn Kerr’s technique of determining the occurrence of multiple mating Hymenoptera by sperm counts, and to apply it to a variety of social and semi-social Hymenoptera. This question of multiple mating has an important bearing on my idea of how social behavior might have evolved in the group” (Z1XJO/1/5, May, 15, 1963).

In Part II of the 1964 work, Hamilton reported the problematic case of multiple mating in Hymenoptera and wrote: “Clearly multiple insemination will greatly weaken the tendency to evolve worker-like altruism” (1964b, 33). By mating with multiple males, the queen’s progeny becomes very genetically diverse. Thus, multiple mating decreases the degree of relatedness among self-sacrificing workers and the queen or her brood. This makes it difficult to explain why the workers would perform altruistic behaviors in such colonies. According to Hamilton, this clearly posed a challenge to the power of the haplodiploidy hypothesis and raised the problem of how self-sacrificing behaviors in wasps were even possible, if the colonies are made out of workers with different genetic origins. He wrote: “It does seem at first rather surprising that altruism towards sisters so much less related than full sisters can be maintained at its observed pitch of perfection” (1964b, 34).

Besides multiple-mating, Polygyny, the phenomenon of multiple egg-laying queens was another aspect that made wasp societies somewhat contradictory to Hamilton’s theory. Hamilton argued that: “Clearly this social mode presents a problem to our theory. Continuing cycle after cycle colonies can come into existence in which some individuals are almost unrelated to one another.” (Hamilton 1964b, 36). In polygynous colonies, the workers attend a brood produced by more than one female, which means that they are not attending a brood composed only by full sisters. Also in this case, the puzzling nature of polygyny is due to the fact that it lowers the degree of relatedness in the colony. According to Hamilton, rather than favoring altruistic behavior, polygyny seems to be favorable to the spreading of genes causing selfish behaviors, which would lower the efficiency of social life. Yet, and here is the puzzle: “(...) it does not seem to do the colonies much harm and the species concerned are highly successful in many cases” (Hamilton 1964b, 36).

Hamilton looked at the polygyny puzzle in two groups of the Vespidae family: the subfamily Polybiinae and the genus Polistes belonging to the subfamily Polistinae (Richards and Richards 1951). Polybiinae are mostly swarm founding wasps, where colony reproduction happens by swarming with several fertilized queens. In most species of this subfamily, there are at least several queens that engage in egg-laying on each nest (Ducke 1914; Richards and Richards 1951). In the case of swarm founding wasps, the problems posed by polygyny is extremely severe due to the high number of egg laying queens. In this case, Hamilton noticed, the probability is higher to obtain colonies where individuals are almost unrelated to each other.

The situation is slightly different in the partially polygynous and partially monogynous Polistes, as wasps of this genus show different modes of nest foundation depending on the climate and on the latitude (Richards and Richards 1951). Hamilton wrote: “The geographic distribution of the association phenomenon in Polistes is striking” (Hamilton 1964b, 37). Polisteshave different modes of colony foundation that go from mostly monogynous in colder regions to polygynous in the tropics. In temperate regions, usually, several wasps contribute to the foundation of the nest, but one of them becomes the only egg-laying and dominant one (Pardi 1942, 1948). The rest of the wasps, the auxiliaries or subordinates cannot reproduce and, if any, they succeed in laying only a few eggs. But with many of Polistes species, mostly in warmer climates, nest foundation is carried out by two or more fertilized queen-sized wasps (Pardi 1942, 1948). This condition led in earlier studies on Polistes to discuss whether the polygyny at nest foundation in Polistes was real or fictitious (Pardi 1942).

Hamilton thought that, hierarchy formation in Polistes posed a challenge to his hypothesis, as he found difficult to explain the ready acceptance of non-reproductive roles by the auxiliaries (Hamilton 1964b). Although Hamilton was not able to explain this phenomenon, he mentioned that: “There is good reason to believe that the initial nest-founding company is usually composed of sisters, which brings the phenomenon closely into line with the pleometrosis of the polybiines” (Hamilton 1964b, 37). Some years later, Hamilton was still puzzled by whether or not the foundresses of Polistes nests were actually sisters or not. In a letter to M.J. West-Eberhard who had recently published an article in Science about the evolution of social behavior in Polistes (West-Eberhard 1967), Hamilton asked West- Eberhard about the evidence she had the degree of relatedness among the founding wasps in two different species of Polistes (West-Eberhard 1967, 1969).

 
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