Origin of Eusociality in Insects: Resolving the Problem ...

UDC 595.7:591.512.12

Entomological Review, 71 (4), ·1993

Origin of Eusociality in Insects: Resolving the Problem of the Polygynous Founding of Colonies within the Framework of the Concept of Haplodiploidy v. G. RADCHENKO Institute of Zoology, Ukrainian Academy of Sciences, Kiev Abstract. Hamilton's hypothesis of haplodiploidy offers the best explanation of the origins of eusociality in wasps; but the fad of polygynous colony foundation by bees and wasps has been a stumbling block to the acceptance of this hypothesis. Polygynous colonies are usually founded by sisters that divide the reproductive function; because they always develop into ordinary matrifilial colonies, the calculation of the genetic contribution of the gyne that performs the worker function at the time of polygynous colony foundation must be made over a period of time corresponding to a full cycle of colony development. This gyne produces nephews and nieces with which it has a mean genetic similarity of 3/8; over the same period of time, a solitary gyne produces second-generation offspring with which it has a genetic similarity of only 1/4. Polygynous colony foundation is supported by kin selection, but this occurs only after the beginning of eusociality. Keywords. Hymenoptera; social behavior. True social life, or eusociality, the essence of which is the presence of a nonreproductive caste of workers caring for the offspring of their own parents, is known in four groups of insects: bees, wasps. ants, and termites. The appearance and development of eusociality poses a serious problem for biologists inasmuch as it may not be explained from the position of classical natural selection, which is always opposed to. any restrictions on the reproductive possibilities of individuals. Thus, eusociality arises only when individual selection is blocked by certain factors or is defeated by some kind of specific type of selection in an opposing direction. Among various hypotheses proposed to explain the origin of eusociality, only the kin-selection theory offers a reasonable explanation of the genetic mechanism making it possible to support the existence of a sterile caste of workers. This theory, and, in particular, the associated concept of haplodiploidy, have a whole series of limiting conditions and have been disputed by many authors. The objective of this brief communication is to refute one of the principal arguments advanced against the concept of haplodiploidy (the origin and evolution of eusociality are examined in detail in Radchenko and Pesenko, 1992). The kin-selection theory. The key concept in the kin-selection theory developed by Hamilton (1964a) is the possibility for the individual to pass on its genes to the next generation not only directly through reproduction but also in caring for close relatives who carry copies of its genes to one or another degree. According to this theory, selection favors the appearance of a nonreproductive caste only when the fraction of genes shared by the worker and another's offspring that it is raising in the

-Originally published in Entoll1ologicheskoye obozreniye, Vol. 71, No. 3, 1992. pp. 505-509.

ISSNOO 13-8738193/0004-000 I 01993 Scripta Tecbnica.lnc .

colony (the family, the group of individuals jointly caring for the offspring in a nest) is greater than the fraction of shared genes passed on individually in independent reproduction. . In particular, if there is no difference in the mean genetic similarity of the nonreproductive individual to another's offspring and its own possible offspring, then for the mechanism postulated by the kin-selection theory to function, the number of foreign offspring raised by the individual must be somewhat greater than the number of offspring which it could have raised independently. The fulfillment of this condition is unrealistic inasmuch as eusociality is absent in typical diploid organisms for whom there is no difference in genetic similarity between their own offspring and the offspring of their parents.

The concept of haplodiploidy. Within the framework of the kin-selection theory, Hamilton (1964b) found the explanation for eusociality in Hymenoptera. In them there is an asymmetry in genetic similarity between individuals due to the haplodiploid mechanism of sex determination. As is known, in the Hymenoptera ｾ＠ s are produced by unfertilized haploid eggs through arrhenotoky and '? s by fertilized diploid eggs. Because ｾ＠ s derive from a haploid egg and thus have gametes of only one type in the genome, this gamete must be present in the genome of all its daughters. The second gamete received from the mother will be one of her two gametes. As a result, the mean genetic similarity (the proportion of identical gametes, hereinafter indicated by the letter r) among sisters (based on the parents) is 3/4 while between'? s and their offspring it is 112, because they carry only one of her gametes. Thus, all things being equal (primarily when there is on average an equal number of offspring raised independently or in a colony per '?), due to asymmetry in ·the arrangement of gametes in the offspring, it is genetically advantageous for the 9 to be nonreproductive in order to raise her sisters and to become a worker for her mother. At the same time this is also advantageous for the mother: in becoming the queen, she may instead of secondary offspring (with which r = 1/4), which she would have by the end of the season in a solitary existence, produce her own offspring (with which r - 112). It is precisely this 'mutual interest that was the basis of the appearance of eusociality in Hymenoptera. Hamilton's discovery was called the haplodiploidy hypothesis or the 3/4-coefficient-of-relationship hypothesis. Subsequently, asymmetry in genetic similarity between the individual and siblings of the opposite sex was also found in termites, the only group of eusocial diploid insects. It is true that such asymmetry in termites is the result of a complex system of translocations of sex chromosomes (Lacy. 1984; Luykx, 1985). Statement of the problem. The main argument against the haplodiploidy hypothesis, which has still not been resolved, involves cases of polygynous founding of colonies among bees and wasps. The polygynous founding of colonies presents the haplodiploidy hypothesis wi.th.a problem which in the interpretation of critics of the hypothesis appears as follows: If a colony is established by sibling sisters (r - 3/4), then those which function as workers should care for their own nephews and nieces, for which r - 3/8. The latter magnitude is 1/8 less than the r value between the 9 and her offspring, which should make it unfavorable for her to refrain from reproduction in favor of one of her sisters. Naturally, it is even less advantageous for her to care for the offspring of an unrelated individual. Polygyny in the founding of colonies in bees and wasps is of a short-lived nature and differs sharply from true polygyny or "multiple queens" in ants, although many researchers confuse these concepts. For the founding of a colony, young 9s, potentially reproductive, that is, with developed ovaries, and fertilized 9S, as a rule, sisters, come together. After a brief period of "working out relationships" a hierarchy of dominance is established among the united individuals: Usually only one of the sisters oviposits while the others begin to function as workers. Cofounders of a colony helping their

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sister quickly waste and die before the first brood is hatched or are chased out by the dominant sister who then creates with her own daughters a eusocial colony. Hamilton (1964b), the author of the haplodiploidy hypothesis, himself pointed out the problem associated with the polygynous founding of a colony. In an attempt to fit this phenomenon into the hypothesis, he advanced the idea of "population viscosity," according to which closely related inbreeding increases the mean genetic similarity between '" functioning as a worker and her nephews and nieces. Genetic population models constructed later showed that inbreeding did not favor development of a sterile caste inasmuch as the overall genetic similarity between all descendants increases, which does not provide her with an advantage in caring for her sister's offspring as compared to her own (Trivers and Hare, 1976). No other explanation has been offered for the polygynous founding of a nest using the haplodiploidy hypothesis. This has made it possible for some researchers (e.g., West-Eberhard, 1978; Andersson, 1984; Fletcher and Ross, 1985; Kipyatkov, 1986; and others) to reject the entire hypothesis. Approach to resolving the problem. The problem of the polygynous founding of a colony in fact has a rather simple solution if we consider the following two circumstances: 1) polygynously established colonies in all species develop into typical matrifilial colonies. 2) usually only sisters

participate in the polygynous founding of a colony. The founding of colonies jointly by several 9 s usually is observed only among eusocial species with a Social organization at a very low level. Many 9 s of such species only partially and not always successfully use the help of their offspring when independently establishing nests. This suggests the possibility of the parallel existence in primitive eusocial species of bees and wasps of two life forms: solitary (more precisely, subsocial) and eusocial. Both life forms within a single population are known, for example, in Evylaeus Iinearulus. E. problematicus. Augochlorella striata. Ceratina japonica. C. okinawana. Euglossa cordata, and a number of other species of bees. Thus, each potentially reproductive 9 of a primitive eusocial species in theory may "choose" one of three strategies: 1) the queen (including the dominant? in a polygynous colony) preserves the reproductive capability after the first brood batches, and, with the help of daughters, continues to the end of the season (or the next year in univoltine biennial species) to raise her own reproductive offspring; 2) a solitary? is able until her death to raise only a single brood, which by the end of the season (or in the following year) produce her second generation; 3) a 9 functioning as a worker in a polygynous colony participates in raising only the 1st (worker) brood of her dominant sister. Of course, the actual selection is determined by a great many circumstances associated with the level of development of eusociality in a given species and with the peculiarities of a given 9, primarily her reproductive potential and time of hatching. In assessing the advantages of one or another strategy of? s, it is necessary to relate their generic contribution to the reproductive offspring to the segment of time corresponding to the entire cycle of development of the colony. In the case of a polygynous founding of a colony, 9: s functioning as workers should thus be compared with solitary 9 s that produced a second generation. This is ignored by all authors who have discussed the problem of the polygynous founding of a family (although in assessing the genetic advantage of a queen the analogous calculation for the second generation was made). They are restricted only to the time period during which 9 s functioned as workers, and in so doing their direct contribution to raising the offspring of the sister was calculated as compared to their possible contribution to their own offspring during the same period of time. In addition, 'i's helping their egg-laying sister raise only workers. Therefore their actual contribution in this stage in such an approach in general is equal to zero (or 1/8 if the d's in the reproductive offspring of the colony are the sons of unfertilized workers of

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nieces) and not the 31& fraction of identical gametes carried by individuals raised with their help as the majority of authors believe. Genetic advantages of 95 in polygyny. '?S that function as workers release their egg-laying sister, the future queen, from much labor and substantially increases her longevity and chances of enabling a colony to produce reproductive offspring and thus increase its size. At the same time, the individual that participated in founding a colony but then functioned as a worker under her egg-laying sister gains advantages compared to the strategy of a solitary? With respect to the ? who becomes a worker, the reproductive offspring of the colony raised after the breeding of true workers consists of her nephews and nieces (offspring of the egg-laying sister who becomes the queen) with r = 3/8 and of great-nephews (offspring of unfertilized workers of the nieces) with r = 3/16. As a result, the mean genetic similarity of the sister functioning as a worker to offspring that would be produced at the end of the existence of a polygynous colony, even if all d's would be great-nephews (which corresponds to the genetic interests of the workers of nieces) amounts to (3/8 + 3/16) / 2 - 9/32, which is 12.5% higher than genetic similarity to second-generation offspring which the ? would have produced in that same period of time if it were solitary. Such advantages should be even greater for ?s which for any reasons are not strong enough reproductively to dependably produce workers and reproductive broods. Thus, the proof provided above not only refutes the main argument against the haplodiploidy hypothesis but also demonstrates that the polygynous founding of a colony in bees and wasps is supported by the kin-selection theory in the initial stages of the evolution of eusociality, although only after the appearance of the latter. The polygynous founding of a colony is not necessary for those eusocial species in which all potentially reproductive 9s have a great chance not only to raise broods of workers but also to produce reproductive offspring. The solitary founding of a colony makes it possible for? 1I most fully to realize the possibility of passing on their genes to offspring. LITERATIJRE CITED ANDERSSON, M. 1984. The evolution ofeusociality. Ann. Rev. Eeo!. Syst. 15: 165-189. FLETCHER, D. J., and K. G. ROSS. 1985. Regulation of reproduction in eusocial Hymenoptera. Ann. Rev. Entomol. 30: 319-343. HAMILTON, W. D. 1964a, b. The genetical evolution of social behavior. I. Theor. BioI. 7(1): I-52. KIPYATKOV, V. E. 1986. The problem of the origin of social insects: review and synthesis. In: Dok!. 38 Ezhegod. chtenii pamyati N. A. Kholodovskogo, 4 Apr. 1985 (Report of the 38th Annual Meeting in Memory ofN. A. KIroIOdo\'skiy,4 April 1985): 3-42. LACY, R. C. 1984. The evolution oftennite eusociality: reply to Leinaas. Amer. Nat. 123(6): 876-878. LUYKX, P. 1985. Genetic relations among castes in lower tennites. In: Watson, J. A. L. et al. (Eds.) Caste Differentiation in Social Insects. Pergamon Press 3: 17·25. RADCHENKO, V. G., and YU. A. PESENKO. 1992 (in press). Biologiya pchel (Biology of Bees). SI. Petersburg. . TRIVERS, R. L., and H. HARE. 1976. Haplodiploidy and the evolution of social insects. Science 191(4224): 249-262. ｗｅｓｔｾｂｒｈａｄＬ＠

M. J. 1978. Polygyny and the evolution of social behavior in wasps. 1. Kansas .. Entomoi. Soc. 51(4): 832-856. . 4