Evolution of Sociality in Insects

Kin selection has been used to explain evolution of man altruistic traits found in those social insect castes which have reduced reproductivity. Kin selection is most probable among organisms living in family groups. It is commonly assumed, therefore, that (1) the most primitive social insects, like the more specialized ones, live in mother-daughter (eusocial) colonies, (2) colonies of individuals of the same generation and showing castes (semisocial colonies) are abnormal or originate only in inbreeding populations, and (3) transfer of individuals among colonies must be selected against, except in inbreeding populations. Numerous Hymenoptera are cited, however, in which semisociality or transfer occurs in populations lacking evidence for inbreeding; and we believe that, in explaining the origin of social behavior in insects, Hamilton and others have placed too much emphasis on the evolution of altrustic behavior through kin selection. There is considerable evidence that social behavior in insects is in part mutualistic. Social colonies without altruism are therefore considered a probability. Factors in addition to kin selection that could promote social behavior are examined, and it is our view that a whole series of factors acting jointly or alternately is responsible for the numerous origins of sociality in Hymenoptera, compared to only one in all the other insects. An important factor favoring mutual tolerance and initial colony formation is the need for defense. Hymenopteran workers are commonly reproductive and produce most of the male offspring in some primitively as well as highly eusocial forms (90% of the males in a species of Bombus; 95% in a Trigona). Individual selection for sources of males should favor production of workers. Presence of ovaries and of reproductive behavior in many workers suggests that reproductivity is retained by selection. In the most primitive social Hymenoptera, queens and workers together vary little more than do females of related solitary species. If both the more and the less reproductive individuals profit from the association, selection will favor colonies. The more reproductive individuals tend to start nests first and to be joined by delayed reproducers that are often workerlike. Thus semisocial colonies of very similar castes can arise without kin selection or altruism; they are preadaptations to eusocial evolution and provide immediate improved protection for the nest. Joiners will be more certain to arrive, although much delayed, if they are progeny of the colony or lone founder. This leads to eusocial colonies among which kin selection can operate. Eusocial colonies need not, but probably often do, arise from semisocial ones, as is suggested (1) by the frequency of nest aggregations providing numerous acceptors and joiners of the same generation, and (2) by the ontogeny of many bee and wasp colonies. There is no certainty that kin selection and altruism will arise with eusociality, but they probably usually do; they may also arise in semisocial groups if the individuals are closely enough related as a result of inbreeding. Eusocial colonies without altruism are possible if male production by workers is important enough. Long life, and ability to produce female offspring under suboptimum conditions so that they will become joiners, or ability to dominate other females with the same result, and other queenlike features should be favored by individual selection operating on queens, regardless of the origin of the society. Male haploidy is related to many aspects of hymenopteran evolution. Among these is the origin and evolution of social behavior because of (1) partial immunity to inbreeding resulting from the loss of lethals, allowing long-term aggregations and colonies and effective kin selection to arise, (2) sperm storage by females, absence of a king in social groups, and the control of the sex of offspring, permitting the extraordinary sex ratios found in highly social Hymenoptera, (3) the importance of male-production by workers in primitively social groups and some highly social ones, and (4) the closer relation of sisters to one another than to their daughters, an arrangement that ecourages effective kin selection. Male-producing workers increase genetic recombinations and permit retention of the advantages of a haplodiploid genetic system while permitting also some advantages of the ordinary fully diploid system. The loss of variation due to male haploidy may be partly responsible for the evolution of outbreeding devices, including acceptance of joiners. The joiners are ordinarily workers which, as male-producers, will increase variation, but may in error be members of related species, a situation resulting in the potential for evolution of social parasites. Immunity to inbreeding permits aggregations, in which pressure from natural enemies is likely to promote development of colonies. None of the special features described above applies to termites, in which the need to transfer intestinal symbionts must be the prime factor that encouraged social evolution. In the initial stages (as in the roach, Cryptocercus) there is no altruism, a feature that, however, characterizes subsequent stages in termite evolution.