Eusocial Colonies Research Articles

The Socioecology of Body Size Variation in the Primitively Eusocial Sweat Bee, Halictus ligatus (Hymenoptera: Halictidae)

Patterns of demographic and social variation exhibited by the sweat bee Halictus ligatus, reveal that the expression of eusocial colony organization is associated with local environmental conditions, harsher conditions promoting more classical eusociality and gentler conditions promoting diminished eusociality. We examined a variety of factors affecting body size variation of H. ligatus at a nesting aggregation near Victoria in southern Ontario. Canada during the summers of 1984, 1990, and 1991. Body size variation was associated with gender and reproductive caste as expected. and there were significant colony effects on size as well. An unexpected result was the dramatic effect of local environmental conditions on body size. Changes in weather patterns from year to year resulted in significant body size variation among all classes of adult sweat bees, including queens, workers, gynes, and males. In 1990 cool, rainy weather led to the production of brood with relatively small body sizes, while in 1984 and 1991, relatively dry, warm weather had the opposite effect. Weather probably influenced brood body size by affecting the ability of adult female bees to gather provisions for the larvae, and so indirectly affecting food availability to brood. Since queens are produced a year before their own workers, environmental factors affecting their relative body sizes are uncorrelated. Nevertheless, the degree of eusocial colony organization is strongly affected by variation in the relative sizes of queens and workers, and this illustrates the extent to which stochastic environmental variation structures opportunities for behavioural interactions in primitively eusocial bees. The pattern of inverse variation between temperature and body size in this bee contradicts the general pattern of increased body size at higher temperatures generally seen in insects and other ectotherms, and indicates that social insects could be an exception to this rule.

Primer effect of queen pheromone on juvenile hormone biosynthesis in adult worker honey bees

Juvenile hormone synthesis in adult worker honey bees was measured by an in vitro corpora allata bioassay. Adult queenless workers exhibit higher rates of juvenile hormone biosynthesis than queenright workers. Hormone synthesis is not correlated with the volume of the glands. Extract of queen mandibular glands, applied to a dummy, reduces juvenile hormone biosynthesis in caged queenless workers to the level of queenright workers. The same result was obtained with synthetic (E)-9-oxo-2-decenoic acid, the principal component of the queen mandibular gland secretion. This pheromonal primer effect may function as a key regulating element in maintaining eusocial colony homeostasis. The presence of brood does not affect the hormone production of the corpora allata.

On foraging, recruitment systems and optimum number of scouts in eusocial colonies

A numerical model of an eusocial colony foraging for food showed that, for each set of values of resource density, resource size and recruitment system employed, a given optimal proportion of scouts in the colony maximize the amount of resources retrieved by a colony during a fixed period. The model predicts that ants using mass recruitment systems should have larger colonies with small foragers, and should forage on large food sources. Retrieval of small food sources by small colonies is best achieved with large workers using individual foraging strategies. For mass foragers, several food sources are best retrieved using democratic decision-making systems in recruitment, whereas for very large food sources at very low mean food patch density, autocratic decision-making systems are optimal. Some of the experimental evidence available is discussed in the light of these findings, as they confirm the prediction that large colonies with small workers have mass recruitment systems, whereas workers of small colonies with large workers are generally lone foragers.

Adaptive colony sex ratios in primitively eusocial bees

Colony-level predictions about sex-ratio optimization in eusocial Hymenoptera are different from the ones that apply to the population level. A recent empirical study on the sweat bee Halictus rubicundus has revealed a distinct pattern in the colony sex ratio of the summer brood: eusocial colonies produced more female-biased sex ratios and non-eusocial colonies produce more male-biased sex ratios. These data are consistent with theoretical hypotheses as put forward by Trivers and Hare and several later authors. When interpreted in the light of these theoretical contentions, the sex-ratio variation in Halictus rubicundus appears to be adaptive for workers, replacement queens and — under reasonable additional assumptions — also for foundresses.

Defense of Food Supply by Eusocial Colonies

Overdispersion of colonies exists in many eusocial insects. Overdispersion can be generated by direct attack on colonies or founders, by defense of space, by defense of food resources being harvested, or by exploitative competition. When direct competitive interactions lead to colony overdispersion, territoriality is said to occur. Whereas solitary territory holders typically defend space, most eusocial colonies defend resource patches rather than space per se. Also unlike solitary territory holders, colonies with forager communication can simultaneously defend several spatially separated food patches. A model explores optimal numbers of scouts (discoverers of patches) and recruits (followers) needed to maximize net rate of energy intake by the colony. Territorial costs are added to the model by requiring a higher investment of foragers per unit resource collected. According to the model, optimal colony size and percentage scouts are more sensitive to changes in patch size than in patch density. If patch defense is required for resource control, a decline occurs in optimal percentage of scouts; the decline is greatest for small colonies. Colonies that must defend patches in order to harvest from them suffer a loss in net energy intake; the loss is greatest for small colonies. It is predicted that among eusocial insects, those with territorial defense of resources should preferentially visit large patches and have comparatively large colony sizes and relatively few scouts. Ways of testing these predictions are discussed.

First Steps into Eusociality: The Sweat Bee Dialictus lineatulus

The primitively eusocial halictid bee Dialictus lineatulus has two generations per year in New York. Spring nests are initiated by one to six female bees; in multifoundress nests all bees are potentially reproductive but the largest individual doesn't forage. Summer nests contain an average of seven female bees which occur in reproductive castes, with workers almost the same size as queens. Some summer nests briefly form eusocial colonies where the foundress queen lives with her worker daughters. Foundress bees soon die in the summer, and most nests are then semisocial and contain only summer generation bees. The replacement queens are the dominant and older sisters of the workers. I hypothesize that reproductive castes first evolved in such sister associations due to environmental factors that prohibit subordinate bees from leaving and successfully starting their own nests.

The biology of a subtropical population of Halictus ligatus Say (Hymenoptera: Halictidae)

A large population of Halictus ligatus was studied in the subtropical climate of Knights Key, Monroe County, Florida. The dissection of 858 female bees caught on flowers and 420 bees from completely excavated nests gives the following picture of phenology, colony development and social organisation. In the Florida keys, H. ligatus is continuously brooded and multivoltine. However, towards the coldest time of year young gynes may rest in their natal nests rather than found a new colony. This may result in a partial synchronisation of nest initiation when warm weather returns after a particularly cold spell. Most nests are started by a single foundress that usually survives until near the end of the production of reproductives. The first brood is very variable in size and males average 11% of the bees produced at this stage. This figure increases to 56% when the first brood workers begin provisioning. Queens are produced some time after the rise in male production and colony longevity is extended by the presence of some worker brood during this phase. Queens average 16% larger than their workers but appear to exert little inhibition of worker reproductivity: 57% of worker bees mate and 68% show ovarian development. This population is unique amongst social halictines in being continuously brooded, multivoltine and in having such weak physiological caste differentiation. It seems to represent an intermediate stage between the primitively eusocial colonies of H. ligatus found in temperate regions and the communal-like ones of the tropics.

Multiple mating and the evolution of social behavior in the hymenoptera

The data on the frequency of mating by queens of eusocial Hymenoptera are reviewed. It is pointed out that the issue of sperm clumping is probably irrelevant to the evolution of eusociality. The hypothesis is presented that multiple mating is an adaptation for maintaining large colonies. In ants there is a significant relation between the size of the colony and the frequency of mating. The effect of multiple mating on the spread of a gene for worker behavior is explored. If a female mates twice, the effective number of matings is less than two except in the case of identical sperm contribution by the males. Sperm bias is defined as the contribution of unequal amounts of sperm by the males that mate with a queen. Sperm bias can be produced as a sampling phenomenon, by inter-male competition for females and by sperm competition. The relation between the ergonomic efficiency of the workers at the production of reproductives and the number of matings that is consistent with the evolution of eusociality is derived. If workers are only about 10% more efficient at producing reproductives within a eusocial colony than they are solitarily, then two matings by the queen will still produce a selective advantage to eusocial behavior.

Haploidploidy and the evolution of the social insect.

Halminton (1) was apparently the first to appreciate that the synthesis of Mendelian genetics with Darwin's theory of natural selection had profound implications for social theory. In particular, insofar as almost all social behavior is either selfish or altruistic (or has such effects), genetical reasoning suggests that an individual's social behavior should be adjusted to his or her degree of relatedness, r, to all individuals affected by the behavior. We call this theory kinship theory. The social insects provide a critical test of Hamilton's kinship theory. When such theory is combined with the sex ratio theory of Fisher (9), a body of consistent predictions emerges regarding the haplodiploid Hymenoptera. The evolution of female workers helping their mother reproduce is more likely in the Hymenoptera than in diploid groups, provided that such workers lay some of the male-producing eggs or bias the ratio of investment toward reproductive females. Once eusocial colonies appear, certain biases by sex in these colonies are expected to evolve. In general, but especially in eusocial ants, the ratio of investment should be biased in favor of females, and in it is expected to equilibrate at 1 : 3 (male to female). We present evidence from 20 species that the ratio of investment in monogynous ants is, indeed, about 1 : 3, and we subject this discovery to a series of tests. As expected, the slave-making ants produce a ratio of investment of 1 : 1, polygynoys ants produce many more males than expected on the basis of relative dry weight alone, solitary bees and wasps produce a ratio of investment near 1 : 1 (and no greater than 1 : 2), and the social bumblebees produce ratios of investment between 1 : 1 and 1 : 3. In addition, sex ratios in monogynous ants and in trapnested wasps are, as predicted by Fisher, inversely related to the relative cost in these species of producing a male instead of a female. Taken together, these data provide quantitative evidence in support of kinship theory, sex ratio theory, the assumption that the offspring is capable of acting counter to its parents' best interests, and the supposition that haplodiploidy has played a unique role in the evolution of the social insects. Finally, we outline a theory for the evolution of worker-queen conflict, a theory which explains the queen's advantage in competition over male-producing workers and the workers' advantage regarding the ratio of investment. The theory uses the asymmetries of haplodiploidy to explain how the evolved outcome of parent-offspring conflict in the social Hymenoptera is expected to be a function of certain social and life history parameters.

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.