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4. ALTRUISM IN SOCIAL INSECTS

SEX-RATIO CONFLICTS, KIN SELECTION, AND THE EVOLUTION OF ALTRUISM

W.J. Alonso and C. Schuck-Paim (University of Oxford, UK) discuss altruism, the authors making the following points:

1) Ever since its formulation in 1963 by William Hamilton (1-4), kin-selection theory has flourished in the prospect of explaining a wide range of sophisticated patterns of animal behavior, being often regarded as one of the most (or even the most) important evolutionary insights of the recently finished century (5). Among its greatest contributions is the formulation of an evolutionarily acceptable framework for the appearance and maintenance of the so-called biological "altruism," through which individuals behave by lowering their own potential for reproduction or survival in favor of the reproduction of other individuals of the same species.

2) A central problem addressed under the theory's scope is the evolution of sterile castes of workers in colonies of eusocial organisms, such as ants, termites, and some bees and wasps. According to the theory, the evolution of worker castes was possible only because of the success of genes (hereafter "altruistic genes") codifying for behaviors whereby their carriers sacrifice their own reproductive output by helping the reproduction of individuals who most likely have these genes. The conditions for these genes to spread are given in the well-known Hamilton rule: rb - c > 0, where r is the coefficient of kinship between the altruist and the receiver of the altruism, b is the benefit in terms of extra offspring for the receiver of the altruistic act and c is the cost for the altruist's offspring production.

3) An alternative explanation for the emergence and evolution of sterile castes in eusocial organisms states that the characteristic (or "gene", in the present operational language) under selection is one that imposes the nonreproductive role to part of the brood, by handicapping its full reproductive development through a shortage of resources and/or agonistic interactions ["parental-manipulation theory"). As a result, the eusocial system would not emerge because of the expression of altruistic genes, but instead because of the evolutionary advantage provided by a developmental process comprising several individuals, functioning at a new level of selection (the eusocial colony). Nowadays some kin-selection defenders support the idea that the two theories are complementary, and that in fact the role of manipulation is to create better conditions for the fixation of the altruistic gene.

4) In summary: Kin-selection theory has thrived in the explanation of a wide variety of biological phenomena, chiefly the evolution of biological altruism as that found in sterile castes of eusocial insects. Much of the way in which it has been tested is based on the existence of conflicts over sex-ratio production within eusocial colonies. However, despite neatly showing eusocial colonies as arenas where selection at the gene level triggers the appearance of sophisticated disputes, these studies have only demonstrated the existence of genes that act by biasing sex ratios to promote their own spread. The authors argue that such genes depend on the social organization of the colonies where they are expressed, but that they are not, in any way, the precursors of these societies -- the major implication being that unequivocal evidence that eusociality evolved through the action of kin-selected altruistic genes is still lacking. Additionally, the authors highlight the neglect of alternative theories on the explanation of both biological altruism and sex-ratio conflicts, and propose that enthusiasm with the latter has, in some cases, led to its inappropriate use as a basis for the explanation of other biological characteristics of eusocial organisms, when accounts based on phylogenetic or physiological constraints are also available.

References (abridged):

1. Hamilton, W. D. (1963) Am. Nat. 97, 354-356

2. Hamilton, W. D. (1964) J. Theor. Biol. 7, 1-16

3. Hamilton, W. D. (1964) J. Theor. Biol. 7, 17-32

4. Hamilton, W. D. (1972) Annu. Rev. Ecol. Syst. 156, 477-488

5. Queller, D. C. (2001) Behav. Ecol. 12, 261-264

Proc. Nat. Acad. Sci. 2002 99:6843

Related Background:

GENETIC CONFLICT AND CONDITIONAL ALTRUISM IN SOCIAL APHID COLONIES

P. Abbot et al (University of Arizona, US) discuss altruism in social aphids, the authors making the following points:

1) There are various scenarios for the evolution of soldiers in aphids (1), but two elements thought to be decisive are the high relatedness afforded by the isolation of clonally produced colonies within galls (2,3) and the need for defending long-lived galls from attack by natural enemies (4,5). In purely clonal groups, the social traits exhibited by soldiers, like risky defense against enemies and reproductive altruism, reflect clone-level allocations to defense over reproduction, without conflict between group members (1). But if clones mix, the advantages of defense are weakened because the benefits of sacrificial behaviors accrue in part to unrelated aphids. Thus, the genetic structure of colonies is crucial to understanding the selective advantages of social traits in aphids.

2) Pemphigus obesinymphae is the only North American aphid known to have soldiers (1,4). Its complex life cycle involves phases of sexual and asexual reproduction on alternative host plants. In the spring, a "foundress" initiates a globular gall at the base of a leaf of a cottonwood (Populus spp.). Permanently entombed in the hollow cavity of the gall, she asexually produces a caste of up to 300 first-instar soldiers, which can exit and reenter through a small ostiole. Aphid soldiers effectively deter attack by much larger enemies, often sacrificing themselves in the process. Colonies of P. obesinymphae, for example, suffer less than half the predation experienced by colonies of nondefending Pemphigus species on the same trees.

3) Near the end of the growing season, all colonies make a conspicuous transition from defense to reproduction as nymphs mature beyond the first-instar soldier stage. The maturing nymphs, which as adults will fly from the gall to reproduce on another host plant, no longer participate in group defense (4). Before they mature, the development of P. obesinymphae soldiers into more advanced instars is inhibited in the presence of the foundress. Thus, soldiers are altruistic, because delayed development and aggressive behaviors toward other arthropods result in an extended period of risk and lowered likelihood of successful reproduction (4).

4) In summary: Although kin selection is central to the modern study of social evolution, recent studies of social species have revealed that no simple relationship exists between levels of kinship and sociality. The soldier-producing aphids are unique among highly social animals because, barring movement by aphids between colonies, they occur in clonal groups of genetically identical individuals. Potentially, clonality simplifies efforts to understand social evolution in aphids by obviating issues of intragroup conflict. However, the authors report high levels of clonal mixing and conflict in an aphid society. The gall-dwelling colonies of a social aphid species (Pemphigus obesinymphae) are not pure clones, but are invaded by large numbers of aphids from other clones. Intruders behave and develop selfishly once they have invaded a colony of non-kin. They refrain from risky defensive behaviors and accelerate their own development into reproductive rather than defensive stages. This conditionality in the social life of P. obesinymphae reveals complex dynamics and a degree of behavioral plasticity not previously known in aphid societies.

References (abridged):

1. Stern, D. L. & Foster, W. A. (1996) Biol. Rev. 71, 27-79

2. Aoki, S. (1977) Kontyu 45, 333-334

3. Hamilton, W. D. (1997) in The Biology of Social Insects, eds. Breed, M. D., Michener, C. D. & Evans, H. E. (Westview, Boulder, CO), pp. 81-102

4. Moran, N. A. (1993) Insect Soc. 40, 391-402

5. Foster, W. A. & Northcott, P. A. (1994) in Plant Galls: Organisms, Interactions, Populations, ed. Williams, M. A. J. (Clarendon, Oxford), pp. 161-182

Proc. Nat. Acad. Sci. 2001 98:12068

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