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Social behavior and comparative genomics: new genes or new gene regulation?

Molecular analyses of social behavior are distinguished by the use of an unusually broad array of animal models. This is advantageous for a number of reasons, including the opportunity for comparative genomic analyses that address fundamental issues in the molecular biology of social behavior. One issue relates to the kinds of changes in genome structure and function that occur to give rise to social behavior. This paper considers one aspect of this issue, whether social evolution involves new genes, new gene regulation, or both. This is accomplished by briefly reviewing findings from studies of the fish Haplochromis burtoni, the vole Microtus ochrogaster, and the honey bee Apis mellifera, with a more detailed and prospective consideration of the honey bee.

Animals↗

The origins of human ageing.

The origins of human ageing are to be found in the origins and evolution of senescence as a general feature in the life histories of higher animals. Ageing is an intriguing problem in evolutionary biology because a trait that limits the duration of life, including the fertile period, has a negative impact on Darwinian fitness. Current theory suggests that senescence occurs because the force of natural selection declines with age and because longevity is only acquired at some metabolic cost. In effect, organisms may trade late survival for enhanced reproductive investments in earlier life. The comparative study of ageing supports the general evolutionary theory and reveals that human senescence, while broadly similar to senescence in other mammalian species, has distinct features, such as menopause, that may derive from the interplay of biological and social evolution.

Aging↗

[And then, the dinosaurs disappeared].

"This paper starts by putting the present fertility decline experienced by many industrialized countries, in a global prospect of social evolution, and shows to what extent this decline is a new phenomenon. Using a so-called 'infernal' scenario, wherein Canadian fertility continues to fall, the author then emphasizes that society would have at its disposal a remarkably long delay for bending the path leading to extinction, although some forces may also lead to an acceleration of the demographic decline." (SUMMARY IN ENG AND SPA)

Americas↗

From individual control to majority rule: extending transactional models of reproductive skew in animal societies.

Transactional concession models of social evolution explain the reproductive skew within groups by assuming that a dominant individual completely controls the allocation of reproduction to other group members. The models predict when the dominant will benefit from donating parcels of reproduction to other members in return for peaceful cooperation. Using linear programming methods, we present a 'majority-rules' model in which the summed actions of all society members, each with equal power, completely determine the reproductive share of any single member. The majority-rules model predicts that, despite the diffusion of power, a 'virtual dominant' (a dominant lacking special behavioural power) will emerge and that the reproductive skew will be exactly that predicted if the virtual dominant were to control completely the group's reproductive partitioning. The virtual dominant is the individual to which group members have the maximum average genetic relatedness. This result greatly broadens the applicability of transactional models of reproductive skew to social groups of any size, such as large-colony eusocial insects, and explains why queens in such colonies can achieve reproductive domination without any behavioural enforcement. Moreover, the majority-rules model unifies transactional-skew theory with models of worker policing and even generates a new theory for the cooperation among somatic cells in a multicellular organism.

Animals↗

Restricted gene flow between two social forms in the ant Formica truncorum.

We studied genetic differentiation between two social forms (M-type: single queen, independent nest founding; P-type: multiple queens, dependent nest founding, building of colonial networks) of the ant Formica truncorum in a locality where the social types characterize two sympatric populations. The genetic results indicate restricted gene flow between the social forms. Female gene flow between the forms appears to be absent as they did not share mitochondrial haplotypes. Significant nuclear differentiation and the distribution of private alleles suggest that male gene flow between the forms is weak. However, the assignment analysis indicates some gene flow with P males mating with M females. The results have potentially important implications concerning social evolution within the forms but they need to be confirmed in other localities before they can be generalized. The colonies in the M-type population have earlier been shown to produce split sex ratios, depending on the mating frequency of the queens. The inferred gene flow from the P to the M type means that the split sex ratio is partly suboptimal, possibly because the P populations are not long-lived enough to influence the behavioural decisions in the M colonies.

Animals↗

Group founding and breeding structure in the subsocial spider stegodyphus lineatus (Eresidae)

Co-operative behaviour may evolve by enhancing the genetic similarity of group members. Increased group similarity is thought to be the basis for the 'subsocial route' of social evolution in the spider family Eresidae. Two processes may promote the similarity of individuals within populations or breeding groups, namely philopatry in stable environments and founder events in a stochastic environment. We show that both processes led to genetic differentiation within and among populations of the subsocial spider Stegodyphus lineatus. Within populations we distinguished between the genetic structure caused by random mating and philopatry in old breeding groups and that caused by newly founded groups consisting of sibs. Such sib-groups suggest that new breeding groups are established primarily by single females. The different gene coancestries among breeding groups resulted in high variances among single-locus data. The results imply that sex-specific dispersal behaviour (random male mating-dispersal or female group founding) had different impacts on the population structure. This type of population structure, where within-population philopatry and founder events may lead to differential proliferation of breeding groups, is very similar to that presumed for social spiders, and is also one that could provide the conditions for interdemic selection.

Journal Article↗

Preference for sons and sex ratio in two non-Western societies.

Moroccan Berbers and the Bolivian Aymara are two unrelated peasant groups living in adverse environments with a still rather traditional agriculture. Precarious life conditions may be responsible for the importance given to male labor and hence for the cultural preference conferred on male descent. This preference, expressed in the social valorization of sons to the detriment of daughters, is more emphasized if the socioeconomic status of the family is lower. Interpreted according to the cost/benefit approach of Fisher (1958 Genetical Theory of Natural Selection, New York: Dover) of variations in the sex ratio and to its later developments (Trivers and Willard 1973 Science 179:90-91; Trivers 1985 Social Evolution, Menlo Park: Benjamin/Cummings; Hewlett 1991 J. Anthropol. Res. 47:1-37; Smith 1993 Ethol. Sociobiol. 14:39-44), these cultural characteristics could determine that parents bias the care allocated to their progeny in favor of sons, to the detriment of daughters. This could eventually affect their respective survival and finally modify the offspring tertiary sex ratio. This study compares differences in survival as indicators of parental care according to a child's sex and across three economic strata: poor, medium, and high. The Moroccan data express no other sex differences in survival than an advantage for daughters during the preweaning period in the medium and high strata. Within the same sex and across economic strata, a greater mortality between age 10-20 years is observed for boys of the poorest stratum. The Aymara data do not show sex differences by economic stratum, except for an advantage to daughters between birth and 5 years in the medium group, and no survival differences within the same sex across economic strata. These results suggest either that despite the social valorization of male progeny no differences in parental care according to sex occur, or that their magnitude is not great enough to contrast the survival of sons and daughters.

Adolescent↗

Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis.

Understanding how a single genome can produce a variety of different phenotypes is of fundamental importance in evolutionary and developmental biology. One of the most striking examples of phenotypic plasticity is the female caste system found in eusocial insects, where variation in reproductive (queens) and non-reproductive (workers) phenotypes results in a broad spectrum of caste types, ranging from behavioural through to morphological castes. Recent advances in genomic techniques allow novel comparisons on the nature of caste phenotypes to be made at the level of the genes in organisms for which there is little genome information, facilitating new approaches in studying social evolution and behaviour. Using the paper wasp Polistes canadensis as a model system, we investigated for the first time how behavioural castes in primitively eusocial insect societies are associated with differential expression of shared genes. We found that queens and newly emerged females express gene expression patterns that are distinct from each other whilst workers generally expressed intermediate patterns, as predicted by Polistes biology. We compared caste-associated genes in P. canadensis with those expressed in adult queens and workers of more advanced eusocial societies, which represent four independent origins of eusociality. Nine genes were conserved across the four taxa, although their patterns of expression and putative functions varied. Thus, we identify several genes that are putatively of evolutionary importance in the molecular biology that underlies a number of caste systems of independent evolutionary origin.

Adaptation, Physiological↗

A community-level evaluation of the impact of prey behavioural and ecological characteristics on predator diet composition.

Although predation avoidance is the most commonly invoked explanation for vertebrate social evolution, there is little evidence that individuals in larger groups experience lower predation rates than those in small groups. We compare the morphological and behavioural traits of mammal prey species in the Taï forest, Ivory Coast, with the diet preferences of three of their non-human predators: leopards, chimpanzees and African crowned eagles. Individual predators show marked differences in their predation rates on prey species of different body sizes, but clear patterns with prey behaviour were apparent only when differences in prey habitat use were incorporated into the analyses. Leopard predation rates are highest for terrestrial species living in smaller groups, whereas eagle predation rates are negatively correlated with group size only among arboreal prey. When prey predation rates are summed over all three predators, terrestrial species incur higher predation rates than arboreal species and, within both categories, predation rates decline with increasing prey group size and decreasing density of groups in the habitat. These results reveal that it is necessary to consider anti-predator strategies in the context of a dynamic behavioural interaction between predators and prey.

Animals↗

Peacekeeping and peacemaking: the conceptual foundations of a plan to reduce violence and improve the quality of life in a midsized community in Jamaica.

Thomas Jefferson noted that social ills breed economic ills and vice versa. An endless regress can occur with violence and mayhem as a chorus: Every community in the world has its own thresholds and patterns of violence, and communities experience varied levels of deterioration of safety with a reciprocal increase in violence. The United States, having undergone 200 years of social evolution as an independent nation, has a spiraling problem with violence. Jamaica, with only recent independence from British sovereignty, is an ideal crucible for the study of evolution of violence in a very young democracy and, hopefully, to identify problems and provide some solutions. Having gained independence from British rule in 1962, Jamaica immediately demonstrated a facile experimentation with forms of government that differed dramatically from what had been previously experienced under the rather rigid, autocratic British administration. In its 33 years of independence, this country has gone through some extraordinary shifts. An initial courtship with Communist theory led to a destructive liaison with Fidel Castro's version of Marxism. During this brief interlude, the intellectual ideals of equality and peace came into direct contrast with facts of a failing Communist regime. During this period, there was a steady exodus of wealthy Jamaican families for whom heavy taxation threatened financial ruin. The prime minister, the Honorable Michael Manley, a highly sophisticated left-wing intellectual liberal, soon realized the political cost of the alliance with his Caribbean neighbor, Fidel Castro, who was then and is now dedicated to old-fashioned, state-controlled Communism. He attempted to return to a free-market democracy with financial foundations that were, by then, very shaky. To succeed in a project to reduce violence and improve the quality of life, the entire community needs to be involved. From our work in countries where community projects were primarily financed by federal and state agencies, we were aware that the participation of private citizens in projects was essential for success. Commitment has an added intensity when personal time and funding is involved. Prime Minister Manley enthusiastically embraced and inspired this project, believing that it embodied the fundamental principles of democratic involvement to which he was committed. When the authors personally presented their plan to him, he accepted it immediately and with an obvious personal sense of urgency. Illness led him to resign the post of Prime Minister in 1993, but his successor, Mr. P.J. Patterson, has continued in the same committed, democratic mode.

Developing Countries↗

An experimental study of behavioural group size effects in tammar wallabies, Macropus eugenii.

As animals aggregate with others, the time they allot to social and nonsocial activities changes. Antipredator models of vigilance and foraging group size effects both predict a nonlinear relationship between group size and the time allocated to behaviour. Group size effects were experimentally studied in captive adult female tammar wallabies, a small macropodid marsupial, by increasing group size from 1 to 10. Tammars foraged more, looked less, groomed more, engaged in more aggressive interactions and moved about less as group size increased. Nonlinear regression models explained more variation in the time allocated to foraging, looking, locomotion and affiliative behaviour than linear models. Variation in self-grooming and aggression was better explained by linear models. Wallabies lay down significantly more, and walked significantly less, as group size increased: these relationships were significantly nonlinear. Thus, changes in perceived predation risk, which are characterized by nonlinear relationships, explain tammar wallaby group size effects for most activities. These results support the assertion that predation has played an important role in macropodid social evolution. Moreover, the findings suggest that conservation biologists should pay particular attention to group size when translocating or reintroducing endangered macropodids. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

Treatment of schizophrenic disorder, paranoid type, with intramuscular recombinant alpha-2b interferon.

Twenty patients meeting DSM-III criteria for Schizophrenic Disorder, Paranoid Type were studied. After a 30 day drug-free period the patients were randomized in two groups. During a year, patients in Group 1 received intramuscular injections of a placebo while Group 2 received recombinant IFN alpha-2b. Both groups took anti-psychotic medication (APM) as needed on an individual basis, depending on their psychiatric symptomatology. Double blind evaluations, were performed at the beginning and at the end of the trial, using the Brief Psychiatric Rating Scale (BPRS) and the Reyes Scale for Social Evolution (RSSE). Information about relapses was gathered such as months without relapse, number and duration of the relapses and maximum dosages of APM given for relapse control. The statistical analysis of the results was performed with a matched pairs sign or Student's t tests for comparisons of each group before and after treatment. Groups were compared between them using the Fisher's exact test for frequencies and Student's t test for continuous variables. In Group 1: only one patient improved on the BPRS score; two had improved ratings on the RSSE; 2 patients got worse; and there were no changes in the rest of the group; three patients had no relapses and one increased in relapse frequency. These changes were not significant. The rate of relapses per year and their duration were not significantly modified in Group 1. The maximum dose of APM required for their relapse control was larger than before treatment although not significantly. All these patients required continuous APM. In Group 2 (IFN treated): 6 patients had improved BPRS scores (N = 6, K = 6, p < 0.01) and 5 improved their RSSE scores (n = 5, K = 5, p < 0.05). In 5 patients there were no relapses on their frequency decreased. There was significant reduction in the duration of the relapses (37.8 +/- 14.6 to 20.7 +/- 12.5 days; t = 4.83; d.f. = 9; p = 0.0009) after treatment. Only 3 patients in Group 2 needed continuous APM after a relapse and the maximum dose required for control was significantly less (1281 +/- 527 to 687 +/- 552 chlorpromazine-equivalent mg. per day; t = 5.56, p < 0.001). Comparisons between groups showed advantage for the IFN treated group in the BPRS change, proportion of patients needing continuous APM and integral evaluation. These results indicate that alpha IFN may be useful in the treatment of Schizophrenic Disorder, Paranoid Type.

Adult↗

The phylogeny of the social Anelosimus spiders (Araneae: Theridiidae) inferred from six molecular loci and morphology.

We use fragments of three nuclear genes (Histone 3, 18SrDNA, and 28SrDNA) and three mitochondrial genes (16SrDNA, ND1, and COI) totalling approximately 4.5kb, in addition to morphological data, to estimate the phylogenetic relationships among Anelosimus spiders, well known for their sociality. The analysis includes 67 individuals representing 23 of the 53 currently recognized Anelosimus species and all species groups previously recognized by morphological evidence. We analyse the data using Bayesian, maximum likelihood, and parsimony methods, considering the genes individually as well as combined (mitochondrial, nuclear, and both combined) in addition to a 'total evidence' analysis including morphology. Most of the data partitions are congruent in agreeing on several fundamental aspects of the phylogeny, and the combined molecular data yield a tree broadly similar to an existing morphological hypothesis. We argue that such congruence among data partitions is an important indicator of support that may go undetected by standard robustness estimators. Our results strongly support Anelosimus monophyly, and the monophyly of the recently revised American 'eximius lineage', although slightly altered by excluding A. pacificus. There was consistent support for the scattering of American Anelosimus species in three clades suggesting intercontinental dispersal. Several recently described species are reconstructed as monophyletic, supporting taxonomic decisions based on morphology and behaviour in this taxonomically difficult group. Corroborating previous results from morphology, the molecular data suggest that social species are scattered across the genus and thus that sociality has evolved multiple times, a significant finding for exploring the causes and consequences of social evolution in this group of organisms.

Animals↗

[Communication between radiologist and cancer patients].

Along with advances in medicine and social evolution, we are seeing an increase in the number of patients afflicted with cancer, and a change in the doctor-patient relationship. Patients' rights are now registered in the Hospitalised Patient's Charter, the Huriet Act and the Act of March 4, 2002. The evolution in cancer diseases is monitored by a range of imaging examinations, putting the radiologist in the front line. Lesions are typically first detected by the radiologist. This task is complicated by the fact that radiologists usually have no formal training with regards to the disclosure of cancer diagnoses to patients. There is a great risk of inappropriate responses which can have a profoundly damaging effect on the patient's state of mind. Even if we have the best of ideals and intentions, there is a great need for us to examine and improve our modes of interaction, in dealing with the patient's need for information. The radiologist possesses technical know-how, but technique alone is not enough - the right amount of information, based on clinical competence, is required; but so is empathy towards the patient, and respect for his or her wishes and rights.

Communication↗

Dental development of the Taung skull from computerized tomography.

Just over 60 years ago, Dart's description and analysis of the Taung child's skull triggered an intellectual revolution about human origins. Recently, several authors have suggested that one of the most significant hominid-like traits of australopithecines, delayed maturation, may not after all be valid. This is a radical departure from Mann's classic study of australopithecine maturation and palaeodemography based on dental eruption patterns. The resolution of this debate has important implications for the history of the biological and social evolution of the human species. In view of the controversies generated by recent studies, and particularly because the Taung skull is the type specimen of Australopithecus africanus, we have investigated the relevant anatomy of the Taung 'child' using computerized tomography. We conclude that the Taung 'child' shows some important dental maturational affinities with great apes, although as Dart noted, other hominid-like features are clearly present.

Age Determination by Teeth↗

Altruism and social cheating in the social amoeba Dictyostelium discoideum.

The social amoeba, Dictyostelium discoideum, is widely used as a simple model organism for multicellular development, but its multicellular fruiting stage is really a society. Most of the time, D. discoideum lives as haploid, free-living, amoeboid cells that divide asexually. When starved, 10(4)-10(5) of these cells aggregate into a slug. The anterior 20% of the slug altruistically differentiates into a non-viable stalk, supporting the remaining cells, most of which become viable spores. If aggregating cells come from multiple clones, there should be selection for clones to exploit other clones by contributing less than their proportional share to the sterile stalk. Here we use microsatellite markers to show that different clones collected from a field population readily mix to form chimaeras. Half of the chimaeric mixtures show a clear cheater and victim. Thus, unlike the clonal and highly cooperative development of most multicellular organisms, the development of D. discoideum is partly competitive, with conflicts of interests among cells. These conflicts complicate the use of D. discoideum as a model for some aspects of development, but they make it highly attractive as a model system for social evolution.

Animals↗

Mate fidelity and intra-lineage polygyny in greater horseshoe bats.

Mating strategies that lead to increased kinship within socially cooperative groups may offer inclusive fitness benefits to individuals, but can also result in higher levels of inbreeding. Here we show in a sexually segregated bat species that females avoid this conflict through two mating behaviours. First, most females revisit and breed with specific, individual males across years, so that their single offspring born in different years are full siblings. Second, relatives in the maternal line, including mothers and daughters, share breeding partners (intra-lineage polygyny) more often than expected by chance. Although these behaviours increased levels of co-ancestry among colony members, there was no concomitant rise in inbreeding. We suggest that when females engage in mate fidelity and intra-lineage polygyny, kin ties among female roost mates will be strengthened, thereby potentially contributing to social group cohesiveness. Our findings reveal the hidden complexity that can underlie polygynous breeding, and highlight a new potential route by which female mate choice could influence social evolution.

Animals↗

Kin discrimination and sex ratios in a parasitoid wasp.

Sex ratio theory provides a clear and simple way to test if nonsocial haplodiploid wasps can discriminate between kin and nonkin. Specifically, if females can discriminate siblings from nonrelatives, then they are expected to produce a higher proportion of daughters if they mate with a sibling. This prediction arises because in haplodiploids, inbreeding (sib-mating) causes a mother to be relatively more related to her daughters than her sons. Here we formally model this prediction for when multiple females lay eggs in a patch, and test it with the parasitoid wasp Nasonia vitripennis. Our results show that females do not adjust their sex ratio behaviour dependent upon whether they mate with a sibling or nonrelative, in response to either direct genetic or a range of indirect environmental cues. This suggests that females of N. vitripennis cannot discriminate between kin and nonkin. The implications of our results for the understanding of sex ratio and social evolution are discussed.

Animals↗