Eusociality in History

For more than 100,000 years, H. sapiens lived as foragers, in small family groups with low reproductive variance. A minority of men were able to father children by two or three women; and a majority of men and women were able to breed. But after the origin of farming around 10,000 years ago, reproductive variance increased. In civilizations which began in Mesopotamia, Egypt, India, and China, and then moved on to Greece and Rome, kings collected thousands of women, whose children were supported and guarded by thousands of eunuchs. Just a few hundred years ago, that trend reversed. Obligate sterility ended, and reproductive variance declined. For H. sapiens, as for other organisms, eusociality seems to be an effect of ecological constraints. Civilizations rose up in lake and river valleys, hemmed in by mountains and deserts. Egalitarianism became an option after empty habitats opened up.     

A food web/landscape interaction model for microtine rodent density cycles

I present here a conceptual model that combines several factors known individually to be important in microtine population dynamics, but are insufficient separately as causal agents. Specifically, I bring together insights from trophic web theory, particularly the role of generalist and specialist predators, with landscape theory, particularly the influence of habitat patchiness on demographic processes. The resulting trophic/ROMPA interaction model (TRIM) is sufficiently complex and realistic to be used as a substrate for building even more complex and/or locally specific models. Yet, it remains simple enough to be general and widely applicable. The model suggests that predators are an important but not sufficient factor in causing multi-annual cycles greater than two years in length. In a patchy system, generalist predators have a slightly more severe impact than do specialists, and spillover predation plays a significant role. The ratio of optimal to marginal patch areas (ROMPA) influences the tendency for multi-annual cycles to occur such that medium ratios generate the strongest tendency toward cycling. However, cycles can occur with high ROMPA and specialist predators. Communities with more than three trophic levels and greater species diversity will be less likely to show cycles. Finally, it should be noted that the model combines factors intrinsic to microtines, extrinsic food-web interactions, and contextual landscape processes into an integrated framework. A plethora of null hypotheses are thereby generated against which population data can be compared.     

Relatedness,Conflict, and the Evolution of Eusociality

The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene. Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness. Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false. Contrary to their claims, genetic relatedness is important and causal, workers are agents that can evolve to be in conflict with the queen, and eusociality is not so difficult to evolve. The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values. For example, all of their models implicitly assumed high relatedness, but modifying the model to allow lower relatedness shows that relatedness is essential and causal in the evolution of eusociality. Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection. This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.     

The myology of the manus of microtine rodents

A study of the muscles of the manus of 13 genera and subgenera of microtine rodents revealed considerable variation which could be organized into 23 primitive-derived evolutionary hypotheses (transmutation series). The results, when compared with those for other mammals, produced functional/ecological hypotheses which were tested by comparing their predictions with the literature. The microtine manus is morphologically distinguished by nine characters and is adapted for a terrestrial/semi-fossorial niche. In particular, Dicrostonyx and Lemmus (distinguished by eight characters) possess the most highly fossorial manus, while the manus of Arborimus (distinguished by eight characters) contains a combination of primitive characters and derived characters which give the Tree vole the most highly developed 'clasping' ability among the microtines studied. The study has revealed characters which have potential systematic value but it is probable that parallelism has occurred in the microtine manus. When the manual characters are combined with characters from other functional complexes, their systematic value can be more clearly determined.     

Comparative solubilities and electrophoresis of microtine hemoglobins.

1. The electrophoretic mobilities of the hemoglobins of 7 taxa of microtines were compared. Microtus oeconomus, M. pennsylvanicus pullatus and M. xanthognatus showed identical 2-band patterns on electrophoresis of their hemoglobins while M. pennsylvanicus tananaensis showed only a single hemoglobin corresponding to the major band of the others. Dicrostonyx rubricatus and D. stevensoni exhibited identical patterns different from the Microtus species. Lemmus sibiricus had a slow hemoglobin component with mobility slightly different from the slow ones of the Microtus species while the fast component appeared the same. 2. Electrophoresis of individual globin chains from hemolysates, purified hemoglobins, and isolated chains indicated a large degree of similarity between the species studied, although there were significant differences in hemoglobin patterns. 3. The minor hemoglobin band in Microtus seems to be the result of a second alpha chain locus as determined from the hemoglobins from hybrids of two subspecies. 4. Salting-out studies indicated differences between hemoglobins that were not detectable by electrophoresis of either whole hemoglobins or isolated chains. 5. M. xanthognathus hemolysate was considerably less soluble than those of M. oeconomus and M. pennsylvanicus pullatus which had essentially the same solubility. 6. The major hemoglobin components of M. pennsylvanicus pullatus and M. xanthognathus were considerably less soluble than either the corresponding unfractionated hemolysates or purified minor components.     

Gyr Falcons, ptarmigan and microtine rodents in northern Sweden

A Gyr Falcon Falco rusticolus population in Northern Sweden (66°N, 17°E) was monitored from 1996 to 2002 in relation to its predator–prey interactions with its main and alternative prey species. Ptarmigan species Lagopus spp., and especially Rock Ptarmigan L. mutus , were the Gyr Falcons' most important prey and constituted more than 90% of the prey biomass. A 21-fold difference in ptarmigan abundance was found across Falcon breeding territories. However, this great variation in prey availability corresponded to only about a 10% shift in Gyr Falcon diet across territories, suggesting that the Falcons were reluctant or unable to compensate for declining ptarmigan availability by using alternative prey categories. Gyr Falcons did not respond functionally to microtine rodent abundance. Their diets were unaffected by a peak in the microtine rodent population cycle when Norwegian Lemmings Lemmus lemmus occurred in high numbers in the study area. Gyr Falcons responded numerically to their prey in two ways. First, there was a reproductive response with a significant relationship between the number of chicks fledged and the number of ptarmigan in the breeding territories. Secondly, although the Gyr Falcons did not utilize microtines as prey, there was a relationship between the microtine rodent abundance and the number of pairs that attempted to breed each year. This could be a result of an indirect community interaction, assuming that other predators switched from ptarmigan to microtines as prey, which could have had a positive effect on the breeding performance of the Gyr Falcons. The Gyr Falcons acted as true specialist predators, and their narrow food niche probably reflected a general lack of suitable alternative prey in the study area.     

Demography of a mediterranean microtine: the Mediterranean pine vole,Microtus duodecimcostatus

Microtus duodecimcostatus in a mediterranean vole which is not known to display spectacular increases in population numbers as in some microtine species. A population was studied in southern France with a capture-recapture method. The population included resident adults which have a high and constant survival rate (monthly estimate: 0.879), erratic adults (those caught once only), and juveniles which have a lower and constant survival rate. The adult survival rate was not sexbiased but the juvenile survival rate was higher in males (monthly estimates: 0.710 and 0.596 for males and females, respectively). Adult body weight did not vary seasonally. Residents had a higher mean body weight than erratics. Reproduction occurred all the year round. The proportion of reproductive females was higher among residents than among erratics. Population numbers varied seasonally. Our study points out thatM. duodecimcostatus is very different from microtine species which display cyclic fluctuations. Population studies on the subgenusPitymys (which containsM. duodecimcostatus and its closest related species) suggest that they are typically non-cyclic. The importance of social factors in the control of reproduction and maturation was evidenced inM. pinetorum. The role of such factors in the population regulation ofM. duodecimcostatus is discussed.     

Wooded habitat edges as refugia from microtine herbivory in tallgrass prairies

Meadow voles, Microtus pennsylvanicus , affect the species composition, distribution, and succession of plants in grassland ecosystems, but the effects of voles on herbaceous plants when grasslands are bordered by wooded edges is not known. We investigated the impact of wooded edges on vole distribution and herbivory of relatively palatable and unpalatable native prairie plant species by studying five reconstructed tallgrass prairies with wooded edges in central Iowa. A 50×50 m trapping grid at each site was established to determine the proportion of voles captured at various distances from the edge. We found that meadow voles were less abundant at wooded edges and, in general, increased in number toward the prairie interior. Seedlings of purple prairie clover ( Dalea purpurea ) and Illinois bundleflower ( Desmanthus illinoensis ), a relatively palatable and unpalatable species, respectively, were transplanted onto simulated gopher mounds 2, 5, 10, 20 and 30 m from the edge. The number of plants grazed per species per mound was determined 1 week and 4 weeks after planting. The amount of herbivory on both species was significantly different by distance, with fewer plants eaten 2 m from the edge. Interestingly, the amount of herbivory on relatively unpalatable plants did not differ from more palatable plants. Herbivory on both plant species also varied by site, such that sites with lower vole density tended to have lower amounts of herbivory. These results indicate that wooded edges do have an effect on meadow vole distribution and native prairie seedling herbivory. Because voles avoid wooded edges, seedlings of any species may experience a small refuge from herbivory along wooded edges.     

Recovery of evergreen clonal dwarf shrubVaccinium vitis-idaea after simulated microtine herbivory in a boreal forest

The evergreen dwarf shrub lingonberry (Vaccinium vitis-idaea L.) was subjected to microtine herbivory simulations to investigate its recovery in a boreal forest. Beside the control (A), the study included three levels of herbivory: clipping of half the annual branches from 50% of ramets (B), removal of 50% of ramets (C), and removal of 100% of ramets (D). Density, growth, and fecundity of the ramets were monitored during the study. New ramets emerged rapidly from dormant basal buds at the base of the removed ramets in groups C and D. After three growth seasons, 60–117% and 42–112% of density and biomass, respectively, had been regained in the groups damaged relative to the control, the difference being insignificant between the treated groups apparently because of the small sample size. Survival, fecundity and net growth of ramets were not affected by the treatment. Mean dry weight of annual branches in new ramets was lower in the damaged groups than the control. The recovery of the lingonberry was unexpectedly good. The results suggest that, since natural herbivory seldom is as heavy as in this work, the time between population density peaks of microtine rodents is usually long enough for the lingonberry to recover in boreal ecosystems.     

Model of microtine cycles caused by lethal toxins in non-preferred food plants

A recent model of microtine cycles has hypothesized that plant chemical defences can drive the precipitous decline phase, through periodic lethal toxin production (PLTP) by non-preferred plant foods. Here we enumerate possible mechanisms using a previously published model of optimal foraging by one consumer (microtine rodent) of two types of food plant (1 preferred and 1 non-preferred). Rate constants for each of the model parameters were sought from the extensive literature on vole cycles. For a range of likely values of input parameters, we evaluated model fit by applying five empirically derived criteria for cyclic behaviour. These were: cycles with a period length of 2-5 yr, peak densities of 100-350 voles per ha and trough densities of 0-25 ha(-1), ratio of peak to trough densities of 10-100, and the occurrence of a catastrophic collapse in the vole population followed by a prolonged low phase. In contrast to previous models of food-induced microtine cycles, the optimal foraging model successfully reproduced the first four criteria and the prolonged low phase. The criterion of population collapse was met if the non-preferred food began producing lethal toxins at a threshold grazing intensity, as predicted by PLTP. Fewer criteria could be met in variations on the model, in which the non-preferred food was equally as nutritious as the preferred food or was continuously toxic.     

Dispersal and the microtine cycle: comparison of two hypotheses

Summary The hypotheses suggested by Chitty (1960) and by Charnov and Finerty (1980) in order to explain the occurrence of the microtine density cycle are investigated from a theoretical point of view. The former hypothesis assumes that the polymorphic behavioural patterns being observed in natural populations are genetically determined whereas the latter assumes these polymorphic behavioural patterns to be environmentally determined. For both theories we assume a patchy environment with dispersal between patches.We find, on the basis of a series of mathematical models comparing the two hypotheses, that Chitty's hypothesis does not seem to generate cycles whereas the Charnov-Finerty hypothesis may generate persistent density cycles: this is particularly so if dispersing individuals have the capacity to choose which patch to settle in and if the carrying capacity of each patch is high.Work carried out while HWD was visiting the Dept. of Biology, Division of Zoology, University of Oslo on a Norwegian Government Scholarship     

Eusociality: From the First Foragers to the First States

People have always been social. Ethnographic evidence suggests that transfers of food and labor are common among contemporary hunter-gatherers, and they probably were common in Paleolithic groups. Archaeological evidence suggests that cooperative breeding went up as we settled down: as territory defenders became more successful breeders, their helpers’ fertility would have been delayed or depressed. And written evidence from the Neolithic suggests that the first civilizations were often eusocial; emperors fathered hundreds of children, who were provided for and protected by workers in sterile castes. Papers in this issue of Human Nature look at helpers and workers across the eusociality continuum—from hardworking grandmothers and grandfathers, to celibate sisters and brothers, to castrated civil servants—from the first foragers to the first states.