Multiple mating and the evolution of social behavior in the hymenoptera

Summary 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.     

Testing the impact of social forces on the evolution of Sahelian farming systems: A combined agent-based modeling and anthropological approach

This article presents the results of a methodology based on an extensive sociological fieldwork in three different sites settled along a gradient of aridity in Nigerien Sahel. This fieldwork led to build a set of rules for the behaviour of individuals in non-pastoralist villages. We implemented these rules into an agent-based model simulating three village archetypes. Each archetype includes biophysical, economical, social agricultural and livestock modules. Results from simulations with no social transition processes show that villages specialize themselves into different economic activities according to natural resource specificities: A decreasing intensification gradient is observed from the most favoured site, with more local productions and good ecological indicators, to the less-favoured site, with a growing proportion of the population wealth coming from migration remittances and “off-shore” livestock. Two family transition processes were implemented, following field observations and literature-based hypotheses: family organizations evolve between a patriarchal mode and a non-cooperative mode following tensions due to income redistribution. Family inheritance systems evolve from a “customary” one-heir mode to a “local Muslim” mode in which all males inherits land. This evolution depends on family tensions due to land availability. Once introducing these processes, the population of each site differentiates itself into specialized groups according to size, assets and social status. Meanwhile, the group proportions and specializations strongly vary according to the sites but they are all characterized by the emergence of individualistic family types and the increase of the village populations’ robustness.     

The evolution of female social relationships in nonhuman primates

Considerable interspecific variation in female social relationships occurs in gregarious primates, particularly with regard to agonism and cooperation between females and to the quality of female relationships with males. This variation exists alongside variation in female philopatry and dispersal. Socioecological theories have tried to explain variation in female-female social relationships from an evolutionary perspective focused on ecological factors, notably predation and food distribution. According to the current “ecological model”, predation risk forces females of most diurnal primate species to live in groups; the strength of the contest component of competition for resources within and between groups then largely determines social relationships between females. Social relationships among gregarious females are here characterized as Dispersal-Egalitarian, Resident-Nepotistic, Resident-Nepotistic-Tolerant, or Resident-Egalitarian. This ecological model has successfully explained differences in the occurrence of formal submission signals, decided dominance relationships, coalitions and female philopatry. Group size and female rank generally affect female reproduction success as the model predicts, and studies of closely related species in different ecological circumstances underscore the importance of the model. Some cases, however, can only be explained when we extend the model to incorporate the effects of infanticide risk and habitat saturation. We review evidence in support of the ecological model and test the power of alternative models that invoke between-group competition, forced female philopatry, demographic female recruitment, male interventions into female aggression, and male harassment. Not one of these models can replace the ecological model, which already encompasses the between-group competition. Currently the best model, which explains several phenomena that the ecological model does not, is a “socioecological model” based on the combined importance of ecological factors, habitat saturation and infanticide avoidance. We note some points of similarity and divergence with other mammalian taxa; these remain to be explored in detail. Received: 30 September 1996 / Accepted after revision: 20 July 1997     

Biofilm grazing in a higher vertebrate: the western sandpiper, Calidris mauri

We show that a higher vertebrate can graze surficial intertidal biofilm, previously only considered a food source for rasping invertebrates and a few specialized fish. Using evidence from video recordings, stomach contents, and stable isotopes, we describe for the first time the grazing behavior of Western Sandpipers (Calidris mauri) and estimate that biofilm accounts for 45-59% of their total diet or 50% of their daily energy budget. Our finding of shorebirds as herbivores extends the trophic range of shorebirds to primary consumers and potential competitors with grazing invertebrates. Also, given individual grazing rates estimated at seven times body mass per day and flock sizes into the tens of thousands, biofilm-feeding shorebirds could have major impacts on sediment dynamics. We stress the importance of the physical and biological processes maintaining biofilm to shorebird and intertidal conservation.     

Indiscriminate care of offspring predates the evolution of sociality in alloparenting social spiders

Alloparental care—the care of other’s offspring—is a key aspect of sociality in many groups of animals. Understanding how this complex behavior arises requires identifying both the selective forces that may favor it, as well as characteristics of particular lineages that facilitate or hinder its evolution. One potential hindrance is the existence of discrimination against foreign offspring, an obstacle that would need to be overcome in order for alloparental care to evolve. In this study, we explored whether offspring discrimination may have constrained the evolution of alloparental care in social spiders in the genus Anelosimus. Social spiders are known for their cooperative behaviors, which include alloparental care. After quantitatively assessing the extent of alloparenting in the care of egg sacs in natural nests of these spiders, we investigated whether discrimination against foreign egg sacs existed in ancestral pre-social species in the genus. We did so by testing for discrimination between a female’s own and foreign egg sacs in three subsocial sister taxa of each social species investigated. We found no detectable evidence of discrimination in the care of egg sacs by female Anelosimus, regardless of level of sociality. We used these data, along with those from previous studies, to infer that a lack of discrimination is likely the ancestral state in the genus Anelosimus. This supports the idea that offspring discrimination was not a constraint on the evolution of alloparental care in social Anelosimus species. We discuss the evolutionary implications of this finding, and suggest that lack of offspring discrimination may have eased the transition from solitary to cooperative breeding.     

The influence of size-specific indirect interactions in predator-prey systems

Nonlethal indirect interactions between predators often lead to nonadditive effects of predator number on prey survival and growth. Previous studies have focused on systems with at least two different predator species and one prey species. However, most predators undergo extreme ontological changes in phenotype such that interactions between different-sized cohorts of a predator and its prey could lead to nonadditive effects in systems with only two species. This may be important since different-sized individuals of the same species can differ more in their ecology than similar-sized individuals of different species. This study examined trait-mediated indirect effects in a two-species system including a cannibalistic predator with different-sized cohorts and its prey. I tested for these effects using larvae of two stream salamanders, Gyrinophilus porphyriticus (predator) and Eurycea cirrigera (prey), by altering the densities and combinations of predator size classes in experimental streams. Results showed that the presence of large individuals can significantly reduce the impact of density changes of smaller conspecifics on prey survival through nonlethal means. In the absence of large conspecifics, an increase in the relative frequency of small predators significantly increased predation rates, thereby reducing prey survival. However, with large conspecifics present, increasing the density of small predators did not decrease prey survival, resulting in a 14.3% lower prey mortality than predicted from the independent effects of both predator size classes. Small predators changed their microhabitat use in the presence of larger conspecifics. Prey individuals reduced activity in response to large predators but did not respond to small predators. Both predators reduced prey growth. These results demonstrate that the impact of a predator can be significantly altered by two different types of trait-mediated indirect effects in two-species systems: between different-sized cohorts and between different cohorts and prey. This study demonstrates that predictions based on simple numerical changes that assume independent effects of different size classes or ignore size structure can be strongly misleading. We need to account for the size structure within predator populations in order to predict how changes in predator abundance will affect predator-prey dynamics.     

Revisiting the evolution of ecological specialization, with emphasis on insect-plant interactions

Ecological specialization is a fundamental and well-studied concept, yet its great reach and complexity limit current understanding in important ways. More than 20 years after the publication of D. J. Futuyma and G. Moreno's oft-cited, major review of the topic, we synthesize new developments in the evolution of ecological specialization. Using insect-plant interactions as a model, we focus on important developments in four critical areas: genetic architecture, behavior, interaction complexity, and macroevolution. We find that theory based on simple genetic trade-offs in host use is being replaced by more subtle and complex pictures of genetic architecture, and multitrophic interactions have risen as a necessary framework for understanding specialization. A wealth of phylogenetic data has made possible a more detailed consideration of the macroevolutionary dimension of specialization, revealing (among other things) bidirectionality in transitions between generalist and specialist lineages. Technological advances, including genomic sequencing and analytical techniques at the community level, raise the possibility that the next decade will see research on specialization spanning multiple levels of biological organization in non-model organisms, from genes to populations to networks of interactions in natural communities. Finally, we offer a set of research questions that we find to be particularly pressing and fruitful for future research on ecological specialization.     

Boldness by habituation and social interactions: a model

Most studies of animal personality attribute personality to genetic traits. But a recent study by Magnhagen and Staffan (Behav Ecol Sociobiol 57:295–303, 2005) on young perch in small groups showed that boldness, a central personality trait, is also shaped by social interactions and by previous experience. The authors measured boldness by recording the duration that an individual spent near a predator and the speed with which it fed there. They found that duration near the predator increased over time and was higher the higher the average boldness of other group members. In addition, the feeding rate of shy individuals was reduced if other members of the same group were bold. The authors supposed that these behavioral dynamics were caused by genetic differences, social interactions, and habituation to the predator. However, they did not quantify exactly how this could happen. In the present study, we therefore use an agent-based model to investigate whether these three factors may explain the empirical findings. We choose an agent-based model because this type of model is especially suited to study the relation between behavior at an individual level and behavioral dynamics at a group level. In our model, individuals were either hiding in vegetation or feeding near a predator, whereby their behavior was affected by habituation and by two social mechanisms: social facilitation to approach the predator and competition over food. We show that even if we start the model with identical individuals, these three mechanisms were sufficient to reproduce the behavioral dynamics of the empirical study, including the consistent differences among individuals. Moreover, if we start the model with individuals that already differ in boldness, the behavioral dynamics produced remained the same. Our results indicate the importance of previous experience and social interactions when studying animal personality empirically.     

Lifetime reproductive success in the spotted sandpiper (Actitis macularia) : sex differences and variance components

Summary Lifetime reproductive success (LRS) of male (N=103) and female (N= 66) spotted sandpipers (Actitis macularia) was studied for 13 years of a 17-year study at Little Pelican Island, Leech Lake, Minnesota. There was no sex difference in longevity, but females had significantly more mates, eggs, chicks, fledged young, and young returning in subsequent years than did males. Variance in LRS was partitioned into five life-history components: longevity (L), mates per year (M), eggs per mate (E), proportion eggs hatched (H), and proportion of chicks fledged (F). For both sexes, F accounted for the greatest proportion of variance in LRS (males, 43%; females, 47%), followed by L (males, 26%; females, 43%) and H (males, 21%; females, 28%). Positive covariance between H and F was consistent with predator-caused clutch and brood loss. Contrary to our expectations, males had a higher coefficient of variation in reproductive success than did females. This was because males were relatively more likely than females to produce no young.Offprint requests to: L.W. Oring at the current address     

Using phylogenetic comparative methods to gain insight into the evolution of social complexity

Behavioral Ecology and Sociobiology - Social complexity has been one of the recent emerging topics in the study of animal and human societies, but the concept remains both poorly defined and...     

The effect of social interactions on calling energetics in the gray treefrog (Hyla versicolor)

Summary The vocal behavior of Hyla versicolor was studied in the field by means of behavioral observations and playback experiments, and these data were coupled with measurements of oxygen consumption in calling frogs to estimate the effect of social interactions on calling energetics. Male gray treefrogs have intense calls (median peak SPL=109 dB, fast RMS SPL=100 dB at 50 cm). At an air temperature of 23° C, males produced an average of 1,200–1,300 calls/h for 2–4 h per night. Calling rates and call durations differed among individuals, but were relatively constant for each male during periods of sustained calling. Males in dense choruses gave calls about twice as long as isolated males, but produced calls at about half the rate. Consequently, total calling effort and estimated aerobic costs were largely independent of chorus density. Playbacks of recorded calls to males in the field elicited increases in call duration and decreases in calling rate, regardless of the rate or duration of the stimulus. Males gave longer calls in response to long calls or to stimuli presented at high rates, but they did not precisely match either stimulus rate or duration. Calling effort and estimated oxygen consumption changed only slightly during stimulus playbacks. These results indicate that male-male competition elicits pro-found changes in the vocal behavior of calling males, but these changes have little effect on energy expenditure. We estimated that most calling males had metabolic rates of about 1.7–1.8 ml O₂/(g\h), or about 280 J/h for an average size (8.6 g) male at 20° C. Although changes in call duration and calling rate did not affect aerobic costs of calling, males producing long calls at slow rates called for fewer hours per night than males producing shorter calls at higher rates. This suggests that calling time may be limited by the rate at which muscle glycogen reserves are depleted.     

Natal dispersal in two mice species with contrasting social systems

We compared the natal dispersal behaviour of two mice species under laboratory conditions. Natal dispersal is a movement of an animal from its birthplace to its breeding area. This behaviour is known to be influenced by the mating system. In polygamous species, males are more likely to disperse, while in most of the monogamous species, both sexes disperse. Our subjects, the house mouse (Mus musculus) and the mound-building mouse (Mus spicilegus) are two sympatric species of the genus Mus. Both are native in Hungary, but they differ in their habitat type mating system and overwintering strategy. The house mouse is a polygynous species and adapted to human environment, known for mature and reproduce early. On the contrary, the mound-building mice are monogamous, and they inhabit extensively used agricultural fields, where they spend the unfavourable winter period in nest chambers under mounds, which they construct from soil and plant material. Successful overwintering for this species demands delayed maturity and reduced dispersion during the winter. Our results showed that the natal dispersal of these two species differ; both sexes of the mound-building mice dispersed later than the house mice, where a difference between sexes also occurs; house mice males dispersed earlier than females. The mound-building mice showed no sexual dimorphism in this behaviour.     

Influence of residency and social odors in interactions between competing native and alien rodents

Residency status of individuals in populations may be an important determinant of the outcomes of interspecific competition between native and introduced species. We examined direct behavioral interactions between two similarly sized rodents, the alien Rattus rattus and native Rattus fuscipes when they were respective residents and intruders in a small enclosure. Resident individuals were dominant in their behaviors toward intruders irrespective of the species that was resident. In contrast, interactive behaviors between conspecifics were often neutral or amicable, supporting suggestions that R. rattus and R. fuscipes are social animals. We then tested whether rodent species use heterospecific odors to avoid aggressive competitive interactions and partition space in the field. Neither R. fuscipes nor R. rattus responded to traps scented with the odors of male or female heterospecifics. If R. fuscipes does not recognize the odor of introduced R. rattus, then odors will not be cues to the presence or territorial space of competing heterospecifics. Rather, findings from both enclosure and field trials suggest that direct aggressive interactions between individual R. rattus and R. fuscipes probably facilitate segregation of space between these two species in wild populations, where resident animals may typically be the winners and exclude heterospecific intruders. These findings have implications for the invasion success of introduced rodents such as R. rattus into intact forests, where native populations may have competitive advantage because of their residency status.     

Evidence for differential selection and potential adaptive evolution in the worker caste of an inquiline social parasite

Social parasites exploit the socially managed resources of social insect colonies in order to maximise their own fitness. The inquilines are among the most specialised social parasites, because they are dependent on being fully integrated into their host's colony throughout their lives. They are usually relatives of their host and so share ancestral characteristics (Emery's rule). Closely related inquiline-host combinations offer a rare opportunity to study trade-offs in natural selection. This is because ancestral adaptations to a free-living state (e.g. the production of a worker caste) become redundant and may be replaced by novel, parasitic traits as the inquiline becomes more specialised. The dynamics of such processes are, however, unknown as virtually all extant inquiline social parasites have completely lost their worker caste. An exception is Acromyrmex insinuator, an incipient permanent social parasite of the leaf-cutting ant Acromyrmex echinatior. In the present study, we document the size distribution of parasite and host workers and infer how selection has acted on A. insinuator to reduce, but not eliminate, its investment in a worker caste. We show that the antibiotic producing metapleural glands of these parasite workers are significantly smaller than in their host counterparts and we deduce that the metapleural gland size in the host represents the ancestral state. We further show experimentally that social parasite workers are more vulnerable to the general insect pathogenic fungus Metarhizium than are host workers. Our findings suggest that costly disease resistance mechanisms are likely to have been lost early in inquiline evolution, possibly because active selection for maintaining these traits became less when parasite workers had evolved the ability to exploit the collective immune system of their host societies.     

The evolution of polyandry by queens in social Hymenoptera: the significance of the timing of removal of diploid males

Summary Multiple mating by queens in social Hymenoptera with single locus sex determination may be an adaptation to reduce the effect of genetic load caused by the production of diploid males, if there is a concave relationship between queen fitness and the proportion of diploid male offspring in the colony. In this situation queens should be selected to reduce the variance in the production of diploid male offspring by multiple mating. It has been suggested that this concave relationship occurs in species such as the honey bee, Apis mellifera, in which reproduction occurs near the peak of colony population. This paper suggests that the timing of diploid male removal may influence mating frequency, with early removal of diploid males favoring multiple mating and late removal of diploid males favoring single mating. This idea is explored in two ways. A mathematical model shows that cell use in the brood area of species that rear young in cells will be more efficient with multiple mating. This would favor multiple mating in species, such as the honey bee, in which brood rearing is constrained by the usable area of the brood chamber. Secondly, comparison of polyandrous honey bees (early removal of diploid males as young larvae) with monandrous fire ants, Solenopsis invicta, and Melipona bees (non-removal of immature diploid males) suggests that in the species without diploid male removal, variance reduction may reduce queen fitness. Suggestions are made for testing this hypothesis.     

Soft systems thinking and social learning for adaptive management

The success of adaptive management in conservation has been questioned and the objective-based management paradigm on which it is based has been heavily criticized. Soft systems thinking and social-learning theory expose errors in the assumption that complex systems can be dispassionately managed by objective observers and highlight the fact that conservation is a social process in which objectives are contested and learning is context dependent. We used these insights to rethink adaptive management in a way that focuses on the social processes involved in management and decision making. Our approach to adaptive management is based on the following assumptions: action toward a common goal is an emergent property of complex social relationships; the introduction of new knowledge, alternative values, and new ways of understanding the world can become a stimulating force for learning, creativity, and change; learning is contextual and is fundamentally about practice; and defining the goal to be addressed is continuous and in principle never ends. We believe five key activities are crucial to defining the goal that is to be addressed in an adaptive-management context and to determining the objectives that are desirable and feasible to the participants: situate the problem in its social and ecological context; raise awareness about alternative views of a problem and encourage enquiry and deconstruction of frames of reference; undertake collaborative actions; and reflect on learning.     

The mechanism of nestmate discrimination in the tropical social wasp Ropalidia marginata and its implications for the evolution of sociality

Summary We have demonstrated that females of the primitively eusocial tropical wasp Ropalidia marginata can discriminate nestmates from nonnestmates outside the context of their nests. This was accomplished by recroding all behavioural interactions in a neutral arena and comparing tolerance levels. In order for these wasps to make such a discrimination, however, it was essential that after eclosion both the discriminated and the discriminating animals were exposed to their respective natal nests and nestmates. The results suggest that both recognition labels and templates are acquired by the animals from sources outside their body, perhaps from their nest or nestmates. It is thus unlikely that different genetic lines within a colony can be distinguished. We conclude, therefore, that genetic asymmetries created by haplodiploidy, but often broken down by multiple mating and polygyny, are not restored by preferential altruism towards full rather than half sisters by means of kin recognition. Hence we recommend caution in ascribing the multiple origins of eusociality in the Hymenoptera to haplodiploidy.