Fitness consequences of ecological constraints and implications for the evolution of sociality in an incipiently social bee

Ecological constraints such as resource limitation, unfavourable weather conditions, and parasite pressure have long been considered some of the most important selective pressures for the evolution of sociality. In the present study, we assess the fitness consequences of these three ecological factors on reproductive success of solitary nests and social colonies in the socially polymorphic small carpenter bee, Ceratina australensis, based on 982 nests collected over four reproductive periods. Nest site limitation was predicted to decrease opportunities for independent nest initiation and increase the frequency of social nesting. Nest sites were not limiting in this species and the frequency of social nesting was consistent across the four brood‐rearing periods studied. Unfavourable weather was predicted to lower the frequency of female dispersal from their natal nests and to limit the brood‐rearing season; this would increase the frequency and fitness of social colonies. Daily temperature and precipitation accumulation varied between seasons but were not correlated with reproductive success in this bee. Increased parasite pressure is predicted to increase the frequency and fitness of social colonies because solitary bees must leave the nest unattended during foraging bouts and are less able to defend the nest against parasites. Severe parasitism by a chalcid wasp (Eurytoma sp.) resulted in low reproductive success and total nest failure in solitary nests. Social colonies had higher reproductive success and were never extirpated by parasites. The high frequency of solitary nests suggests that this is the optimal strategy. However, social colonies have a selective advantage over solitary nesting females during periods of extreme parasite pressure, and we suggest that social nesting represents a form of bet‐hedging against unpredictable fluctuations in parasite number. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 57–67.     

Why Wasp Foundresses Change Nests: Relatedness,Dominance, and Nest Quality

The costs and benefits of different social options are best understood when individuals can be followed as they make different choices, something that can be difficult in social insects. In this detailed study, we follow overwintered females of the social wasp Polistes carolina through different nesting strategies in a stratified habitat where nest site quality varies with proximity to a foraging area, and genetic relatedness among females is known. Females may initiate nests, join nests temporarily or permanently, or abandon nests. Females can become helpers or egglayers, effectively workers or queens. What they actually do can be predicted by a combination of ecological and relatedness factors. Advantages through increased lifetime success of individuals and nests drives foundresses of the social wasp Polistes from solitary to social nest founding. We studied reproductive options of spring foundresses of P. carolina by monitoring individually-marked wasps and assessing reproductive success of each foundress by using DNA microsatellites. We examined what behavioral decisions foundresses make after relaxing a strong ecological constraint, shortage of nesting sites. We also look at the reproductive consequences of different behaviors. As in other Polistes, the most successful strategy for a foundress was to initiate a nest as early as possible and then accept others as subordinates. A common feature for many P. carolina foundresses was, however, that they reassessed their reproductive options by actively monitoring other nests at the field site and sometimes moving permanently to new nests should that offer better (inclusive) fitness prospects compared to their original nests. A clear motivation for moving to new nests was high genetic relatedness; by the end of the foundress period all females were on nests with full sisters.     

Queen-worker conflict and social parasitism in bumble bees (Hymenoptera: Apidae)

Psithyrus ashtoni (Hymenoptera: Apidae) is an obligate, workerless bumble, bee social parasite which invades nests of Bombus affinis. Although parasites are limited by host worker defence to invading very small colonies, there is considerable flexibility in the way parasites control host brood bionomics once they are accepted inside the nest. A study of 46 parasitized and 22 non-parasitized laboratory colonies of B. affinis showed that P. ashtoni females cohabited with host queens and workers while the worker force increased, but not to the maximum normally achieved in non-parasitized nests. While colony reproductive success was correlated with the number of workers reared, parasites risked being killed or ejected from the comb by workers, after the queen had lost dominance. Host bees usually succeeded in rearing offspring, and Psithyrus reproductive success was related to the ability of parasites to control proportional investment in the two species. In addition to displacing P. ashtoni females, host bees ate the eggs of parasites and ejected their larvae. These behaviours were also exhibited by workers in the later stages of development of non-parasitized colonies. These results indicate that social parasites are at least partially subject to the conflict of genetic self-interest between the queen and her workers which is believed to influence the control of reproductive investment in haplodiploid Bombus societies.     

Social structure of perennial Vespula squamosa wasp colonies

Many social species show variation in their social structure in response to different environmental conditions. For example, colonies of the yellowjacket wasp Vespula squamosa are typically headed by a single reproductive queen and survive for only a single season. However, in warmer climates, V. squamosa colonies sometimes persist for multiple years and can grow to extremely large size. We used genetic markers to understand patterns of reproduction and recruitment within these perennial colonies. We genotyped V. squamosa workers, pre‐reproductive queens, and males from perennial colonies in the southeastern United States at 10 polymorphic microsatellite loci and one mitochondrial DNA locus. We found that V. squamosa from perennial nests were produced by multiple reproductives, in contrast to typical annual colonies. Relatedness of nestmates from perennial colonies was significantly lower than relatedness of nestmates from annual colonies. Our analyses of mitochondrial DNA indicated that most V. squamosa perennial colonies represented semiclosed systems whereby all individuals belonged to a single matriline despite the presence of multiple reproductive females. However, new queens recruited into perennial colonies apparently mated with non‐nestmate males. Notably, perennial and annual colonies did not show significant genetic differences, supporting the hypothesis that perennial colony formation represents an instance of social plasticity. Overall, our results indicate that perennial V. squamosa colonies show substantial changes to their social biology compared to typical annual colonies and demonstrate variation in social behaviors in highly social species.     

Colony structure and caste distribution in living trees of the Ryukyu drywood termite,Neotermes sugioi (Blattodea: Kalotermitidae) in Okinawa Island

Termites are major pests of houses and buildings, and also living plants such as agricultural crops, trees in forests, urban areas and gardens. However, in Japan, the basic ecology of termites nesting in living trees is not fully understood. In this study, we observed 255 colonies (nests) of the drywood termite Neotermes sugioi, collected in the field on Okinawa Island, and reported the frequency composition of the reproductive castes, the size of wood with termite gallery, the population size of colonies, and the relative position of the reproductive and non-reproductive castes within nests. Most colonies were headed by a primary queen and a primary king. However, colonies headed only by primary queens, primary kings, or neotenic kings, each accounted for approximately 5% of the colonies. A colony size of 1,000– 4,000 individuals (2058.2 ± 1695.0 [mean ± SD]) was common and the average length of colony branches was less than 100 cm. Queens and kings were found in the same or nearby nest areas, and more predominantly in the central or root side of nest wood areas. The termites may experience colony fragmentation and reproductive loss as a consequence of typhoons. Incipient colonies (i.e., colonies at an early stage of development) were found on 11.3% of branches of Leucaena leucocephala that did not show any obvious signs of infestation. In future research, it will be necessary to update the list of trees damaged by this termite species, compare the damage by tree species, and evaluate the economic impact.     

The Role of Non-Foraging Nests in Polydomous Wood Ant Colonies

A colony of red wood ants can inhabit more than one spatially separated nest, in a strategy called polydomy. Some nests within these polydomous colonies have no foraging trails to aphid colonies in the canopy. In this study we identify and investigate the possible roles of non-foraging nests in polydomous colonies of the wood ant Formica lugubris. To investigate the role of non-foraging nests we: (i) monitored colonies for three years; (ii) observed the resources being transported between non-foraging nests and the rest of the colony; (iii) measured the amount of extra-nest activity around non-foraging and foraging nests. We used these datasets to investigate the extent to which non-foraging nests within polydomous colonies are acting as: part of the colony expansion process; hunting and scavenging specialists; brood-development specialists; seasonal foragers; or a selfish strategy exploiting the foraging effort of the rest of the colony. We found that, rather than having a specialised role, non-foraging nests are part of the process of colony expansion. Polydomous colonies expand by founding new nests in the area surrounding the existing nests. Nests founded near food begin foraging and become part of the colony; other nests are not founded near food sources and do not initially forage. Some of these non-foraging nests eventually begin foraging; others do not and are abandoned. This is a method of colony growth not available to colonies inhabiting a single nest, and may be an important advantage of the polydomous nesting strategy, allowing the colony to expand into profitable areas.     

Developmental plasticity in the queen-polymorphic ant Temnothorax longispinosus

Females of social Hymenoptera show developmental plasticity in response to varying social and environmental conditions, though some species have strong genetic influences on the form of the female reproductives. In ants, a queen polymorphism can occur in which large queens initiate new colonies on their own, while small queens enter established nests. Most queen polymorphisms studied to date originate due to genetic differences between individuals of differing form. Here, we report on the development of female form in response to social factors within the nest in the queen-polymorphic ant Temnothorax longispinosus. Three queen size morphs occur: a rare large queen with higher fat stores that can found new colonies independently, a large queen that has low fat stores and is behaviorally flexible, and a small queen that rejoins the natal nest. Both in nesting units collected from the field and those reared in the lab, queen presence during larval development led to fewer larvae developing as gynes (virgin, winged queens), and most of those gynes were the small morph. This queen effect is transferred to developing gyne larvae by close, physical interaction between queens and workers, and causes slower larval development. We conclude that gyne size, and therefore reproductive behavior, in T. longispinosus is developmentally plastic in response to queen presence. Plasticity in reproductive behavior may be an adaptive response to the nest sites utilized by this species. T. longispinosus nests predominantly in acorns and hickory nuts, which can vary dramatically from 1 year to the next. Since queens are more likely to be present in each nesting unit when fewer nest sites are available, the queen effect that results in more small gynes produced links the expression of colony-founding traits to ecological conditions across habitat patches.     

Soldier diterpene patterns in relation with aggressive behaviour,spatial distribution and reproduction of colonies in Nasutitermes princeps

The territorial organization of the colonies of N. princeps (Desneux) (Isoptera: Temitidae) was studied by four methods: maps of nest systems, tests of aggressiveness, comparison of soldier diterpene patterns, and determination of the reproductive status of the nests. The diterpene patterns are rather variable among sympatric colonies, and allow the tracing of soldiers from their respective colonies throughout their foraging range. Soldiers from neighbouring nests display in some instances closely resembling diterpene patterns, suggesting close genetic relatedness and polycalic colonies, i.e. composed of several linked nests spread over large territories. Most likely, N, princeps colonies reproduce by budding. The number and type of reproductives found in the nests are consistent with this hypothesis. Tests of aggressiveness supported the above conclusions, but absence of aggression did not always indicate that the termites belonged to the same colony.     

Does cooperation mean kinship between spatially discrete ant nests?

Eusociality is one of the most complex forms of social organization, characterized by cooperative and reproductive units termed colonies. Altruistic behavior of workers within colonies is explained by inclusive fitness, with indirect fitness benefits accrued by helping kin. Members of a social insect colony are expected to be more closely related to one another than they are to other conspecifics. In many social insects, the colony can extend to multiple socially connected but spatially separate nests (polydomy). Social connections, such as trails between nests, promote cooperation and resource exchange, and we predict that workers from socially connected nests will have higher internest relatedness than those from socially unconnected, and noncooperating, nests. We measure social connections, resource exchange, and internest genetic relatedness in the polydomous wood ant Formica lugubris to test whether (1) socially connected but spatially separate nests cooperate, and (2) high internest relatedness is the underlying driver of this cooperation. Our results show that socially connected nests exhibit movement of workers and resources, which suggests they do cooperate, whereas unconnected nests do not. However, we find no difference in internest genetic relatedness between socially connected and unconnected nest pairs, both show high kinship. Our results suggest that neighboring pairs of connected nests show a social and cooperative distinction, but no genetic distinction. We hypothesize that the loss of a social connection may initiate ecological divergence within colonies. Genetic divergence between neighboring nests may build up only later, as a consequence rather than a cause of colony separation.     

Sequential mating patterns suggest extra-pair mating is not part of a mixed reproductive strategy by female red-winged blackbirds

Studies aimed at determining why female birds often produce offspring sired by males other than their social mates generally compare traits of social and genetic mates. Here I examine paternity patterns in nests of the same female red-winged blackbirds (Agelaius phoeniceus) in successive breeding seasons. Returning females preferentially selected their former social mates as their new social mates when those males were present. However, paternity patterns were much less consistent. A female''s behaviour (faithful versus unfaithful) in one year did not predict her behaviour the following year. Females unfaithful in successive years did not prefer the same extra-pair males. Females unfaithful in one year that switched social mates the next year did not preferentially choose their former extra-pair mates as their new social mates. By switching genetic mates, females did not generally improve the quality of their mates. These results, together with previous analyses, suggest that female blackbirds in this population have little control over extra-pair mating. Although females may benefit from extra-pair mating because extra-pair males are generally longer lived, paternity patterns in this population are not consistent with extra-pair mating being part of a finely tuned female reproductive strategy.     

Evolution of social behaviour in the primitively eusocial wasp Ropalidia marginata: do we need to look beyond kin selection?

Ropalidia marginata is a primitively eusocial wasp widely distributed in peninsular India. Although solitary females found a small proportion of nests, the vast majority of new nests are founded by small groups of females. In such multiple foundress nests, a single dominant female functions as the queen and lays eggs, while the rest function as sterile workers and care for the queen''s brood. Previous attempts to understand the evolution of social behaviour and altruism in this species have employed inclusive fitness theory (kin selection) as a guiding framework. Although inclusive fitness theory is quite successful in explaining the high propensity of the wasps to found nests in groups, several features of their social organization suggest that forces other than kin selection may also have played a significant role in the evolution of this species. These features include lowering of genetic relatedness owing to polyandry and serial polygyny, nest foundation by unrelated individuals, acceptance of young non-nest-mates, a combination of well-developed nest-mate recognition and lack of intra-colony kin recognition, a combination of meek and docile queens and a decentralized self-organized work force, long reproductive queues with cryptic heir designates and conflict-free queen succession, all resulting in extreme intra-colony cooperation and inter-colony conflict.     

Seasonal patterns of egg production in field colonies of the termite <Emphasis Type="Italic">Reticulitermes speratus</Emphasis> (Isoptera: Rhinotermitidae)

This is the first report on the annual egg production patterns in mature termite colonies in the field. Data on the seasonal patterns of egg production in field colonies are very important for understanding the annual colony growth schedule, resource allocation, and population dynamics of the termites. However, collecting the eggs from a sufficient number of colonies is extremely difficult in Reticulitermes termites because their multiple-site nesting makes it difficult to find the reproductive center of the colonies. Here, we first show the seasonal pattern of egg production in the subterranean termite Reticulitermes speratus by collecting the reproductive center of ten colonies each month from April through October. We had to destructively examine dozens of nests to find eggs from enough field colonies each month. Mature field colonies began to produce eggs in late May, soon after the swarming season, and the egg production rate (EPR) reached its maximum in early July. The eggs hatched until late October. The EPR was significantly correlated with the average monthly temperature. Additional investigation of the egg distributions in the nests showed that most eggs were kept around the royal cell, which contained the reproductives. The largest colony had 109 supplemental queens and 94,023 eggs, suggesting that each queen produced an average of 24.7 eggs per day, based on the known mean hatching period of an inseminated egg of 34.95±0.12 (SE) days.     

Intraspecific queen parasitism in a highly eusocial bee

Insect societies are well-known for their advanced cooperation, but their colonies are also vulnerable to reproductive parasitism. Here, we present a novel example of an intraspecific social parasitism in a highly eusocial bee, the stingless bee Melipona scutellaris. In particular, we provide genetic evidence which shows that, upon loss of the mother queen, many colonies are invaded by unrelated queens that fly in from unrelated hives nearby. The reasons for the occurrence of this surprising form of social parasitism may be linked to the fact that unlike honeybees, Melipona bees produce new queens in great excess of colony needs, and that this exerts much greater selection on queens to seek alternative reproductive options, such as by taking over other nests. Overall, our results are the first to demonstrate that queens in highly eusocial bees can found colonies not only via supersedure or swarming, but also by infiltrating and taking over other unrelated nests.     

An alternative strategy for maintenance of eusociality after nest destruction: new nest construction in a primitively eusocial wasp

Although nests are central to colonial life in social insects, nests are sometimes damaged by predators or natural disasters. After nest destruction, individuals usually construct new nests. In this case, a sophisticated mechanism like the scent trail pheromone used in large insect colonies that recruit individuals to new nest sites would be important for the maintenance of eusociality. In independent-founding Polistes wasps, it is well known that queens enforce workers physiologically on the natal nests even if evidence of trail pheromone use has not been exhibited. We investigated the effect of the queen on an alternative strategy for the maintenance of eusociality by first females after nest destruction in the primitively eusocial wasp Polistes chinensis. We predicted that the first females in queen-absent colonies have various behavioral options after nest destruction. Even if the females construct new nests cooperatively with other individuals, the new nest construction should be conducted more smoothly in queen-present colonies because the queens regulate the behavior of wasps. We made wasps construct new nests by removing the entire brood from existing nests. The presence of the queen did not cause variation in the alternative strategy of the first females, as the first females (workers) usually constructed new nests cooperatively irrespective of the queen-presence. Thus, the workers in the queenpresent colonies affiliated to the new nest construction more smoothly and constructed new nests more efficiently than workers in the queen-absent colonies. Our results suggest that the presence of the queen is important for maintaining eusociality in primitively eusocial wasps after nest destruction. Received 8 February 2005; revised 5 October 2005; accepted 17 October 2005.     

Subfamily‐dependent alternative reproductive strategies in worker honeybees

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.     

Anti-predator behaviour in the ant Pheidole desertorum: The importance of multiple nests

The relationship between emigrations and anti-predator behaviour in the ant Pheidole desertorum was investigated in the field. Frequent emigrations in P. desertorum result in the colony having multiple nests, of which only one is occupied at a time. A field procedure demonstrated that the ants quickly find and enter the unoccupied nests after a nest evacuation caused by the army ant Neivamyrmex nigrescens. When colonies were denied access to their unoccupied nests after an evacuation, survival of the brood and alates was significantly lower than in colonies allowed access to all their nests. These results suggest that emigrations in P. desertorum are part of a defence strategy against army ants.     

Extreme host specificity by Microdon mutabilis (Diptera: Syrphiae), a social parasite of ants

Larvae of the syrphid fly Microdon mutabilis are social parasites which live up to two years, feeding on ant brood in nests of Formica lemani ants. We questioned why M. mutabilis is extremely localized when its host is widespread and abundant. Like endoparasitic diseases, social parasites must penetrate formidable defences before ''infecting'' their hosts. This occurs during the egg stage of M. mutabilis: females are sedentary and oviposit at F. lemani nest entrances, which workers treat as part of their nest, leaving the thin-shelled eggs vulnerable to attack for 10 to 14 days before hatching. We describe experiments which show a strong maternal effect in M. mutabilis. New-laid eggs had > 95% survival when introduced to the individual ant colony that reared each mother fly or to its close neighbours, but survival declined as a sigmoidal logistic function of distance from the mother nest, with F. lemani colonies from 2 and 30 km away killing 80 and > 99% of eggs, respectively, within 24 h. Attacks on eggs also increased in proportion to the delay before introduction to laboratory nests. We suggest that they may be coated with a mimetic chemical disguise that lasts for three to four days after oviposition. The results indicate extreme local adaptation by an M. mutabilis population not simply to one species of host, but to an individual host population and possibly to local strains or family groups within an F. lemani population. This conclusion is discussed in terms of virulence, transmission and coevolution in parasitic diseases.     

Variation in cuticular hydrocarbon signatures, hormonal correlates and establishment of reproductive dominance in a polistine wasp

In many social insects the relationship between reproductive dominance and physiological correlates is poorly understood. Recent evidence now strongly suggests that cuticular hydrocarbons are important in reproductive differentiation in these societies where they are used as signals of ovarian activity in reproductive females. In this study we investigated the relationship between reproductive dominance, size of the corpora allata (CA, producer of Juvenile Hormone, JH) and the proportions of cuticular hydrocarbons present on the cuticle in overwintering foundresses and both associative (polygynous) and solitary (monogynous) pre-emergence colonies of the social wasp Polistes dominulus. Size of the CA was positively correlated with ovarian development in polygynous colonies. In contrast, solitary foundresses possessed significantly smaller CAs than dominant foundresses from polygynous nests, yet ovarian activity was similar for both female types. CA size variation was associated with variation in cuticular hydrocarbon proportions. Overwintering, solitary, dominant and subordinate (from associative nests) females all possessed distinctive cuticular chemical profiles revealed by multivariate discriminant analyses. Our data indicate that the social environment strongly affects reproductive physiology in this wasp, and we discuss the role of cuticular hydrocarbons in reproductive signaling in P. dominulus and other social insects.     

Genetic variation within social insect colonies reduces parasite load

In colonies of social Hymenoptera (ants, bees and wasps), workers are often not very closely related to each other, because queens mate with several different males (polyandry) or because several functional queens are present (polygyny). Both characteristics increase genetic variation among the queens'' reproductive and worker offspring, but the benefits of this increased variation remain obscure. Here we report an experiment where genetically homogeneous and genetically heterogeneous colonies of the bumble bee, Bombus terrestris, have been exposed to parasitism under field conditions. Colonies of high or low genetic variation were achieved by adding and removing brood from donor colonies. The results showed a consistent effect in that genetically variable colonies experienced reduced parasite loads, i.e. lower prevalence, intensity and parasite species richness, for a range of protozoa, nematodes, mites or parasitoids affecting the workers. We therefore propose that polyandry and/or polygyny of social insects may be beneficial under parasitism.     

Food resources, chemical signaling, and nest mate recognition in the ant Formica aquilonia

Animals such as social insects that live in colonies can recognizeintruders from other colonies of the same or different speciesusing colony-specific odors. Such colony odors usually haveboth a genetic and an environmental origin. When within-colonyrelatedness is high (i.e., one or very few reproductive queens),colonies comprise genetically distinct entities, and recognitionbased on genetic cues is reliable. However, when nests containmultiple queens and colonies comprise multiple nests (polydomy),the use of purely genetically determined recognition labelsmay become impractical. This is due to high within-colony geneticheterogeneity and low between-colony genetic heterogeneity.This may favor the use of environmentally determined recognitionlabels. However, because nests within polydomous colonies maydiffer in their microenvironment, the use of environmental labelsmay also be impractical unless they are actively mixed amongthe nests. Using a laboratory experiment, we found that bothisolation per se and diet composition influenced the cuticularchemical profiles in workers of Formica aquilonia. In addition,the level of aggression increased when both the proportionsof dietary ingredients and the availability of food were altered.This suggests that increased aggression was mediated by changesin the chemical profile and that environmental cues can mediaterecognition between colonies. These results also suggest thatthe underlying recognition cues are mutable in response to extrinsicfactors such as the amount and the composition of food.