Increased nest cofounding and high intra-colony relatedness in the bee Exoneura bicolor (Hymenoptera: Apidae): Results from an experimental situation

Abstract Identifying differences in a key social trait between two populations of die same species is important for understanding the evolution of sociality. Previous studies of new colonies in Exoneura bicolor, an Australian allodapine bee, have shown that there are high levels of kin cofounding in a montane population. The only study to examine intra-colony relatedness in a heathland population has found that new multifemale colonies are not formed by kin. In this study we used an experiment to investigate both cofounding behaviour and intra-colony relatedness in E. bicolor from a heathland population. Nest substrate was placed either 0.05 or 1 m distant from source nests in a novel environment. Although there were no differences in cofounding rate or intra-colony relatedness between die two treatments there was, overall, a high rate of cofounding: 53% of new nests were multifemale, approximately twice as high as found in previous field-based studies. Relatedness among cofoundresses was not only different from zero, ^r± SE = 0.597 ± 0.097, but almost identical to that found in montane populations. A constraint, such as nest substrate distribution, is suggested as a proximate factor affecting the expression of cofounding behaviour in E. bicolor. The implication of such proximate constraints for inferring the phylogenetic origins of social behaviour is discussed.     

Sociality in the Australian Allodapine Bee Brevineura elongata: Small Colony Sizes Despite Large Benefits to Group Living

Allodapine bees (family Apidae, subfamily Xylocopinae) provide substantial material for investigating the evolution of sociality because of their wide variation in colony size, life history traits, and caste differentiation. Two recent studies have shown that the Australian allodapine genus Brevineura exhibits a strong increase in per capita brood production (PCBP) in social colonies compared to single-female nests. However both species previously examined, B. xanthoclypeata and B. froggatti, show relatively few multi-female nests, which is puzzling considering the apparently large advantages for group-living in these species. Here we show that in a third species, B. elongata, there are also substantial benefits for group living, involving increased PCBP and a greatly reduced likelihood of nests without brood. As expected from these observations, we also found strongly female biased sex allocation. Nevertheless only a small percentage of nests contained more than one adult female, similar to the other two Brevineura species, raising the question of why multifemale colonies are not more common in this genus. Solving this puzzle will throw light on conditions that constrain sociality when group living apparently provides major advantages.     

FEMALE-BIASED SEX RATIOS IN A FACULTATIVELY SOCIAL BEE AND THEIR IMPLICATIONS FOR SOCIAL EVOLUTION

Montane populations of the Australian allodapine bee, Exoneura bicolor, are characterized by high levels of cooperative nesting and strongly female-biased sex ratios. A conspecific population from heathland shows much lower levels of cooperative nesting and lower levels of female bias. In both habitats, sex-ratio bias is greatest in the smallest brood sizes and becomes successively less biased in larger broods. Parity is approached in the largest heathland colonies, but not for any brood-size category in montane areas. Adult intracolony relatedness is moderately high for colonies in both reused and newly founded nests in the montane habitat, but probably low or zero for newly founded nests in heathland. Colony efficiency, measured as the number of brood per adult, increases with colony size in both habitats, suggesting that cooperation between females increases mean female fitness. It is argued that patterns of sex allocation are consistent with nonlinear fitness-return models, in which the mean reproductive value of daughters increases with the number of daughters produced in a brood. Such increases probably arise from a number of social interactions, including cooperative brood defense, increased task efficiency, and lower per capita costs in nest construction. The term “local fitness enhancement” is introduced here to describe these effects collectively. The female-biased ratios should lower selective thresholds for sib-directed altruism, at least in the earlier stages of colony development. It is argued that local fitness enhancement facilitates eusociality in allodapine bees and could also play a role in other haplodiploid taxa, provided cooperative nesting largely involves sisters, colony efficiency increases with colony size, and optimal colony sizes are only achieved after two or more generations after founding.     

Sociality and sex allocation in an Australian allodapine bee Braunsapis protuberans

Abstract  Herein the first detailed study of sociality and life history in an Australian species of the allodapine bee genus Braunsapis is provided. Colonies of B. protuberans were sampled from the Great Sandy National Park in Queensland from late winter until later summer. Single-female colonies appear to have suffered substantially higher rates of total brood loss, or failure to produce brood, than multifemale colonies, but rearing efficiency in colonies with at least some brood did not differ between these two colony types. There was marked reproductive skew in multifemale colonies and ovary size was strongly linked to relative body size. However, females with smaller body size and smaller ovaries also had lower levels of wing wear, suggesting that they do not specialise in foraging. These patterns are similar to an African species, Braunsapis vitrea , and suggest that colonies may principally comprise a dominant reproductive female who provides food for her juvenile offspring, along with a variable number of subordinate females who may be waiting to inherit their natal nest in the event of their mother's death. However, it is likely that in such events, the remaining female(s) will care for orphaned brood as some single-female colonies contained substantial older brood, even though the sole female had little or no wing wear. Such alloparental care in the case of orphaning may help explain the high level of female bias in sex ratios.     

Social flexibility in a primitively social allodapine bee (Hymenoptera: Apidae): results of a translocation experiment

Many species of social animals are known to exhibit intraspecific variation in social traits between different populations. In the social insects, geographically separate populations may show wide-ranging forms of social behaviour, presumably because of variation in environmental parameters such as climate. For example, several bee species are known to exhibit eusocial or solitary behaviour depending on the latitude or altitude of the population. However, there is little or no empirical evidence to determine if this variation is a result of behavioural plasticity or long-term adaptation to local conditions, both of which have implications for the evolution of sociality. In this study, colonies of the allodapine bees Exoneura robusta and E. nigrescens were translocated between a montane and heathland habitat in southern Australia to assess the effect of habitat change on social behaviour. Results indicate that brood development in translocated colonies of both species differed from control colonies, leading to opportunities for different forms of social behaviour. However, there was also a high degree of variation within each habitat, suggesting an influence of both within and between habitat factors.     

Changing colony growth rates inCamponotus floridanus as a behavioral response to conspecific presence (Hymenoptera: Formicidae)

Previous work with the antCamponotus floridanus demonstrated that perception of competition can be clearly differentiated from effects of mortality and decreased resources. That is, brood biomass in ant colonies decreases as a consequence of a behavioral decision(s) rather than because of limited food availability or reduced numbers of brood tenders. The experiments presented here extend that work. Under experimental conditions, colony growth inC. floridanus is modified by distance between brood and unrelated conspecifics and by worker age distribution. When nonnestmates are encountered at the nest versus at a separate foraging site, less brood is maintained by a colony. Although colonies with older workers maintain a brood biomass similar to that of colonies with younger workers, that biomass is concentrated in fewer, larger, more rapidly maturing larvae. These effects seem to be due entirely to worker control.     

Number of reproductive cycles of Varroa jacobsoni in honey-bee (Apis mellifera) colonies

Very little data exists concerning the number of reproductive cycles performed by individual Varroa mites. To understand the population dynamics of the Varroa mite it is necessary to know the number of fertile female offspring each Varroa female produces during her lifetime. The lifetime reproduction capacity of the mite consists of the mean number of fertile female offspring produced during each reproductive cycle multiplied by the mean number of cell passages. This paper describes an experimental design to estimate the number of reproductive cycles where mites are transferred to new mite-free colonies for reproduction in sealed brood cells. The data presented suggests that the mean number of reproductive cycles performed by the individual female mite is larger than previously accepted. Under optimal conditions, the mean number of reproductive cycles by Varroa females is probably greater than 1.5 but less than 2. Furthermore, the results show that the reproductive success of Varroa females going into cells to reproduce is not influenced by previous brood cycles.     

Diploid males in the bumble beeBombus terrestris

The frequency of colonies that produce diploid males after brother-sister (50%) and nephew-niece (37.5%) matings proves that inB. terrestris the sex is determined by a single multi-allelic sex locus. The diploid males which develop normally into adults make up 50% of the diploid brood. In the laboratory the growth rate of colonies with diploid males is influenced only slightly. Of 41 colony founding queens caught out of a natural population, all produced a colony without any diploid males. Therefore, the number of sex alleles in this population is estimated to be at least 24. This means that in commercial rearing systems for bumble bees, involving several generations, the occurrence of diploid males can largely be prevented by a good scheme for crossings.     

An experimental analysis of pleometrotic advantage in the desert seed-harvester antMessor pergandei (Hymenoptera; Formicidae)

Summary Starting colonies of the desert seed-harvester antMessor pergandei are clumped in the field and face severe intraspecific competition through brood raiding. Single foundress laboratory colonies ofM. pergandei are more likely to succeed at brood raiding with conspecific colonies if they are given additional workers and mature pupae several days prior to brood raiding. Per foundress fecundity remains constant across laboratory starting colonies established with 1, 3 and 5 foundresses. These results suggest that the selective advantage of cooperative colony foundation (pleometrosis) in this and similar species may derive directly from the ability of multiple foundresses to produce a larger brood raiding force.     

Fine‐scale genetic structure reflects sex‐specific dispersal strategies in a population of sociable weavers (Philetairus socius)

Dispersal is a critical driver of gene flow, with important consequences for population genetic structure, social interactions and other biological processes. Limited dispersal may result in kin‐structured populations in which kin selection may operate, but it may also increase the risk of kin competition and inbreeding. Here, we use a combination of long‐term field data and molecular genetics to examine dispersal patterns and their consequences for the population genetics of a highly social bird, the sociable weaver (Philetairus socius), which exhibits cooperation at various levels of sociality from nuclear family groups to its unique communal nests. Using 20 years of data, involving capture of 6508 birds and 3151 recaptures at 48 colonies, we found that both sexes exhibit philopatry and that any dispersal occurs over relatively short distances. Dispersal is female‐biased, with females dispersing earlier, further, and to less closely related destination colonies than males. Genotyping data from 30 colonies showed that this pattern of dispersal is reflected by fine‐scale genetic structure for both sexes, revealed by isolation by distance in terms of genetic relatedness and significant genetic variance among colonies. Both relationships were stronger among males than females. Crucially, significant relatedness extended beyond the level of the colony for both sexes. Such fine‐scale population genetic structure may have played an important role in the evolution of cooperative behaviour in this species, but it may also result in a significant inbreeding risk, against which female‐biased dispersal alone is unlikely to be an effective strategy.     

Social polymorphism in the Australian small carpenter bee, Ceratina (Neoceratina) australensis

The bee tribe Ceratinini provides important insights into the early stages of sociality. Many arthropods exhibit behaviours precursory to social life, including adult longevity, parental care, nest loyalty and mutual tolerance, yet the origins of social behaviour are few. Here we describe the biology of a facultatively social bee, Ceratina (Neoceratina) australensis, which exhibits all of the preadaptations for successful group living, yet presents ecological and behavioural characteristics that seemingly disfavour frequent colony formation. This species is socially polymorphic with both solitary and social nests collected in sympatry. Social colonies consist of two foundresses, one contributing both foraging and reproductive effort and the second which remains at the nest as a passive guard. Cooperative nesting provides no overt reproductive benefits over solitary nesting in this population, although brood survival tends to be greater in social colonies. Maternal longevity, subsociality and bivoltine nesting phenology in this species favour colony formation, while dispersal habits and offspring longevity may inhibit more frequent social nesting in this and other ceratinines.     

Genetic evidence for landscape effects on dispersal in the army ant Eciton burchellii

Inhibited dispersal, leading to reduced gene flow, threatens populations with inbreeding depression and local extinction. Fragmentation may be especially detrimental to social insects because inhibited gene flow has important consequences for cooperation and competition within and among colonies. Army ants have winged males and permanently wingless queens; these traits imply male‐biased dispersal. However, army ant colonies are obligately nomadic and have the potential to traverse landscapes. Eciton burchellii, the most regularly nomadic army ant, is a forest interior species: colony raiding activities are limited in the absence of forest cover. To examine whether nomadism and landscape (forest clearing and elevation) affect population genetic structure in a montane E. burchellii population, we reconstructed queen and male genotypes from 25 colonies at seven polymorphic microsatellite loci. Pairwise genetic distances among individuals were compared to pairwise geographical and resistance distances using regressions with permutations, partial Mantel tests and random forests analyses. Although there was no significant spatial genetic structure in queens or males in montane forest, dispersal may be male‐biased. We found significant isolation by landscape resistance for queens based on land cover (forest clearing), but not on elevation. Summed colony emigrations over the lifetime of the queen may contribute to gene flow in this species and forest clearing impedes these movements and subsequent gene dispersal. Further forest cover removal may increasingly inhibit Eciton burchellii colony dispersal. We recommend maintaining habitat connectivity in tropical forests to promote population persistence for this keystone species.     

Low relatedness and frequent queen turnover in the stenogastrine wasp <Emphasis Type="Italic">Eustenogaster fraterna</Emphasis> favor the life insurance over the haplodiploid hypothesis for the origin of eusociality

Summary The origin of sociality is best studied in taxa with rudimentary social development, like the stenogastrine wasp, Eustenogaster fraterna. Our study of colony structure and relatedness in this species found very small colonies aver-aging only 2.7 adult females, including a single mated, re-productive female. Microsatellite genotyping showed that adult females were related to each other but not generally as full sisters (r = 0.427 ± 0.131, 95% confidence interval). Microsatellite genotyping showed that sociality is not favored by the haplodiploid hypothesis, because relatedness of unmated females to female brood is low (r = 0.210 ± 0.171, 95% confidence interval), far lower than that among sisters in either haplodiploid or diploid species. Relatedness of unmated females to female brood is significantly lower than that of mated females to female brood (r = 0.374 ± 0.266). Mated females are also significantly more related to the male brood (r = 0.871 ± 0.168) than are unmated females (r = 0.588 ± 0.339), suggesting that unmated helpers do not generally produce sons. These results argue against an important role for exceptionally high relatedness in the origin of eusociality. One quarter of the brood could not have been the progeny of any collected female, suggesting high rates of queen turnover. In all, 7/17 nests had some brood that could not be assigned to existing adult females. These high adult mortality rates result in direct advantages to helpers in the form of colony inheritance, and indirect advantages via life insurance benefits.Received 23 October 2002; revised 13 March 2003; accepted 23 April 2003.     

Behavioural specialization in pre-reproductive colonies of the allodapine beeExoneura bicolor (Hymenoptera: Anthophoridae)

Summary Exoneura bicolor is a univoltine allodapine bee common in montane forests of southern Australia, where it exhibits a semisocial/quasisocial colony organization. Within-nest behaviour in postemergence autumn nests ofExoneura bicolor was recorded with the aim of studying behavioural specialization in pre-reproductive colonies. Ten complete colonies were transferred to purpose-built observation nests shortly before brood eclosion in late summer. Behaviour within observation nests was recorded for periods of up to 44 days after establishment, covering a period when colonies are preparing for overwintering. Dispersal of females and brood rearing do not occur at this time, although some females may become inseminated. Analyses of data using multivariate techniques indicated four distinguishable behavioural castes, designated here as Guards, Nest Absenters, Nest Modifiers and Non-recruits. This represents a higher degree of behavioural specialization than recorded to date for other allodapines. Behaviours performed by Guards and Nest Absenters are likely to involve considerable risks, but benefit the colony as a whole, so that some nestmates in prereproductive colonies exhibit altruism that frequently aids adult siblings or cousins. The males in our study were fed by females via trophallaxis and two of the males participated in nest maintenance tasks. Our results suggest that autumn colonies ofE. bicolor form well-integrated behavioural units even though brood rearing does not commence until the following spring.     

The biology of Brevineura froggatti and phylogenetic conservatism in Australian allodapine bees (Apidae,Allodapini)

Summary: We present the first data on the social biology of the allodapine bee, Brevineura froggatti. Colony sizes are small, and only 12.5% of nests contained more than two females. Brood rearing occurs throughout the year, including winter, as it does in the other species of Brevineura studied to date. In both Brevineura species, per capita brood production is much higher in multi-female nests than single female nests, raising the question of why more colonies aren't multifemale. The occurrence of small colony sizes, despite large benefits to group living, differs strongly from species of the sister clade Exoneura. These findings, combined with previous allodapine studies, indicate conservatism in voltinism, brood phenology and colony size within, but not between, Australian allodapine genera.     

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.     

Reproduction of Varroa destructor in worker brood of Africanized honey bees (Apis mellifera)

Reproduction and population growth of Varroa destructor was studied in ten naturally infested, Africanized honeybee (AHB) (Apis mellifera) colonies in Yucatan, Mexico. Between February 1997 and January 1998 monthly records of the amount of pollen, honey, sealed worker and drone brood were recorded. In addition, mite infestation levels of adult bees and worker brood and the fecundity of the mites reproducing in worker cells were determined. The mean number of sealed worker brood cells (10,070 ± 1,790) remained fairly constant over the experimental period in each colony. However, the presence and amount of sealed drone brood was very variable. One colony had drone brood for 10 months and another for only 1 month. Both the mean infestation level of worker brood (18.1 ± 8.4%) and adult bees (3.5 ± 1.3%) remained fairly constant over the study period and did not increase rapidly as is normally observed in European honey bees. In fact, the estimated mean number of mites fell from 3,500 in February 1997 to 2,380 in January 1998. In May 2000 the mean mite population in the study colonies was still only 1,821 mites. The fertility level of mites in this study was much higher (83–96%) than in AHB in Brazil(25–57%), and similar to that found in EHB (76–94%). Mite fertility remained high throughout the entire study and was not influenced by the amount of pollen, honey or worker brood in the colonies. This revised version was published online in July 2006 with corrections to the Cover Date.     

Population responses of Ulex shrubs to fire in a lowland heath community

Question: How does the frequency of heathland fire events affect population growth rates of two woody shrub species, Ulex gallii and U. minor? Location: Dry heathland on the south coast of England, UK. Methods: The population dynamics of U. gallii and U. minor were modelled at each phase of the heathland cycle — pioneer, building, mature and degenerate — using periodic matrix products to investigate the response to different fire regimes. Results: Population growth rates of both Ulex species declined under annual burning. Initially, as the time between burns increased, population growth rate increased for both species. Maximum population growth rates for each Ulex species were achieved under a 16‐yr fire return interval. Fire return intervals > 16 yr resulted in declining population growth rates. Conclusions: A species‐specific critical fire frequency can be predicted, the minimum fire return intervals permitting persistence were 4 yr for U. minor and 3 yr for U. gallii. These patterns are similar to those reported for a range of woody plant species within savanna environments.     

Social polymorphism in the sweat bee <Emphasis Type="Italic">Lasioglossum (Evylaeus) baleicum</Emphasis> (Cockerell) (Hymenoptera,Halictidae) in Hokkaido,northern Japan

Summary The life cycle and social behaviour of the sweat bee Lasioglossum (Evylaeus) baleicum (Cockerell) was investigated in two geographically separate populations in Hokkaido, northern Japan. Colonies were excavated throughout the brood rearing season from an aggregation in Nishioka forest park, Sapporo, and near Kawakita in eastern Hokkaido during 2000 and 2001. The Nishioka population produced two discrete broods during the year and was weakly eusocial; 57% of workers were mated and 28% exhibited some ovarian development, 12–16% of the first brood was male, and workers were on average 4.5% smaller than their respective queen. In contrast, the population at Kawakita was solitary, and produced a single brood per year with an unbiased sex ratio. In addition however, there were some solitary colonies in the Nishioka population and evidence of a partial second brood in some colonies at Kawakita, suggesting differences between the populations are not fixed and that this species is truly socially polymorphic. L. (E.) baleicum is a member of the fulvicorne species group, which includes other examples of social polymorphic species as well as solitary and eusocial species, though this is the only species of this group so far known to exhibit a solitary/non-delayed eusocial polymorphism. Recent studies suggest that social polymorphism has both genetic and environmental influences, raising questions as to the relative import of each.