Multifemale Colonies Research Articles

Ecological predictors of spider sociality in theAmericas

AbstractAimTo evaluate the relative importance of environmental factors relevant to specific hypotheses that have been proposed to explain the distribution of social and subsocialAnelosimusspiders in the American continent andEcuador. For social species, we test the seasonality and prey size hypotheses, which posit that species forming long‐lived multifemale colonies require aseasonal conditions and warm and productive environments in which large insects can develop. For subsocial species, we test the rain intensity and predation risk hypotheses, which posit that species whose colonies contain a single female and her offspring cannot occupy areas where strong rains cause frequent damage to their webs and where warm temperatures and high productivity promote greater predation.LocationAmerica,Ecuador.MethodsUsing generalized linear models, hierarchical variance partitioning,Maxent distribution modelling and phylogenetically controlled regressions, we analysed the relative importance of environmental variables that either directly or indirectly relate to these non‐exclusive hypotheses – temperature and precipitation seasonality (seasonality hypothesis), annual temperature and net primary productivity (insect size and predation hypotheses) and rain intensity (rain intensity hypothesis).ResultsTemperature seasonality, followed by annual temperature and rain intensity, were the most important predictors of the distribution of spider sociality across America, whereas temperature and rain intensity predominated in the largely aseasonalEcuador. In general, social species were associated with lower temperature seasonality, warmer temperatures and higher rain intensity than subsocial species.Main conclusionThe association of socialAnelosimuswith warm and wet areas in the tropics is consistent with both the seasonality and prey size hypotheses, i.e. both aseasonal conditions and warm temperatures, which allow large insects to develop, are needed for large social colonies to form. That subsocialAnelosimusdrop‐out from tropical areas with warm temperatures and high rain intensity is consistent with the hypotheses that high predation risk and disturbance by strong rains exclude subsocialAnelosimusfrom the lowland rain forest.

Reproductive consequences of male body mass and aggressiveness depend on females’ behavioral types

Relatively few investigations explicitly test for concordant versus conflicting selection pressures from intrasexual versus intersexual selection. Here, we examine the effects of male body mass and behavioral type (BT) on reproductive success in the spider Anelosimus studiosus, with emphasis placed on the potential interaction between intrasexual and intersexual selection influences. Female A. studiosus exhibit either an aggressive-active or docile-passive BT, both of which co-occur in multifemale colonies. Males, in contrast, exhibit a more continuous distribution of behavioral tendencies. We investigated the male traits favored by females in five trial types: one docile female, one aggressive female, four docile females, four aggressive females, and two docile and two aggressive females. Male reproductive success was estimated by the number eggs produced by females following staged mating trials. In previous work, it was established that large aggressive males are favored in male–male contests, an intrasexual effect. However, large aggressive males were not universally favored here. We failed to detect an effect of male body mass or aggressiveness on reproductive success in trials with all docile females; however, in situations involving aggressive females, large aggressive males experienced diminished reproductive success relative to small docile males. Large, aggressive males were also more likely to be attacked and killed by aggressive females in the first 20 min of staged encounters and were more likely to be found dead after 72 h of unobserved interactions. Taken together, our data suggest that the reproductive consequences of male traits differ based on (1) the aspect of sexual selection being considered (intrasexual versus intersexual) and (2) the BT of their prospective mates: large aggressive males enjoy advantages in intrasexual selection and when courting docile females and small docile males experience reduced risk of cannibalism and increased reproductive success with aggressive females.

Within-group behavioral variation promotes biased task performance and the emergence of a defensive caste in a social spider

The social spider Anelosimus studiosus exhibits a behavioral polymorphism where colony members express either a passive, tolerant behavioral tendency (social) or an aggressive, intolerant behavioral tendency (asocial). Here we test whether asocial individuals act as colony defenders by deflecting the suite of foreign (i.e., heterospecific) spider species that commonly exploit multi-female colonies. We (1) determined whether the phenotypic composition of colonies is associated with foreign spider abundance, (2) tested whether heterospecific spider abundance and diversity affect colony survival in the field, and (3) performed staged encounters between groups of A. studiosus and their colony-level predator Agelenopsis emertoni (A. emertoni)to determine whether asocial females exhibit more defensive behavior. We found that larger colonies harbor more foreign spiders, and the number of asocial colony members was negatively associated with foreign spider abundance. Additionally, colony persistence was negatively associated with the abundance and diversity of foreign spiders within colonies. In encounters with a colony-level predator, asocial females were more likely to exhibit escalatory behavior, and this might explain the negative association between the frequency of asocial females and the presence of foreign spider associates. Together, our results indicate that foreign spiders are detrimental to colony survival, and that asocial females play a defensive role in multi-female colonies.Electronic supplementary materialThe online version of this article (doi:10.1007/s00265-010-1112-z) contains supplementary material, which is available to authorized users.

Reproductive success in a socially polymorphic spider: social individuals experience depressed reproductive success in isolation

1. Correlated individual differences in behaviour across ecological contexts, or behavioural syndromes, can theoretically constrain individuals' ability to optimally adjust their behaviour for specific contexts. 2. Female Anelosimus studiosus exhibit a unique behavioural polymorphism: ‘social’ females are tolerant of conspecifics and aggregate in multi-female colonies, while ‘solitary’ females aggressively defend their singleton webs from intrusion by adult female conspecifics. Previous work found that social females are also less aggressive toward prey and are more fearful of predators. 3. In this study we quantify potential fitness consequences of these correlated behaviours by examining the potential and realised fecundities of the two phenotypes in naturally occurring colonies, and by quantifying their ability to rear offspring as singleton individuals. 4. There were no differences in the fecundities of laboratory-reared females between the phenotypes, nor were there differences in field-collected brooding females from naturally occurring solitary and social nests. 5. Brooding females from solitary and social colonies that were isolated in new nests for the growing season were both capable of rearing their broods; however, females from solitary nests had significantly greater success. 6. These results suggest a fitness consequence to the reduced-aggression syndrome of social females that may represent a general impediment to the evolution of sociality in spiders.

FREQUENCY-DEPENDENT SUCCESS OF CHEATERS DURING FORAGING BOUTS MIGHT LIMIT THEIR SPREAD WITHIN COLONIES OF A SOCIALLY POLYMORPHIC SPIDER

Although several studies have demonstrated that frequency-dependent effects can promote the maintenance of cooperative behavior in microbes, experimental evidence of frequency-dependent effects in cooperative animal societies is rare. We staged mixed phenotype feeding bouts in the spider Anelosimus studiosus, which shows a within-population social polymorphism, to determine how phenotype frequency affects the foraging success of the social (cooperative) and asocial (cheater) phenotypes. Foraging performance was inferred from average change in percent mass for the respective phenotypes after staged group foraging events. We then performed a field census of multifemale colonies of A. studiosus to determine the phenotypic composition of naturally occurring colonies. Our data indicate that asocial (i.e., cheater) individuals experience negative frequency-dependent foraging success in staged foraging contests. Asocial individuals outperform social individuals when their representation is low, but lose this competitive advantage as their relative numbers increase. Naturally occurring colonies, on average, contained 58.33% social and 41.67% asocial individuals.

Reproductive hierarchies in the African allodapine bee Allodapula dichroa (Apidae: Xylocopinae) and ancestral forms of sociality

The social organization of allodapine bees has been described in detail for most genera, although there remains a notable gap for one major lineage, the genus Allodapula. Here, we provide the first detailed study of social organization in Allodapula dichroa. Colony sizes are small and the frequency of cooperative nesting is low compared with other allodapine taxa, but there is very clear evidence for reproductive differentiation among adult nestmates. Reproductively dominant females tend to be larger than their nestmates and have much higher levels of wing wear, suggesting that they perform most foraging activities. Multi-female colonies have: (1) lower rates of complete brood absence, suggesting a substantial benefit to cooperative nesting; and (2) larger numbers of brood, suggesting that the presence of a second adult female leads to a greater reproductive output. These data suggest a major phylogenetic split in the form of social organization within the allodapines. In the genus Macrogalea (sister clade to all other allodapines), body size does not preclude young females from laying eggs, and there appears to be, at most, weak reproductive queues. However, in most other allodapines, reproductive hierarchies are prominent and younger and/or smaller females queue for reproductive opportunities, adopt permanently subordinate roles, or disperse. Interestingly, the most common forms of reproductive hierarchies in allodapines do not involve subordinates undertaking foraging roles before reproduction, but instead involve the delaying of both reproduction and foraging. This has implications for the understanding of suggested developmental ground plans in the early stages of social evolution.

Patterns of reproductive success associated with social structure and microclimate in a spider system

Species that vary in social structure within and among populations can provide unparalleled insight into the evolution of sociality. The theridiid spider Anelosimus studiosus varies widely in its social structure at the northern edge of its range. Colony sizes range from the solitary/territorial female with her offspring to cooperative colonies of tens to hundreds of adult females. In previous work, we developed an assured fitness returns ‘brood-fostering model’ that predicts that in cooler environments mothers in multiple-female colonies will have a selective advantage over solitary female nests. According to the model, at cool sites the rate of juvenile maturation is slowed, increasing the probability that the mother will die before the brood reaches independence. In her absence, other females would foster her brood. We tested this hypothesis by manipulating colony size and by monitoring the reproductive success of naturally occurring solitary and multifemale colonies in cold and warm temperature environments. Our results indicate that while multiple-female colonies have higher fitness at cool sites, the solitary female nests achieve higher fitness at warmer sites. The higher reproductive success of multifemale colonies at cold sites further reflects the total failure of solitary female nests at these sites. Solitary female nests that survived generally had higher reproductive success than multifemale colonies at all temperatures. In natural colonies, fitness was highest for smaller multifemale colonies in the colder environments and decreased in the larger colonies. We use these data to refine the brood-fostering model and discuss the results with regard to the observed polymorphism in social structure.

Sociality in the phylogenetically basal allodapine bee genus Macrogalea (Apidae: Xylocopinae): implications for social evolution in the tribe Allodapini

Recent phylogenetic studies based on DNA sequence data indicate that the tropical African bee genus Macrogalea is the sister group to the remaining extant allodapine fauna, whereas previously it was thought to be a distal group. This leads to some fundamental changes in our understanding of social evolution in the allodapines. Earlier studies suggested that Macrogalea showed only weak forms of social behaviour and these were not well characterized. However, large samples of Macrogalea zanzibarica presented here show that this species exhibits marked social behaviour. Nearly half of nests collected contained two or more adult females, with up to 10 females per nest. Brood are reared progressively and brood ages within colonies are staggered, giving rise to colonies with very mixed age structures and therefore frequent opportunities for alloparental care. Ovarian dissections indicate non-simple forms of reproductive partitioning within colonies and most multi-female colonies show evidence that more than one female has contributed to egg production, though reproductive episodes among colony members are frequently asynchronous. Some females show signs of much higher wing wear than their nestmates, but always show signs of previous reproduction. Reproductive division of labour appears to be temporally marked, ovarian differentiation among nestmates is linked to relative body size, but permanent worker-like or queen-like castes appear to be absent. This is similar to the communal, continuously brooded and multivoltine behaviour of some tropical halictine species and may be due to the aseasonal nature of brood development in tropical regions. Patterns of per capita brood production indicate large benefits to multi-female nest occupancy, and sex allocation is strongly female biased. These findings strongly suggest that the capacity for complex social interactions and alloparental care is an ancestral trait for all of the extant allodapine lineages. Therefore comparisons among extant allodapines are unlikely to throw light on the initial origin of social behaviour, though they may uncover origins of true caste behaviour and reversals to solitary nesting. Sex ratios in Macrogalea and most other allodapine genera, spanning a broad phylogenetic and ecological range, suggest that one or more allodapine traits have provided persistent selection for female-biased sex allocation.

Sociality and sex allocation in an Australian allodapine bee Braunsapis protuberans

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.

COOPERATIVE NESTING AND OVARIAN DEVELOPMENT IN FEMALES OF THE PREDOMINANTLY SOCIAL BEE EXONEURA BICOLOR SMITH (HYMENOPTERA: ANTHOPHORIDAE) AFTER FORCED SOLITARY ECLOSION

Cooperative nesting is frequent in montane populations of the Australian allodapine bee Exoneura bicolor. In natural populations, multifemale colonies primarily arise from cooperative re-use of natal nests or by the cofounding of new nests by groups of female relatives. In this study we examine ovarian enlargement of females that are artificially placed in solitary nests prior to adult eclosion. After eclosion, females were allowed to move around freely prior to overwintering. Of the females recovered at the end of our experiment, 74% had joined to form either 2 or 3-female colonies. We found no evidence of ovarian inhibition between colony members. However, inseminated females showed significantly greater ovarian development than their uninseminated nestmates. These results indicate that the benefits of cooperative nesting arc great, even when nestmates are unrelated. This may have consequences for kin selection models of altruism in Australian allodapine bees.

Nesting biology of an African allodapine bee Braunsapis vitrea: female biased sex allocation in the absence of worker-like behavioural castes

The life cycle and social behaviour of an African allodapine bee, Braunsapis vitrea, was examined using nest contents data from thorn-nests in Acacia karroo in Limpopo Province, South Africa. The majority of B. vitrea colonies were subsocial, with 34% of nests collected containing more than one adult female. Although brood numbers increased with colony size, per capita brood numbers did not increase. Within multifemale colonies, reproductively active females had greater wing wear than their nestmates, which tended to be uninseminated, and there was no relationship between relative ovary and body size. This suggests that females who were not reproductively active were not workers in the nest, but were instead waiting to either disperse or inherit the nest. There is evidence that these younger females may help rear their mother's brood in the event of orphaning, and the number of brood in multifemale nests was greater than for single–female nests, suggesting that egg layers increase brood production when a potential alloparent is present. Sex allocation was strongly female biased, with a numerical population ratio of r ≈ 0.3. This bias is interesting because our results suggest that it occurs in the absence of behavioural castes, where most colonies are occupied by single females, and where capita brood production does not increase with colony size. We argue that such bias might be selected by the benefits of having potentially alloparental ‘insurance’ daughters, who can help rear their younger siblings in the case of orphaning.

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.

Nesting and life cycle of the Australian green carpenter bees Xylocopa (Lestis) aeratus Smith and Xylocopa (Lestis) bombylans (Fabricius) (Hymenoptera: Apidae: Xylocopinae)

AbstractThis paper expands on previous observations of Australian green carpenter bees by providing information about nesting substrates and the life cycle of Xylocopa (Lestis) aeratus and Xylocopa (Lestis) bombylans from more than 450 colonies from South Australia and New South Wales. Voltinism differs between the two species, but does not appear to vary within species from different locations, such as X. aeratus colonies on Kangaroo Island, South Australia and at Woy Woy, New South Wales. The architecture of nests (unbranched or branched) is related to the substrate diameter and may allow variation in social behaviour because different provisioning strategies can be used in the two nest types. Both species have some multifemale colonies for most of the year and this includes the brood‐rearing period. Differences in voltinism, nest type and the occurrence of multifemale colonies during brood production are likely to lead to variation in social organisation within and between species.

Cooperative breeding, offspring packaging, and biased sex ratios in allodapine bees

It is not generally appreciated that positive kin interactions do not necessarily result in an evolutionarily stable (ES) skewed sex ratio. Stability depends critically on the sex of both the helper and receiver. When help is given within one sex only, no monomorphic ES strategy exists, and local resource enhancement (LRE) between offspring of one sex does not predict a sex ratio bias toward that sex. I developed a model to clarify and examine the sex ratio biases that may be expected under cooperative breeding. I found that LRE between cooperatively breeding female allodapine bees cannot explain their female-biased sex ratios. Allodapine females feed and protect brothers, which may stabilize the female-biased sex ratio, but the model shows this is not the case because benevolence to males is likely to decrease rapidly as the number of females increases. For small broods this helping behavior causes a female bias, but bigger broods could be sufficiently male biased to compensate the population sex ratio. Considering the fact that females need to be packaged into reproductive units (multifemale colonies), of which intermediate-sized units are the most productive, it is shown that fitness returns from females are in fact a wavelike function. This results in a rugged fitness landscape, which could explain the female-biased population sex ratios of allodapine bees as an adaptation to local fitness peaks rather than a global optimum. In behaviors where organisms have to package limited resources into integer numbers of units, the possible solutions are limited, and careful analysis is required.

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.

Life cycle and social behavior in a heathland population of the allodapine bee,Exoneura bicolor (Hymenoptera: Apidae)

Previous studies of the allodapine beeExoneura bicolor have utilised a predominantly social population from tall montane forests. In this report we examine aspects of the sociality and biology of a population from subcoastal heathland in western Victoria, Australia. Entire colonies, nesting inXanthorrhoea minor, were collected at monthly intervals over 12 months between February 1989 and January 1990. In addition, three collections fromMelaleuca squarrosa were made over three consecutive winter months. The heathland population differs from the montane population in several aspects associated with sociality: (i) it shows lower levels of co-occupancy in both newly founded and re-used nests; (ii) foundress dispersal occurs over a larger proportion of the year; and (iii) there may be a partical second brood produced in late summer, during and after adult eclosion of the first brood. The occurrence of a partial second brood gives rise to opportunities for sib-rearing and eusociality. Colony sizes tend to be larger inM. squarrosa thanX. minor, but still smaller than colonies from the montane population. Egg-laying commences several weeks earlier in multifemale colonies than in single female colonies, before spring dispersal begins. It appears that multifemale colonies are more successful at preventing brood loss than single females and that the mean number of brood per female is larger in multifemale colonies than in single female colonies. These two populations, which display differences in several life history traits, provide an ideal system for studying the mechanisms maintaining social behavior.

The effect of the number of queens of the antLasius flavus (Fab.) (Hym., Formicidae) on their survival and on the rate of development of the first brood

Populous colonies ofLasius flavus F. are generally haplometrotic, yet not infrequently several queens combine in founding nests. This aggregation after flight is not always accidental, but may arise from cooperation between the females in the digging of new burrows. Probably the queens become habituated to one another at this stage. In the laboratory the multi-female colonies were at an advantage over the single female ones, as the mortality of the queens was reduced and the first brood of workers was reared more rapidly. Grouping of the queens ofL. flavus and of those ofL. niger did not appear to influence the ovarial development of the survivors, and they all contributed to the establishment and the rearing of the first brood. This pleometrosis was temporary and the multi-queen colonies began to split into smaller units at the time of the appearance of the earliest pupae. InL. niger, fighting to death between the queens, at times of repeated ovipositions, also contributed towards the final state of haplometrosis.