A shift in colony founding behaviour in the obligate plant-ant Crematogaster (Decacrema) morphospecies 2

Summary. A shift in colony founding behaviour from single queen (haplometrosis) to multiple queens (pleometrosis) was observed locally in the obligate plant-ant Crematogaster (Decacrema) morphospecies 2, which is associated with Macaranga trees in Borneo. In addition, about a quarter of all mature colonies (27 of 95 trees examined) were found to be multiple queen colonies. They arose either directly from pleometrotic founding colonies or secondarily by adoption of additional queens. Using microsatellite markers, we showed that queens in colonies founded through pleometrosis are unrelated and each queen participates in producing worker offspring, albeit with significant skew in a third of the colonies. In mature polygynous colonies, all resident queens contributed to the production of workers and sexual offspring. Relatedness of queens in mature polygynous colonies was not significantly higher than in foundress associations. We hypothesize that increased nest site limitation in this specific interaction trigger the observed shift in colony founding behaviour. Crematogaster msp. 2 inhabits the light demanding pioneer plant species Macaranga pearsonii that is typical for early successional stages of secondary forests. Thus suitable host-plants for colonisation are abundant for only a short time in highly disturbed sites and become increasingly sparse when secondary forest matures.Received 6 September 2004; revised 29 November; accepted 10 December 2004.     

Variation in social structure alters queen body mass and productivity in the desert seed-harvester ant Messor pergandei

Parent–offspring conflict theory predicts conflict between parents and their offspring over per-offspring resource investment. Across the range of the desert seed-harvester ant, Messor pergandei, daughter queens use three different social strategies during colony founding that are expected to alter the optimal level of parental investment. To test whether social strategy variation is associated with shifts in body mass, we surveyed queen live mass over 3 years at 25 sites that spanned the range of behavioral strategies and founding group sizes. To test whether reduction in parental investment into individual offspring negatively impacts their productivity, queens were individually isolated and allowed to produce a single worker cohort under common garden conditions. Queen live mass was highly variable, from 24 mg on average at the site with the lightest queens to 1.5 times that size, 37 mg, at the site with the heaviest queens. As predicted by parent–offspring conflict over investment, solitary colony founding sites contained the heaviest queens, followed by secondary monogyny. Polygynous queens were lightest, with a strong negative relationship between group size and live mass. Reductions in body mass had a negative effect on queen productivity across all queen social types; however, queens from sites where queen–queen aggression is typical were significantly more efficient at brood rearing, resulting in lower mass loss during founding per unit offspring biomass. This may represent an adaptation to queen competition to gain a strength advantage over potential rivals.     

Sociogenomics of Cooperation and Conflict during Colony Founding in the Fire Ant Solenopsis invicta

One of the fundamental questions in biology is how cooperative and altruistic behaviors evolved. The majority of studies seeking to identify the genes regulating these behaviors have been performed in systems where behavioral and physiological differences are relatively fixed, such as in the honey bee. During colony founding in the monogyne (one queen per colony) social form of the fire ant Solenopsis invicta, newly-mated queens may start new colonies either individually (haplometrosis) or in groups (pleometrosis). However, only one queen (the “winner”) in pleometrotic associations survives and takes the lead of the young colony while the others (the “losers”) are executed. Thus, colony founding in fire ants provides an excellent system in which to examine the genes underpinning cooperative behavior and how the social environment shapes the expression of these genes. We developed a new whole genome microarray platform for S. invicta to characterize the gene expression patterns associated with colony founding behavior. First, we compared haplometrotic queens, pleometrotic winners and pleometrotic losers. Second, we manipulated pleometrotic couples in order to switch or maintain the social ranks of the two cofoundresses. Haplometrotic and pleometrotic queens differed in the expression of genes involved in stress response, aging, immunity, reproduction and lipid biosynthesis. Smaller sets of genes were differentially expressed between winners and losers. In the second experiment, switching social rank had a much greater impact on gene expression patterns than the initial/final rank. Expression differences for several candidate genes involved in key biological processes were confirmed using qRT-PCR. Our findings indicate that, in S. invicta, social environment plays a major role in the determination of the patterns of gene expression, while the queen''s physiological state is secondary. These results highlight the powerful influence of social environment on regulation of the genomic state, physiology and ultimately, social behavior of animals.     

Development rate and brood production in haplo- and pleometrotic colonies of <Emphasis Type="Italic">Oecophylla smaragdina</Emphasis>

Pleometrosis (colony founding by multiple queens) may improve life history characteristics that are important for early colony survival. When queens unite their initial brood, the number of workers present when incipient colonies open may be higher than for single queen colonies. Further, the time until the first worker emerges may shorten. For territorial species and species that rob brood from neighbouring colonies, a faster production of more workers may improve the chance of surviving intraspecific competition. In this study, the time from the nuptial flight to the emergence of the first worker in incipient Oecophylla smaragdina Fabr. colonies founded by 1–5 queens was compared and the production of brood during the first 68 days after the nuptial flight was assessed. Compared to haplometrotic colonies, pleometrotic colonies produced 3.2 times more workers, their first worker emerged on average 4.3 days (8%) earlier and the queen’s per capita egg production almost doubled. Further, colony production was positively, correlated with the number of founding queens and time to worker emergence was negatively correlated. These results indicate that pleometrotic O. smaragdina colo-nies are competitively superior to haplometrotic colonies as they produce more workers faster and shorten the claustral phase, leading to increased queen fecundity.     

Fitness and the level of homozygosity in a social insect

To date very few studies have addressed the effects of inbreeding in social Hymenoptera, perhaps because the costs of inbreeding are generally considered marginal owing to male haploidy whereby recessive deleterious alleles are strongly exposed to selection in males. Here, we present one of the first studies on the effects of queen and worker homozygosity on colony performance. In a wild population of the ant Formica exsecta, the relative investment of single‐queen colonies in sexual production decreased with increased worker homozygosity. This may either stem from increased homozygosity decreasing the likelihood of diploid brood to develop into queens or a lower efficiency of more homozygous workers at feeding larvae and thus a lower proportion of the female brood developing into queens. There was also a significant negative association between colony age and the level of queen but not worker homozygosity. This association may stem from inbreeding affecting queen lifespan and/or their fecundity, and thus colony survival. However, there was no association between queen homozygosity and colony size, suggesting that inbreeding affects colony survival as a result of inbred queens having a shorter lifespan rather than a lower fecundity. Finally, there was no significant association between either worker or queen homozygosity and the probability of successful colony founding, colony size and colony productivity, the three other traits studied. Overall, these results indicate that inbreeding depression may have important effects on colony fitness by affecting both the parental (queen) and offspring (worker) generations cohabiting within an ant colony.     

Biological constraints and colony founding in the polygynous invasive ant Lasius neglectus (Hymenoptera, Formicidae)

Summary. The polygynous invasive ant Lasius neglectus was described from Budapest, Hungary, as an unicolonial species, with no apparent colony barriers, and inferred intra-nidal mating without a nuptial flight. Here we analyze additional morphological characteristics of gynes, their physiological condition at emergence and at the time of mating and we describe the productivity of different types of colony founding in the laboratory. A low increase in dry weight and in fat content from emergence to mating indicates that gynes can only succeed in dependent colony founding. However, the queen-worker thorax volume ratio is typical of a species with independent colony founding and we were able to demonstrate independent colony founding in the laboratory (both haplo- and pleometrotic). Brood development in independent founding is rapid and the number of nanitics higher than in other Lasius species. Both colony budding and dependent colony founding could also be demonstrated in the laboratory. Worker oviposition was absent. The carbohydrate content of newly mated queens is consistent with the observed loss of mating flight of this species. However the relative wing area clearly indicates that L. neglectus queens should be able to fly. Therefore, both queen morphology and physiological state at maturity show that L. neglectus is intermediate between a monogynous, free-living, non pest ant and a multiqueened (polygynic) invasive tramp ant. This neglected ant thus offers interesting opportunities to study the origin of unicoloniality and the spread of this species in northeast Spain.     

Queen size mediates queen survival and colony fitness in harvester ants

Abstract We examined the effect of queen size on the probability of new colony establishment in the ant Pogonomyrmex occidentalis. Large queens are significantly more likely to survive than small queens through the initial stages of colony founding. These differences in individual fitness correlates have corresponding effects on colony fitness. In species in which individual queens vary in fitness, sexual allocation ratios should incorporate the individual fitness functions.     

Desiccation limits recruitment in the pleometrotic desert seed‐harvester ant Veromessor pergandei

The desert harvester ant Veromessor pergandei displays geographic variation in colony founding with queens initiating nests singly (haplometrosis) or in groups (pleometrosis). The transition from haplo‐ to pleometrotic founding is associated with lower rainfall. Numerous hypotheses have been proposed to explain the evolution of cooperative founding in this species, but the ultimate explanation remains unanswered. In laboratory experiments, water level was positively associated with survival, condition, and brood production by single queens. Queen survival also was positively influenced by water level and queen number in a two‐factor experiment. Water level also was a significant effect for three measures of queen condition, but queen number was not significant for any measure. Foundress queens excavated after two weeks of desiccating conditions were dehydrated compared to alate queens captured from their natal colony, indicating that desiccation can be a source of queen mortality. Long‐term monitoring in central Arizona, USA, documented that recruitment only occurred in four of 20 years. A discriminant analysis using rainfall as a predictor of recruitment correctly predicted recruitment in 17 of 20 years for total rainfall from January to June (the period for mating flights and establishment) and in 19 of 20 years for early plus late rainfall (January–March and April–June, respectively), often with a posterior probability > 0.90. Moreover, recruitment occurred only in years in which both early and late rainfall exceeded the long‐term mean. This result also was supported by the discriminant analysis predicting no recruitment when long‐term mean early and late rainfall were included as ungrouped periods. These data suggest that pleometrosis in V. pergandei evolved to enhance colony survival in areas with harsh abiotic (desiccating) conditions, facilitating colonization of habitats in which solitary queens could not establish even in wet years. This favorable‐year hypothesis supports enhanced worker production as the primary advantage of pleometrosis.     

Energetics of newly-mated queens and colony founding in the fungus-gardening ants Cyphomyrmex rimosus and Trachymyrmex septentrionalis (Hymenoptera: Formicidae)

Abstract.  The energetics of colony founding is investigated in the fungus gardening ants (Attini) Trachymyrmex septentrionalis and Cyphomyrmex rimosus . Similar to most ants, inseminated queens of these two species found nests independently unaccompanied by workers (haplometrosis). Whereas most ant founding queens seal themselves in a chamber and do not feed when producing a brood entirely from metabolic stores (claustral founding), the majority of fungus gardening ants must forage during the founding phase (semiclaustral founding). Laboratory-reared T. septentrionalis individuals comprise 84 dealate females collected after mating flights in June 2004. Twenty are immediately killed to obtain values for queen traits and another 20 after worker emergence for queen, fungus garden and worker traits. Cyphomyrmex rimosus comprise 22 dealate females collected in June 2005; ten of which are immediately killed and similarly prepared. Newly-mated T. septentrionalis queens have 25% of their dry weight as fat; whereas newly-mated C. rimosus queens contain 11% fat. These amounts are 50–75% less than most independently founding ant species. Trachymyrmex septentrionalis queens lose merely 5% of their energetic content during colony founding, whereas the total energetic content of their brood is more than three-fold the amount lost by the queen. Incipient T. septentrionalis colonies produce approximately half as much ant biomass per gram of fungus garden as do mature colonies. Similar to most ants, T. septentrionalis produces minim workers that are approximately 40% lighter than workers from mature colonies. Regardless of their size, T. septentrionalis workers contain much lower fat than do workers of claustral species. These data indicate that fungus gardening is adaptive because colonies can produce much cheaper offspring, making colony investment much lower.     

The influence of intraspecific competition on resource allocation during dependent colony foundation in a social insect

Organisms face a trade-off between investment in fewer, larger offspring, or more, smaller offspring. Most organisms can adjust investment through variation in the size and number of offspring in response to factors such as resource availability and competition. In some social animals, established colonies divide into groups of individuals that become autonomous, a process known as colony fission (also dependent colony foundation in social insects). Resource allocation under fission can be fine-tuned by adjusting the number of new groups (offspring number) and the number of individuals in each new group (offspring size). We assessed the influence of competition on resource allocation during fission in the ant Cataglyphis cursor, by allowing colonies to fission in experimental enclosures of high or low conspecific colony density. The pattern of colony fission was similar to that observed in the field: each fissioning colony produced a few new nests comprising a highly variable number of workers and a single queen, the old queen was often replaced, and new queens were produced in excess. The number of new nests produced depended on the available workforce in the parent colony but was not affected by differences in colony density. Comparison with data from fission under natural field conditions, however, indicates that colonies in enclosures produced fewer, larger new nests, suggesting that resource investment patterns during fission are indeed subject to extrinsic factors. The density of conspecific colonies in the immediate surroundings may be an unreliable estimate of competition intensity and other factors should be considered.     

Sex allocation conflict between queens and workers in Formica pratensis wood ants predicts seasonal sex ratio variation

Sex allocation theory predicts parents should adjust their investment in male and female offspring in a way that increases parental fitness. This has been shown in several species and selective contexts. Yet, seasonal sex ratio variation within species and its underlying causes are poorly understood. Here, we study sex allocation variation in the wood ant Formica pratensis. This species displays conflict over colony sex ratio as workers and queens prefer different investment in male and female offspring, owing to haplodiploidy and relatedness asymmetries. It is unique among Formica ants because it produces two separate sexual offspring cohorts per season. We predict sex ratios to be closer to queen optimum in the early cohort but more female‐biased and closer to worker optimum in the later one. This is because the power of workers to manipulate colony sex ratio varies seasonally with the availability of diploid eggs. Consistently, more female‐biased sex ratios in the later offspring cohort over a three‐year sampling period from 93 colonies clearly support our prediction. The resulting seasonal alternation of sex ratios between queen and worker optima is a novel demonstration how understanding constraints of sex ratio adjustment increases our ability to predict sex ratio variation.     

Cooperative foundation of colonies by unrelated foundresses in the antPolyrhachis moesta

Summary Field studies ofPolyrhachis moesta revealed that colonies were facultatively founded by more than one queen, even though each established colony was inhabited by only one queen with her workers. In pleometrotic colonies, it was found that cofoundresses frequently exhibited cooperative behaviors, including trophallaxis. The results of DNA fingerprinting showed that multiple foundresses were not genetically to one another. It seems that they aggregate randomly and independently of their relatedness. A discussion of the reasons why foundresses ofP. moesta do not aggregate preferentially with genetically related females.     

Fitness in invasive social wasps: the role of variation in viral load,immune response and paternity in predicting nest size and reproductive output

Within any one habitat, the relative fitness of organisms in a population can vary substantially. Social insects like the common wasp are among the most successful invasive animals, but show enormous variation in nest size and other fitness‐related traits. Some of this variation may be caused by pathogens such as viruses that can have serious consequences in social insects, which range from reduced productivity to colony death. Both individual immune responses and colony‐level traits such as genetic diversity are likely to influence effects of pathogen infections on colony fitness. Here we investigate how infections with Kashmir Bee Virus (KBV), immune response and intracolony genetic diversity (due to queen polyandry) affect nest size in the invasive common wasp Vespula vulgaris. We show that KBV is highly prevalent in wasps and expression of antiviral immune genes is significantly increased with higher viral loads across individuals. Patriline membership within a nest did not influence KBV susceptibility or immune response. A permutational MANCOVA revealed that polyandry, viral load and expression of the immune gene Dicer were significant predictors of variation in nest size. High intracolony genetic diversity due to polyandry has previously been hypothesized to improve colony‐level resistance to parasites and pathogens. Consistent with this hypothesis, we observed genetically diverse colonies to be significantly larger and to produce more queens, although this effect was not driven by the pathogen we investigated. Invasive wasps clearly suffer from pathogens and expend resources, as indicated here by elevated immune gene expression, toward reducing pathogen‐impact on colony fitness.     

Colony size and individual fitness in the social spider Anelosimus eximius

ABSTRACT The effects of colony size on individual fitness and its components were investigated in artificially established and natural colonies of the social spider Anelosimus eximius (Araneae: Theridiidae). In the tropical rain forest understory at a site in eastern Ecuador, females in colonies containing between 23-107 females had india significantly higher lifetime reproductive success than females in smaller colonies. Among larger colonies, this trend apparently reversed. This overall fitness function was a result of the conflicting effects of colony size on different components of fitness. In particular, the probability of offspring survival to maturity increased with colony size while the probability of a female reproducing within the colonies decreased with colony size. Average clutch size increased with colony size when few or no wasp parasitoids were present in the egg sacs. With a high incidence of egg sac parasitoids, this effect disappeared because larger colonies were more likely to be infected. The product of the three fitness components measured-probability of female reproduction, average clutch size, and offspring survival-produced a function that is consistent with direct estimates of the average female lifetime reproductive success obtained by dividing the total number of offspring maturing in a colony by the number of females in the parental generation. Selection, therefore, should favor group living and itermediate colony sizes in this social spider.     

Genetic variance of mating frequency in the honeybee (Apis mellifera L.)

Summary. The genetic variance of queen mating frequency was studied in honeybees (Apis mellifera carnica). Worker offspring (N = 966) of 28 naturally mated half sister-queens (r = 0.25) from seven unrelated breeding lines were genotyped at four DNA microsatellites. The mating frequencies of the queens were derived from the offspring genotypes. The number of observed matings per queen ranged from 10 to 28 with an average of 17.32 ± 1.10 (number of estimated matings: 24.94 ± 2.51; number of effective matings: 20.09 ± 1.73). Half-sib analyses of the breeding lines were used to estimate heritability. Heritability was h² = 0.449 ± 0.135 for the estimated number of matings and h² = 0.262 ± 0.103 for the number of effective males, which are both significantly different from zero. We conclude that a high genetic variance for polyandry in honeybees can be favored by balanced selection between individual queen and colony level.Received 16 October 2003; revised 4 May 2004; accepted 4 May 2004.     

Independent colony founding by ergatoid queens in the ant genus Pogonomyrmex: queen foraging provides an alternative to dependent colony founding

Ant queens exhibit two primary strategies to initiate nests, independent colony founding (ICF) by solitary queens and dependent colony founding (DCF) when the queen starts a nest with a group of workers that disperse on foot from the parent nest. Numerous ant species have wingless (ergatoid) queens, and it is generally assumed that these species exhibit obligate DCF because their lack of wing musculature provides them with few resources to divert towards producing their first brood of workers. Thus, ICF by ergatoid queens is viewed as maladaptive because these queens need to take additional dangerous foraging trips to garner sufficient food to rear their first brood of workers. Contrary to this prediction, I document ICF by ergatoid queens for three species of harvester ants in the genus Pogonomyrmex (subfamily Myrmicinae), P. cunicularius cunicularius, P. cunicularius pencosensis, and P. huachucanus. Queens of P. huachucanus were obligate foragers, i.e., no minim workers could be produced without external food, and one queen of P. cunicularius pencosensis was observed foraging in the field. Abundant and/or predictable food resources likely select for the evolution of semi-claustral nest founding and ICF by these ergatoid queens. Under these conditions, foraging time would be minimized and the number and size of minim workers would be maximized. These benefits should increase founding success, which could compensate for loss of long-range dispersal. Overall, this study demonstrates that care should be taken before concluding that ant colonies employ DCF based solely on queen morphology.     

Life-History Characteristics and Fitness in Descendents of Parthenogenetic and Ex-Ephippio Females of Daphnia Magna

Daphnids of ex-ephippial and parthenogenetic origin differ substantially in life-history. Possible maternally transmitted ex-diapause effects of differing female origin on the fitness of their offspring were studied across multiple clones in Daphnia magna. Ex-ephippial daphnids responded in egg size to different constant food concentrations with the same pattern as parthenogenetic females. Significant differences in egg characteristics between females of different origin were only found for the first clutch produced under high food. The smaller size of eggs in ex-ephippial females, however, did not translate into size differences of first-clutch neonates. A trend for lower mass density per body volume was detected in offspring from ex-ephippial females in comparison with parthenogenetic daphnids. Hence, an ex-diapause effect transmitted by ex-ephippial mothers to their parthenogenetic offspring is likely. However, there was no difference in life-histories and fitness between offspring produced by females of ex-ephippial and parthenogenetic origin at both, high and low food concentrations across multiple clones. Thus, a significant ex-diapause effect on fitness in successive parthenogenetic generations may not be expected in D. magna at the population level.     

Digging effort in leaf-cutting ant queens (<Emphasis Type="Italic">Atta sexdens rubropilosa</Emphasis>) and its effects on survival and colony growth during the claustral phase

Nest foundation in the leaf-cutting ant Atta sexdens is claustral, and the single queen completely relies on its body reserves throughout, approximately, 9 weeks until the first workers emerge and initiate foraging. Nest digging is much time- and energy-consuming, and it is an open question how queens decide on the length of the tunnel they dig and therefore the depth of the initial chamber. Shallow founding nests may be energetically cheaper to dig, but queens may be more exposed to changing environmental variables. Deeper nests, on the other hand, may be climatically more stable and suitable, but more expensive to dig. We hypothesized that the maximal nest depth excavated by Atta founding queens may represent the outcome of an evolutionary trade-off between maximizing nest depth and minimizing energy expenditure during digging, so as to save energy for the long claustral phase. We tested this hypothesis by comparing the fitness consequences of increased digging effort in queens that were experimentally stimulated to excavate a complete founding nest either once, twice or three times consecutively compared to control queens that did not dig. Fitness was quantified as mortality rates, rates of egg-laying and offspring production, and size of the fungus garden until the emergence of the first workers. Results showed that, in contrast with the initial expectations, fungus growth, egg-laying rates and offspring production were not affected by the increased digging effort in the experimentally induced successive excavations. However, a significant higher mortality was observed in queens with increased digging effort, i.e., those that dug two or three nests consecutively. It is argued that in queens a behavioral mechanism for the control of nest depth has evolutionary been selected for as a trade-off between maximizing nest depth, to favor protection of the queen against unsuitable environmental variables, and minimizing energy expenditure during digging, which significantly affects survival.     

Queen recruitment and split sex ratios in polygynous colonies of the ant Formica exsecta

Sex ratios in social insects have become a general model for tests of inclusive fitness theory, sex ratio theory and parent–offspring conflict. In populations of Formica exsecta with multiple queens per colony , sex ratios vary greatly among colonies and the dry-weight sex ratio is extremely male-biased, with 89% of the colonies producing males but no gynes (reproductive females). Here we test the queen-replenishment hypothesis, which was proposed to explain sex ratio specialization in this and other highly polygynous ants (i.e. those with many queens per nest). This hypothesis proposes that, in such ants, colonies produce gynes to recruit them back into the colony when the number of resident queens falls below a given threshold limiting colony productivity or survival. We tested predictions of the queen-replenishment hypothesis by following F. exsecta colonies across two breeding seasons and relating the change in effective queen number with changes in sex ratio, colony size and brood production. As predicted by the queen-replenishment hypothesis, we found that colonies that specialized in producing females increased their effective queen number and were significantly more likely to specialize in male production the following year. The switch to male production also coincided with a drop in productivity per queen as predicted. However, adoption of new queens did not result in a significant increase in total colony productivity the following year. We suggest that this is because queen production comes at the expense of worker production and thus queen production leads to resource limitation the following year, buffering the effect of greater queen number on total productivity.     

A modeling approach to swarming in honey bees (Apis mellifera)

Identifying the mechanisms of colony reproduction is essential to understanding the sociobiology of honey bees. Although several proximate causes leading to the initiation of queen rearing – an essential prerequisite to swarming – have been proposed, none have received unequivocal empirical support. Here we model the main proximate hypotheses (colony size, brood comb congestion, and worker age distribution) and show that all proposed swarming triggers occur as a function of the ultimate cause of a colony reaching replacement stability, the point at which the queen has been laying eggs at her maximal rate. We thus present a reproductive optimization model of colony swarming based on evolutionary principles. All models produce results remarkably similar both to each other and to empirically-determined swarming patterns. An examination of the fit between the individual models and swarm-preventing techniques used by beekeepers indicates that the reproductive optimization model has a relatively broad explanatory range. These results suggest that an examination into the behavioral correlates of a queen’s maximum egg laying rate may provide a unified proximate mechanistic trigger leading predictably to colony fission. Generating a predictive model for this very well studied animal is the first step in producing a model of colony fission applicable to other swarm-founding eusocial animals. Received 16 November 2004; revised 31 May 2005; accepted 27 June 2005.