Group defense by colony-founding queens in the fire ant Solenopsis invicta

Mutualistic associations among nonkin can form when animalsin groups have a greater chance of overcoming challenges presentedby the environment than do solitary animals. Colony foundingby small groups of unrelated queens, a habit documented in severalspecies of ants, is often interpreted as a mutualistic interactionselected by intense competition among incipient colonies. However,many new colonies in these species are founded in areas wheretheir chief enemies are mature ant colonies, rather than othernewly founded colonies. In this study, we tested whether groupnest-founding in the fire ant Solenopsis invicta improved theability of queens to survive attacks by mature colonies. Inthe laboratory, queens in groups of three were more likely thansolitary queens to survive attacks by workers of the nativefire ant Solenopsis geminata. When newly mated queens were establishedexperimentally in the field, workers from mature S. invictacolonies caused the majority of queen deaths. Queens in groupsof two, but not in groups of four, had higher survival ratesthan did solitary queens during the period between colony establishmentand the appearance of the first workers. The advantage of cooperativedefense approximately counterbalanced the disadvantages causedby competition within foundress associations of two to threequeens. Previous studies have shown that colonies founded bymultiple queens produce larger worker populations than coloniesfounded by solitary queens; however, experimentally increasingworker number in incipient colonies had no effect on colonysurvival in the field.     

Reproductive development and ontogeny of queen pheromone production in the fire ant Solenopsis invicta

Queens of the fire ant, Solenopsis invicta Buren, produce several releaser and primer pheromones. Using bioassays, the ontogeny of three of these pheromones related to reproductive development was investigated. Virgin queens, in which the process of wing-shedding (dealation) serves as an indicator of the initiation of reproductive development, were studied. First, the production of two queen pheromones produced in the poison gland was examined. The pheromone responsible for initiation and maintenance of retinue formation, a releaser effect, was found to be produced in detectable quantities 2 days after dealation, at which time queens showed significant ovary development and many (30%) had started laying eggs. A primer pheromone that inhibits alate virgin queens from dealating was detected in queens 3 days following wing-shedding, when 80% of the queens were ovipositing. Second, I examined the onset of a pheromone of unknown glandular origin produced by reproductively active virgin queens which leads to their destruction in queenright colonies by stimulating workers to attack and kill them. This pheromone is secreted in quantities detectable by bioassay 2 days after dealation. Thus, in S. invicta, the ontogeny of three distinct queen pheromones is tightly linked with ovary development and initiation of egg laying. These results demonstrate reproductive and communicative functions are closely associated during the transition from potential to functional queen.     

红火蚁的社会型及其相关基因Gp-9的研究综述

红火蚁Solenopsis invicta Buren的蚁巢具有2种基本的社会组织形态:单后型和多后型。蚁巢中蚁后的数量是由工蚁和蚁后的基因型共同决定的。红火蚁的Gp-9基因编码一种气味结合蛋白并控制这种社会多态性的表达。Gp-9基因的发现首次证明单个基因在昆虫复杂的社会行为中起关键的作用。从红火蚁的社会型特征、Gp-9基因与不同社会型的关系以及Gp-9基因的相关研究对该领域的研究进展进行综述。     

Oviposition and oogenesis in virgin fire ant females Solenopsis invicta are associated with a high level of dopamine in the brain

Abstract. In the fire ant Solenopsis invicta Buren, virgin females are capable of shedding their wings (dealation) and laying haploid eggs. However, dealation and reproduction are inhibited by a queen primer pheromone that depresses the release of Juvenile Hormone by the corpora allata. In an attempt to identify other neural signals that trigger the reproductive system, we measured the effect on brain biogenic amines of separation from the queen. Dopamine in the brain of virgin females increased from 552 ± 42 to 971 ± 65 fMol/brain when reproduction and dealation were stimulated by 15 days of separation. Octopamine and 5-hydroxytryptamine did not change significantly after the separation. Isolated virgin females fed with a tyrosine hydroxylase inhibitor 3-iodo- l -tyrosine mixed in sucrose for 15 days laid significantly fewer eggs and had fewer chorionated oocytes in their ovarioles than females fed with sucrose only. Restoring dopamine biosynthesis by adding l -dopa to the food also restored oogenesis and oviposition. Dealation was not affected by 3-iodo- l -tyrosine or l -dopa. The possible role of dopamine as the neural target of the queen pheromone regarding its potent allotoregulatory effect in other insects is discussed.     

Major gene effects on phenotype and fitness: the relative roles of Pgm-3 and Gp-9 in introduced populations of the fire ant Solenopsis invicta

The objective of this study was to disentangle the relative effects of Pgm-3 and Gp-9 and/or other closely linked genes on the phenotypes and reproductive success of queens in introduced (USA) populations of S. invicta. Gp-9 or a closely linked gene(s) was found to have major effects on queen weight, the likelihood that queens shed their wings (a behaviour associated with the onset of reproduction), and the probability that queens are accepted in polygyne (multiple-queen) colonies. Our analyses show that once the effect of Gp-9 genotype is taken into account, Pgm-3 genotype no longer is significantly associated with differences in queen phenotype or the probability of queens being accepted in polygyne colonies. This suggests that the associations of Pgm-3 genotype with weight, wing shedding rate and probability of acceptance by polygyne colonies previously reported in studies that did not control for the effects of Gp-9 are due to the strong linkage disequilibrium that exists between Pgm-3 and Gp-9, or to linkage disequilibria between these and other genes affecting queen phenotype and fitness. Several lines of evidence, including data from the native South American range, suggest that additional cryptic alleles at Gp-9, or additional genes in the same linkage group as Gp-9, must be involved in controlling queen phenotype and the large suite of traits important in determining social organization of S. invicta colonies.     

Modelling the potential spread of Solenopsis invicta Buren (Hymenoptera: Formicidae) (red imported fire ant) in Australia

Abstract  Quantifying the potential spread and density of an invading organism enables decision-makers to determine the most appropriate response to incursions. We present two linked models that estimate the spread of Solenopsis invicta Buren (red imported fire ant) in Australia based on limited data gathered after its discovery in Brisbane in 2001. A stochastic cellular automaton determines spread within a location (100 km by 100 km) and this is coupled with a model that simulates human-mediated movement of S. invicta to new locations. In the absence of any control measures, the models predict that S. invicta could cover 763 000–4 066 000 km² by the year 2035 and be found at 200 separate locations around Australia by 2017–2027, depending on the rate of spread. These estimated rates of expansion (assuming no control efforts were in place) are higher than those experienced in the USA in the 1940s during the early invasion phases in that country. Active control efforts and quarantine controls in the USA (including a concerted eradication attempt in the 1960s) may have slowed spread. Further, milder winters, the presence of the polygynous social form, increased trade and human mobility in Australia in 2000s compared with the USA in 1940s could contribute to faster range expansion.     

带土园艺植物传播红火蚁的风险调查

调查了广东广州、深圳40余个苗木花卉场74种带土园艺植物上红火蚁Solenopsis invicta Buren发生情况。调查结果表明,桉树苗、海枣、垂叶榕、黄金香柳、小叶榕、狗尾草、罗汉松等17种植物上红火蚁发生比率超过1%,是高风险带土植物。不同生产环境、不同栽培方式中盆/钵/袋栽红火蚁发生高于地面栽培方式,露天置于砂土、泥土、碎石上红火蚁发生风险较高,置于水泥地上的风险较低。提出了降低带土园艺植物传播红火蚁的管理措施。     

Queen recruitment in a multiple-queen population of the fire ant Solenopsis invicta

We assessed patterns of new queen recruitment in a polygyne(multiple queens per nest) population of the fire ant Solenopsisinvicta in its introduced range. Newly recruited queens wereidentified using four physiological markers, and genotypic datafrom nuclear and mitochondrial markers were used to estimaterelatedness of new nest mate queens to each other and to theolder nest mate queens. In total, 1.7% of the queens collectedin late spring and early summer were deemed to be new recruits.The relatedness of these queens to each other and to the olderqueens within nests was not significantly different from zero,suggesting that newly recruited queens represent a random sampleof potential reproductive queens in the population. Moreover,the number of new queens recruited within nests was not correlatedwith the number of older queens present and did not differ significantlyfrom a Poisson distribution. Thus, queen recruitment in this populationof S. invicta appears to occur at random with respect to thenumber of older queens present within nests.     

Differential gene expression between adult queens and workers in the ant Lasius niger

Ants and other social insects forming large societies are generally characterized by marked reproductive division of labour. Queens largely monopolize reproduction whereas workers have little reproductive potential. In addition, some social insect species show tremendous lifespan differences between the queen and worker caste. Remarkably, queens and workers are usually genotypically identical, meaning that any phenotypic differences between the two castes arise from caste-specific gene expression. Using a combination of differential display, microarrays and reverse Northern blots, we found 16 genes that were differentially expressed between adult queens and workers in the ant Lasius niger, a species with highly pronounced reproductive division of labour and a several-fold lifespan difference between queens and workers. RNA ligase mediated rapid amplification of cDNA ends (RLM-RACE) and gene walking were used to further characterize these genes. On the basis of the molecular function of their nearest homologues, three genes appear to be involved in reproductive division of labour. Another three genes, which were exclusively overexpressed in queens, are possibly involved in the maintenance and repair of the soma, a candidate mechanism for lifespan determination. In-depth functional analyses of these genes are now needed to reveal their exact role.     

Characteristics of 11 polymorphic microsatellite markers in the red imported fire ant, Solenopsis invicta Buren

We have characterized 11 polymorphic microsatellite loci in the invasive ant Solenopsis invicta. Primer pairs were evaluated on fire ants collected from monogyne mounds in Lauderdale County, Mississippi. The observed and effective number of alleles ranged from two to six and from 1.31 to 2.64, respectively. The observed and expected heterozygosity values ranged from 0.1613 to 0.7826 and from 0.1491 to 0.6242, respectively. The polymorphism information content of the microsatellites ranged from 0.1482 to 0.6208. Probability tests indicated significant deviations from the Hardy-Weinberg equilibrium at three loci. Pairwise tests did not detect linkage disequilibrium between any pair of loci.     

Experimental analysis of territory size in a population of the fire ant Solenopsis invicta

Alternative models of territoriality are based on contrastingassumptions about the behavioral processes determining territorysize. In a series of controlled field experiments on the fireant Solenopsis invicta, I tested whether territory size is affectedby the availability of food, as predicted by most economic models,and whether territory size is affected by fighting ability,as predicted by models of competition among neighbors. Abundantfood was offered for 30–35 days to selected colonies eitherimmediately next to the nest (experiment 1) or at peripheralsites near the territory boundary (experiment 2). These foodsupplements had no detectable effect on territory size. Furthermore,food placed near the periphery of the territory did not significantlyalter local boundary positions. During both experiments, largecolonies lost more territory than did small colonies, reflectingtemporary declines in worker number due to the seasonal productionof reproductives. Such losses by large colonies during the summermonths create opportunities for newly founded colonies to expandterritories. In a third experiment, colonies from which workerswere removed lost significantly more territory than did unmanipulatedcontrols. These results show that territory areas in S. invictaare strongly affected by the relative fighting ability of neighboringcolonies but provide no evidence that colonies adjust territoryarea in response to short-term changes in the availability offood.     

The success of alternative reproductive tactics in monogyne populations of the ant Solenopsis invicta: significance for transitions in social organization

Newly produced queens from monogyne (single-queen) coloniesof the ant Solenopsis invicta usually initiate reproductionindependently, that is, without worker assistance. However,some recently mated queens attempt to bypass this risky phaseof new colony foundation by entering established nests to reproduce,although it is unclear how often these queens are successfulin natural populations. We surveyed a mature monogyne populationof S. invicta in both 1995 and 1996 for colonies headed by queensincapable of independent colony founding (diploid-male-producingqueens) in order to estimate the frequency of colonies thatare headed by queens that initiated reproduction within establishednests (adopted queens). Using the frequency of diploid-male-producingqueens among the recently mated queens in this population, weestimated that the overall rate of queen replacement by adoptedqueens is about 0.7% per colony per year. Although theory suggeststhat a change to a novel queen reproductive tactic could beassociated with a fundamental change in social organization(queen number), this does not appear to be the case in monogyneS. invicta. However, the evolution of nest-infiltrating reproductivetactics by queens in a monogyne population and the evolutionof multiple-queen societies may result from similar ecologicalpressures facing newly mated queens. We therefore incorporatethis strategy into an existing theoretical framework that wasdeveloped to explain the evolution of alternative social organizationsin ants, providing testable predictions regarding the distributionand frequency of queen adoption in other single-queen ant societies.     

Trophallaxis by temporal subcastes in the fire ant, Solenopsis invicta, in response to honey

ABSTRACT. Trophallactic behaviour of temporal subcastes in Solenopsis invicta Buren colonies was studied in two separate experiments. First, radiolabeled honey was presented to small colonies containing larvae, queens and marked workers; radioactivity in the head, thorax and abdomen of each ant was measured after 0.25, 1, 6, 12, 24, 48 and 72 h. The quantity of honey per subcaste was dependent on the total amount of honey collected. As more honey entered the colony, the quantity in foragers, queens and reserves increased more rapidly than that in nurses or larvae. The internal distribution of radioactivity in the head, thorax or abdomen indicated that differences between subcaste members in either the rate of food exchange or digestion existed. In a second experiment behavioural observations were made on marked workers in colonies before and after the presentation of honey. Reserves spent significantly more time engaged in trophallaxis than either foragers or nurses, both as active donors and active receivers. Based on number of encounters, nurses were more likely to receive honey while reserves and foragers were more likely to donate honey. The duration of encounters involving nurses tended to be shorter than those involving reserves or foragers.     

Behaviour of worker subcastes in the fire ant, Solenopsis invicta, in response to proteinaceous food

ABSTRACT. The effects of division of labour on response behaviour to food in the red imported fire ant, Solenopsis invicta Buren, were examined to determine if caste members differ in amount of food taken, in rate of food transfer, or in internal distribution of food; and to see if food availability, time, or temporal subcaste pairing affect feeding behaviour. To measure differences in behaviour we fed radioiodinated albumin mixed with egg yolk to colonies containing larvae, queens, and (a) foragers and nurses, or (b) foragers and reserves, or (c) nurses and reserves. Samples were taken over a 72-h period and radioactivity in the head, thorax and abdomen of each worker was determined. There were significant differences between nurses, foragers and reserves in quantity of food consumed, rate of transfer, and internal distribution of radioactivity. These differences were related to their respective roles of foraging, food storage and transfer, and brood tending. The quantity of food taken per subcaste was dependent on the total amount of food in the colony, with transfer rates differing between subcastes as the quantity of food in the colony increased. The rate at which protein was transferred between subcastes was slower in the reserves than that in either foragers or nurses. Therefore, reserves may serve as a temporary store of protein for the colony.     

Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta

Supergenes are clusters of tightly linked loci maintained in specific allelic combinations to facilitate co-segregation of genes governing adaptive phenotypes. In species where strong selection potentially operates at different levels (e.g. eusocial Hymenoptera), positive selection acting within a population to maintain specific allelic combinations in supergenes may have unexpected consequences for some individuals, including the preservation of disadvantageous traits. The nuclear gene Gp-9 in the invasive fire ant Solenopsis invicta is part of a non-recombining, polymorphic supergene region associated with polymorphism in social organization as well as traits affecting physiology, fecundity and behaviour. We show that both male reproductive success and facultative polyandry in queens have a simple genetic basis and are dependent on male Gp-9 genotype. Gp-9(b) males are unable to maintain exclusive reproductive control over their mates such that queens mated to Gp-9(b) males remain highly receptive to remating. Queens mated to multiple Gp-9(B) males are rare. This difference appears to be independent of mating plug production in fertile males of each Gp-9 genotype. However, Gp-9(b) males have significantly lower sperm counts than Gp-9(B) males, which could be a cue to females to seek additional mates. Despite the reduced fitness of Gp-9(b) males, polygyne worker-induced selective mortality of sexuals lacking b-like alleles coupled with the overall success of the polygyne social form act to maintain the Gp-9(b) allele within nature. Our findings highlight how strong worker-induced selection acting to maintain the Gp-9(b) allele in the polygyne social form may simultaneously result in reduced reproductive fitness for individual sexual offspring.     

Effect of queen number on the production of sexuals in natural populations of the fire ant, Solenopsis invicta

ABSTRACT. To determine whether the production of sexuals in the fire ant, Solenopsis invicta Buren, is related to queen number in the field, the numbers of sexuals in monogyne (M) and polygyne (P) colonies of this species were compared. Large colonies ( n =25 M and 25 P) were collected at random during spring, summer and fall when sexuals are actively produced, and the numbers of sexuals present were counted. The numbers of alates plus sexual pupae and larvae in M colonies far exceeded those in P colonies in each season. Significant differences between M and P colonies were also found when the numbers of alates and sexual immatures (pupae + larvae) were compared separately in each season. In addition, M colonies contained significantly more female sexuals (alates + pupae) than did P colonies in the summer and fall, and significantly more males in all three seasons. The negative relationship between queen number and number of sexuals provides evidence that queen control over the production of sexuals, previously established in laboratory experiments, also occurs under natural conditions.     

Propagule pressure and colony social organization are associated with the successful invasion and rapid range expansion of fire ants in China

We characterized patterns of genetic variation in populations of the fire ant Solenopsis invicta in China using mitochondrial DNA sequences and nuclear microsatellite loci to test predictions as to how propagule pressure and subsequent dispersal following establishment jointly shape the invasion success of this ant in this recently invaded area. Fire ants in Wuchuan (Guangdong Province) are genetically differentiated from those found in other large infested areas of China. The immediate source of ants in Wuchuan appears to be somewhere near Texas, which ranks first among the southern USA infested states in the exportation of goods to China. Most colonies from spatially distant, outlying areas in China are genetically similar to one another and appear to share a common source (Wuchuan, Guangdong Province), suggesting that long‐distance jump dispersal has been a prevalent means of recent spread of fire ants in China. Furthermore, most colonies at outlier sites are of the polygyne social form (featuring multiple egg‐laying queens per nest), reinforcing the important role of this social form in the successful invasion of new areas and subsequent range expansion following invasion. Several analyses consistently revealed characteristic signatures of genetic bottlenecks for S. invicta populations in China. The results of this study highlight the invasive potential of this pest ant, suggest that the magnitude of international trade may serve as a predictor of propagule pressure and indicate that rates and patterns of subsequent range expansion are partly determined by the interplay between species traits and the trade and transportation networks.     

Social control of egg-laying rate in queens of the fire ant, Solenopsis invicta*

ABSTRACT Social control of egg-laying rate in queens of the fire ant (Solenopsis invicta Buren) was studied by experimental manipulation of the number of larvae, pupae and workers in colonies, and the age and size of larvae and workers. Workers and pupae do not stimulate oviposition by queens. The number of fourth instar larvae, on the other hand, bears a positive log-log relationship to the queen's egg-laying rate. Such larvae are needed both to stimulate and maintain oviposition. Their withdrawal results, within 48 h, in a decline in queen oviposition almost to zero. Their addition to broodless nests results in peak laying in about 4 days. Larvae in the first three stadia and early in the fourth stadium have a much lower effect upon queen fecundity. Sexual larvae are only c. 5% as stimulating on a weight basis, but equivalent on an individual basis. Several associated measures are positively correlated to egg-laying rate: weight of the queen, the number of her vitellogenic follicles per ovariole, total vitellogenic follicles, the time she spends feeding and (usually) the number of workers in the retinue that cares for her. The egg volume is negatively correlated with laying rate, so that queens lay more eggs for the same expenditure of material as laying rate increases. As body size of workers increases, they become less effective in transmitting the larval stimulation to the queen, but worker age has no effect on this ability. For a given number of larvae, queens in small, naturally growing colonies lay fewer, larger eggs than do queens in experimental colonies, but their fecundity increases more rapidly in relation to number of larvae. When larvae are fed vital-dyed food in one experimental colony, and then transferred to an undyed colony, the dye is rapidly transferred to worker crops, and into the queen's eggs, indicating bulk movement of material from larvae to workers to the queen and eggs. Large larvae are more effective at this than small larvae. Fourth instar larvae may be a digestive and metabolic caste that processes protein for egg production by the queen. If that is the case, the queen and fourth instar larvae are linked in a positive feedback loop. Either the logarithmic relation of fecundity to larval numbers or physical limits of the queen may set the maximum egg-laying rate, and thus determine maximum colony size. The data do not allow a clear choice between these alternatives.