A newly-discovered mode of colony founding among fire ants

Summary Queen ants start new colonies either unassisted by workers (independent founding), assisted by workers from their natal nest (dependent founding), or assisted by the workers of other species (dependent, socially parasitic). The monogyne form of the fire ant,Solenopsis invicta, founds independently in summer, but in the fall it also produces a few sexuals some of which overwinter, then fly and mate in early spring. These overwintered queens lack the nutritional reserves and behaviors for independent colony founding. Rather, they seek out unrelated, mature, orphaned colonies, enter them and exploit the worker force to found their own colony through intraspecific social parasitism. Success in entering orphaned colonies is higher when these lack overwintered female alates of their own. When such alates are present, orphaning causes some to dealate and become uninseminated replacement queens, usually preventing entry of unrelated, inseminated replacement queens. Such colonies produce large, all-male broods. Successful entry of a parasitic queen robs the host colony of this last chance at reproductive success. Only overwintered sexuals take part in this mode of founding.     

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.     

A behavioral repertoire of <Emphasis Type="Italic">Atta sexdens</Emphasis> (Hymenoptera,Formicidae) queens during the claustral founding and ergonomic stages

Founding queens are central to the survival and maintenance of social insect colonies but are often ignored in studies of social insects. We expect the behaviors performed by a newly-mated ant queen to be critical to colony survival and maintenance but what are these behaviors and how do they change over time as colonies grow? The aim of this work was to describe and compare the behavioral repertoire performed by newly mated Atta sexdens queens during both founding and ergonomic stages. Using the Focal Animal Sampling method, 42 behavioral acts were identified and grouped into seven categories, according to their probable biological function. The most frequent behavioral acts were those related to selfgrooming, indicating the potential vulnerability of the colony to parasites at this early stage. Contrary to previous reports, A. sexdens queens feed on the fungus garden when founding new colonies, indicating that, although not exogenous, fungal staphylae, together with trophic eggs, supply the founding queens with a ready energy source they need during the founding stage. The behavioral repertoires of the queens that died during the observational period were compared with those of queens that survived. Before dying, queens performed a behavioral repertoire made almost exclusively of stereotyped behaviors, showing no apparent biological function. Queens that died exhibited lower frequencies of selfgrooming and did not ingest any staphylae, while laying more trophic eggs than the queens that survived. Our results indicate that selfgrooming may be a key behavior for queens to succeed in founding a colony in the absence of worker labor. Further, the behavioral repertoire reported can serve as a foundation for future behavioral work on this important phase in the life of social insects.     

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.     

Raiders from the sky: slavemaker founding queens select for aggressive host colonies

Reciprocal selection pressures in host-parasite systems drive coevolutionary arms races that lead to advanced adaptations in both opponents. In the interactions between social parasites and their hosts, aggression is one of the major behavioural traits under selection. In a field manipulation, we aimed to disentangle the impact of slavemaking ants and nest density on aggression of Temnothorax longispinosus ants. An early slavemaker mating flight provided us with the unique opportunity to study the influence of host aggression and demography on founding decisions and success. We discovered that parasite queens avoided colony foundation in parasitized areas and were able to capture more brood from less aggressive host colonies. Host colony aggression remained consistent over the two-month experiment, but did not respond to our manipulation. However, as one-fifth of all host colonies were successfully invaded by parasite queens, slavemaker nest foundation acts as a strong selection event selecting for high aggression in host colonies.     

Egg Recognition and Social Parasitism in Formica Ants

Nests of social insects are an attractive resource in terms of nutrition and shelter and therefore targeted by a variety of pathogens and parasites that harness the resources of a host colony in their own reproductive interests. Colonies of the ants Formica fusca and F. lemani serve as hosts for mound‐building Formica species, the queens of which use host colonies during colony founding. Here, we investigate whether workers of the host species can mitigate the costs imposed on them by invading parasite queens by recognizing and selectively removing eggs laid by these queens. We used behavioural assays, allowing host workers to choose between con‐colonial eggs and eggs laid by the parasite species F. truncorum. We show that workers of both host species discriminate between the two types of eggs in favour of con‐colonial eggs. Moreover, workers of F. fusca rejected more con‐colonial eggs than F. lemani. This higher rate of error in F. fusca may reflect a greater selectivity or a greater difficulty in discriminating between the two egg types. Nevertheless, both host species removed parasite eggs at a similar rate, when these were artificially introduced into the colonies, although some eggs remained after 10 d. In addition, upon receiving parasite eggs, host workers started to lay unfertilized male‐destined eggs within 6 d, thus employing an alternative pathway to gain direct fitness when the resident queen is no longer present and the colony is parasitized.     

Social interactions between an inquiline ant, <Emphasis Type="Italic">Ectatomma parasiticum</Emphasis>, and its host, <Emphasis Type="Italic">Ectatomma tuberculatum</Emphasis> (Formicidae,Ectatomminae)

Inquilines, workerless social parasites, frequently show advanced adaptations to their parasitic life style that indicate a long co-evolutionary history with their host. Ectatomma parasiticum, the first inquiline described in the poneromorph group, usurps established colonies of E. tuberculatum and produces only sexuals. In laboratory colonies, parasites were specifically attacked by the host workers, showing a failure in their social integration. Social interactions were frequent between parasites and their hosts, especially antennation, interpreted as attempts to promote colonial odor transfer. Inquilines destroyed eggs laid by the other queens (67 out of 209 eggs laid), including conspecific parasites, which is unusual. Such partial integration into the host colony and potential parasite virulence argue for a recent evolution of social parasitism in E. tuberculatum.     

Mode of colony foundation influences the primary sex ratio in ants

In ants, young queens can found new colonies independently (without the help of workers) or dependently (with the help of workers). It has been suggested that differences in the mode of colony founding strongly influence queen survival and colony development. This is because independent queens are constrained to produce a worker force rapidly, before they deplete their body reserves and to resist the intense intercolony competition during the founding stage. By contrast, queens that found colonies dependently remain with the workers, which probably results in a lower mortality rate and earlier production of reproductive offspring. Consequently, in species that found independently, queens of incipient colonies are expected to produce mostly worker brood by laying a lower fraction of haploid (male) eggs than queens in mature colonies; such a difference would not occur in species founding dependently. We compared the primary sex ratio (proportion of male-determined eggs) laid by queens in incipient and mature colonies of two ant species Lasius nigerLinepithema humile, showing independent and dependent modes of colony founding, respectively. As predicted L. niger queens of incipient colonies laid a lower proportion of haploid eggs than queens from mature colonies. By contrast, queens of L. humile laid a similar proportion of haploid eggs in both incipient and mature colonies. These results provide the first evidence that (1) the primary sex ratio varies according to the mode of colony foundation, and (2) queens can adjust the primary sex ratio according to the life history stage of the colony in ants. Copyright 1999 The Association for the Study of Animal Behaviour.     

New microsatellite loci for the socially diverse paper wasp genus Ropalidia

The Polistine wasps include both independent‐founding species, with small, single‐queen colonies founded by one or a few potential queens, and swarm‐founding species, which have larger societies, many queens and initiate colonies as a swarm of queens and workers. Swarm‐founding evolved from independent‐founding and Ropalidia is the only genus with both types, making it an excellent model system for understanding this dramatic shift in colony organization. We have isolated 18 polymorphic microsatellite loci from three species of Ropalidia, including two independent‐founding and one swarm‐founding species. These loci will allow us to reconstruct colony social and genetic structures in this important genus.     

Reproduction by virgin queen fire ants in queenless colonies: Comparative study of three taxa (Solenopsis richteri,hybridS. invicta/richteri,S. geminata) (Hymenoptera: Formicidae)

Summary In the fire ant,Solenopsis invicta, some winged virgin queens are known to shed their wings (dealate) upon removal of the mated mother queen. These virgin queens then develop their ovaries and begin to lay eggs, thereby foregoing the option of leaving on mating flights and attempting to found their own colonies. Such a response of virgin queens to queenlessness has not been reported for other ants. In order to determine if virgin queens of some other fire ants (subgenusSolenopsis) would respond in the same way, experiments were conducted onS. richteri, hybridS. invicta/richteri andS. geminata, a member of a species complex different from that of the other taxa. Just as inS. invicta, virgin queens ofS. richteri and the hybrid dealated and began to lay eggs within days of the removal of the queen. In addition, workers executed many of the reproductively active virgin queens, a phenomenon also found inS. invicta. In contrast, virgin queens ofS. geminata did not dealate or quickly begin to lay eggs upon separation from the queen. Reasons for the variability in the response of virgin queens of the different species may be 1) higher probability of reproductive success for unmated dealated queens compared to normal claustral founding inS. invicta andS. richteri linked to relatively frequent loss of the mother queen; or 2) phylogenetic constraint.     

The economics of brood raiding and nest consolidation during ant colony founding

Summary The most dangerous time for an ant colony is during the founding stage when the small colony is vulnerable to predation and competition. Colonies can grow more rapidly when multiple queens cooperate in raising the first worker brood (pleometrosis) or by raiding other incipient colonies for their brood. This brood raiding has been proposed to be the primary force selecting for pleometrosis, i.e. multiple-queen colonies may have a considerable advantage in destroying neighbours by aggressively stealing their brood. An alternative hypothesis is that incipient nests are part of a larger, interconnected population structure and that brood raiding reflects cooperative pleometrosis with subdivided colonies. A simple mathematical model supports the second hypothesis: workers of incipient colonies are especially favoured to peaceably abandon their nest and join with other colonies if the queens are related or queens from raided colonies can infiltrate the raiding colony. The latter condition is often met in ant species that brood raid and particularly exemplified in fire ants (Solenopsis invicta), where brood raiding involves little mortal combat and combines with pleometrosis to rapidly increase colony size. It is proposed that the term nest consolidation should replace brood raiding to more accurately reflect the relatively non-aggressive and potentially apparently cooperative nature of interactions between incipient ant colonies.     

Queen phenotype and behaviour during cooperative colony founding in Polyrhachis moesta

Summary. Founding queens of the arboreal ant Polyrhachis moesta aggregate independently of kinship and cooperate in caring for their brood. In field studies, the number of queens in a founding nest varied from 1 to 8. The number of queens in the nests with multiple queens decreased significantly with time after the nuptial flight, resulting in monogynous or oligogynous nests. Single- and multiple-founding queens did not differ in characteristics representing nutritional states or body size immediately after the nuptial flight. Wet body weight decreased as days passed, whereas head width of founding queens who overwintered successfully were relatively larger. In laboratory studies, founding queens performed liquid food exchanges more frequently with queens from other founding nests or immature colonies than with those from the same nests. Queens in founding nests and immature colonies were observed to show no aggression against non-nestmate queens, whereas queens in established colonies showed aggressive behaviours against non-nestmates. This indicates that founding queens change drastically in their aggression levels before and after colony establishment. Multiple-founding queens started laying eggs earlier than single-founding queens under laboratory conditions. Higher brood productivity and lower brood mortality were observed in multiple-queen nests. These potential advantages in multiple-queen founding may support the cooperative association among unrelated founding queens.Received 1 December 2003; revised 25 March and 20 May 2004; accepted 3 June 2004.     

Host nest usurpation and colony foundation in the European amazon ant,Polyergus rufescens Latr. (Hymenoptera: Formicidae)

Summary The socially parasitic mode of founding new colonies by queens of the European amazon antPolyergus rufescens was analysed in the laboratory. Newly-mated females of this obligatory slave-maker were individually introduced into queenright and queenless artificially established colonies of bothFormica cunicularia (the slave present in the natal dulotic nest) andF. rufibarbis (another potentialServiformica host). Particular attention was devoted to the behavioural patterns displayed by these young queens during the usurpation phases. Our observations, supported also by video-taping, show that the slave-making female, before laying her eggs, must penetrate the host colony, kill the resident queen, become accepted by the adult workers and appropriate the host brood. The parasite was almost always adopted in the colonies ofF. cunicularia, whereas in the presence ofF. rufibarbis it was generally killed in a short time. The failure in the attempt of usurping the colonies ofF. rufibarbis is discussed in relation to the host specificity typical of this slave-maker. Finally, egg-laying byPolyergus successful usurpers, the subsequent eclosion of the brood, and its complete social integration in the newly-established mixed colonies were also recorded.     

A simple genetic basis for complex social behaviour mediates widespread gene expression differences

A remarkable social polymorphism is controlled by a single Mendelian factor in the fire ant Solenopsis invicta. A genomic element marked by the gene Gp‐9 determines whether workers tolerate one or many fertile queens in their colony. Gp‐9 was recently shown to be part of a supergene with two nonrecombining variants, SB and Sb. SB/SB and SB/Sb queens differ in how they initiate new colonies, and in many physiological traits, for example odour and maturation rate. To understand how a single genetic element can affect all these traits, we used a microarray to compare gene expression patterns between SB/SB and SB/Sb queens of three different age classes: 1‐day‐old unmated queens, 11‐day‐old unmated queens and mated, fully reproductive queens collected from mature field colonies. The number of genes that were differentially expressed between SB/SB and SB/Sb queens of the same age class was smallest in 1‐day‐old queens, maximal in 11‐day‐old queens and intermediate in reproductive queens. Gene ontology analysis showed that SB/SB queens upregulate reproductive genes faster than SB/Sb queens. For all age classes, genes inside the supergene were overrepresented among the differentially expressed genes. Consistent with the hypothesized greater number of transposons in the Sb supergene, 13 transposon genes were upregulated in SB/Sb queens. Viral genes were also upregulated in SB/Sb mature queens, consistent with the known greater parasite load in colonies headed by SB/Sb queens compared with colonies headed by SB/SB queens. Eighteen differentially expressed genes between reproductive queens were involved in chemical signalling. Our results suggest that many genes in the supergene are involved in regulating social organization and queen phenotypes in fire ants.     

Social chromosome variants differentially affect queen determination and the survival of workers in the fire ant Solenopsis invicta

Intraspecific variation in social organization is common, yet the underlying causes are rarely known. An exception is the fire ant Solenopsis invicta in which the existence of two distinct forms of social colony organization is under the control of the two variants of a pair of social chromosomes, SB and Sb. Colonies containing exclusively SB/SB workers accept only one single queen and she must be SB/SB. By contrast, when colonies contain more than 10% of SB/Sb workers, they accept several queens but only SB/Sb queens. The variants of the social chromosome are associated with several additional important phenotypic differences, including the size, fecundity and dispersal strategies of queens, aggressiveness of workers, and sperm count in males. However, little is known about whether social chromosome variants affect fitness in other life stages. Here, we perform experiments to determine whether differential selection occurs during development and in adult workers. We find evidence that the Sb variant of the social chromosome increases the likelihood of female brood to develop into queens and that adult SB/Sb workers, the workers that cull SB/SB queens, are overrepresented in comparison to SB/SB workers. This demonstrates that supergenes such as the social chromosome can have complex effects on phenotypes at various stages of development.     

Genetic and morphological variation over space and time in the invasive fire ant <Emphasis Type="Italic">Solenopsis invicta</Emphasis>

Social insects are among the most successful and damaging of invasive taxa. We studied spatial and temporal variation in two traits, colony genetic structure and worker mass, associated with social insect success in the introduced fire ant Solenopsis invicta. Our aim was to determine if changes in social structure occurred over time and if variation in worker size was related to worker genotype. We sampled 1139 workers from five multiple-queen S. invicta nests on six dates over a one-year period. The genotypes of workers were determined at ten microsatellite loci and at the selected locus general protein-9 (Gp-9). We found little evidence for genetic differentiation of workers sampled from distinct nests or from different dates at the microsatellite loci. However, worker Gp-9 genotype frequencies varied among nests and over time. In addition, worker mass was affected by nest-of-origin, sampling date, ploidy level, and Gp-9 genotype. Our results suggest that large numbers of queens contribute to the production of workers in introduced S. invicta nests throughout the year. Colony boundaries are semi-permeable, although the among-nest variation in Gp-9 genotype frequencies and worker mass does suggest that boundaries are present. In addition, selection operating on Gp-9 genotype depends on nest environment. Finally, worker mass is affected by both endogenous and exogenous factors in S. invicta. Overall, our data suggests that the key traits of colony social structure and worker size reflect the effects of variable selection in invasive social insects.     

The socially parasitic ant Polyergus mexicanus has host‐associated genetic population structure and related neighbouring colonies

The genetic structure of populations can be both a cause and a consequence of ecological interactions. For parasites, genetic structure may be a consequence of preferences for host species or of mating behaviour. Conversely, genetic structure can influence where conspecific interactions among parasites lay on a spectrum from cooperation to conflict. We used microsatellite loci to characterize the genetic structure of a population of the socially parasitic dulotic (aka “slave‐making”) ant (Polyergus mexicanus), which is known for its host‐specificity and conspecific aggression. First, we assessed whether the pattern of host species use by the parasite has influenced parasite population structure. We found that host species use was correlated with subpopulation structure, but this correlation was imperfect: some subpopulations used one host species nearly exclusively, while others used several. Second, we examined the viscosity of the parasite population by measuring the relatedness of pairs of neighbouring parasitic ant colonies at varying distances from each other. Although natural history observations of local dispersal by queens suggested the potential for viscosity, there was no strong correlation between relatedness and distance between colonies. However, 35% of colonies had a closely related neighbouring colony, indicating that kinship could potentially affect the nature of some interactions between colonies of this social parasite. Our findings confirm that ecological forces like host species selection can shape the genetic structure of parasite populations, and that such genetic structure has the potential to influence parasite‐parasite interactions in social parasites via inclusive fitness.     

Social parasitism by Cape honeybee workers in colonies of their own subspecies (Apis mellifera capensis Esch.)

Social parasitism is widespread in the eusocial insects. Although social parasites often show a reduced worker caste, unmated workers can also parasitize colonies. Cape honeybee workers, Apis mellifera capensis, can establish themselves as social parasites in host colonies of other honeybee subspecies. However, it is unknown whether social parasitism by laying workers also occurs among Cape honeybee colonies. In order to address this question we genotyped worker offspring of six queenless A. m. capensis colonies and determined the maternity of the reproducing workers. We found that three non-nestmate workers dominated reproduction in a host colony and produced 62.5% of the progeny. Our results show that social parasitism by laying workers is a naturally occurring part of the biology of Cape honeybees. However, such social parasitism is not frequently found (6.41% of the total worker offspring) probably due to co-evolutionary processes among A. m. capensis resulting in an equilibrium between selection for reproductive dominance in workers, colony maintenance and queen adaptation. Received 28 July 2005; revised 19 September and 11 November 2005; accepted 16 November 2005.     

Back to one: consequences of derived monogyny in an ant with polygynous ancestors

The number of queens per colony is of fundamental importance in the life history of social insects. Multiple queening (polygyny), with dependent colony founding by budding, has repeatedly evolved from ancestral single queening (monogyny) and independent founding by solitary queens in waSPS, bees and ants. By contrast, the reversal to monogyny appears to be rare, as polygynous queens often lack morphological adaptations necessary for dispersal and independent colony founding. In the ant genus Cardiocondyla, monogynous species evolved from polygynous ancestors. Here, we show that queens of monogynous species found their colonies independently, albeit in an unusual way: they mate in the maternal nest, disperse on foot and forage during the founding phase. This reversal appears to be associated with the occurrence of a wing polymorphism, which reflects a trade-off between reproduction and dispersal. Moreover, queens of monogynous species live considerably longer than queens in related polygynous taxa, suggesting that queen life span is a plastic trait.     

Experimental Conversion of Colony Social Organization in Fire Ants (<Emphasis Type="Italic">Solenopsis invicta</Emphasis>): Worker Genotype Manipulation in the Absence of Queen Effects

Colony social organization in the fire ant Solenopsis invicta appears to be under strong genetic control. In the invasive USA range, polygyny (multiple queens per colony) is marked by the presence of the Gp-9 ^b allele in most of a colony’s workers, whereas monogyny (single queen per colony) is associated with the exclusive occurrence of the Gp-9 ^B allele. Ross and Keller, Behav Ecol Sociobiol 51:287–295 (2002) experimentally manipulated social organization by cross-fostering queens into colonies of the alternate form, thereby changing adult worker Gp-9 genotype frequencies over time. Although these authors showed that social behavior switched predictably when the frequency of b-bearing adult workers crossed a threshold of 5–10%, the possibility that queen effects caused the conversions could not be excluded entirely. We addressed this problem by fostering polygyne brood into queenright monogyne colonies. All such treatment colonies switched social organization to become polygyne, coincident with their proportions of b-bearing workers exceeding 12%. Our results support the conclusion that polygyny in S. invicta is induced by a minimum frequency of colony workers carrying the b allele, and further confirm that its expression is independent of queen genotype or history, worker genotypes at genes not linked to Gp-9, and colony genetic diversity.