Significant reproductive skew in the facultatively polygynous ant Pheidole pallidula

Reproductive skew - the extent to which reproduction is unevenly shared between individuals in a social group - varies greatly between and within animal species. In this study, we investigated how queens share parentage in polygynous (multiple queen) colonies of the Mediterranean ant Pheidole pallidula. We used highly polymorphic microsatellites markers to determine parentage of gynes (new queens), males and workers in P. pallidula field colonies. The comparison of the genotypes of young and adult workers revealed a very low queen turnover (less than 2%). The first main finding of the study of reproductive skew in these colonies was that there was a significant departure from equal contribution of queens to gyne, male and worker production. Reproductive skew was greater for male production than for queen and worker production. There was no relationship between the magnitude of the reproductive skew and the number of reproductive queens per colony, their relatedness and the overall colony productivity, some of the factors predicted to influence the extent of reproductive skew. Finally, our study revealed for the first time a trade-off in the relative contribution of nestmate queens to gyne and worker production. The queens contributing more to gyne production contributed significantly less to worker production.     

Breeding system, colony and population structure in the weaver ant Oecophylla smaragdina

Weaver ants ( Oecophylla smaragdina ) are dominant ants in open forests from India, Australia, China and Southeast Asia, whose leaf nests are held together with larval silk. The species, together with its sole congener O. longinoda , has been important in research on biological control, communication, territoriality and colony integration. Over most of the range, only one queen has been found per colony, but the occurrence of several queens per nest has been reported for the Australian Northern Territory. The number of males mating with each queen is little known. Here we report on the colony structure of O. smaragdina using published and new microsatellite markers. Worker genotype arrays reflect the occurrence of habitual polygyny (more than one queen per colony) in 18 colonies from Darwin, Northern Australia, with up to five queens inferred per colony. Monogyny (one queen per colony) with occasional polygyny was inferred for 14 colonies from Queensland, Australia, and 20 colonies from Java, Indonesia. Direct genotyping of the sperm carried by 77 Queensland queens and worker genotypic arrays of established colonies yielded similar results, indicating that less than half of the queens mate only once and some mate up to five times. Worker genotype arrays indicated that queens from Java and the Northern Territory also often mate with more than one male, but less often than those from Queensland. A strong isolation-by-distance effect was found for Queensland samples. The variation uncovered means that O. smaragdina is a more versatile study system than previously supposed.     

Socio-genetic structure and mating system of a wild boar population

Wild boars Sus scrofa have a social organization based on female groups that can include several generations of adults and offspring, and are thus likely matrilineal. However, little is known about the degree of relatedness between animals living in such groups or occupying the same core area of spatial activity. Also, polygynous male mating combined with matrilineal female groups can have strong influences on the genetic structure of populations. We used microsatellite genotyping combined with behavioral data to investigate the fine-scale population genetic structure and the mating system of wild boars in a multi-year study at Châteauvillain-Arc-en-Barrois (France). According to spatial genetic autocorrelation, females in spatial proximity were significantly inter-related. However, we found that numerous males contributed to the next generation, even within the same social group. Based on our genetic data and behavioral observations, wild boars in this population appear to have a low level of polygyny associated with matrilineal female groups, and infrequent multiple paternity. Mortality due to hunting may facilitate the breakup of what historically has been a more predominantly polygynous mating system, and likely accelerates the turnover of adults within the matrilineal groups.     

Mating frequency and mating system of the polygynous ant, Leptothorax acervorum

Multiple mating by queens (polyandry) and the occurrence of multiple queens in the same colony (polygyny) alter patterns of relatedness within societies of eusocial insects. This is predicted to influence kin-selected conflicts over reproduction. We investigated the mating system of a facultatively polygynous UK population of the ant Leptothorax acervorum using up to six microsatellite loci. We estimated mating frequency by genotyping 79 dealate (colony) queens and the contents of their sperm receptacles and by detailed genetic analysis of 11 monogynous (single-queen) and nine polygynous colonies. Results indicated that 95% of queens were singly mated and 5% of queens were doubly mated. The corrected population mean mating frequency was 1.06. Parentage analysis of adults and brood in 17 colonies (10 monogynous, 7 polygynous) showed that female offspring attributable to each of 31 queens were full sisters, confirming that queens typically mate once. Inbreeding coefficients, queen-mate relatedness of zero and the low incidence of diploid males provided evidence that L. acervorum sexuals mate entirely or almost entirely at random. Males mated to queens in the same polygynous colony were not related to one another. Our data also confirmed that polygynous colonies contain queens that are related on average and that their workers had a mixed maternity. We conclude that the mating system of L. acervorum involves queens that mate near nests with unrelated males and then seek readoption by those nests, and queens that mate in mating aggregations away from nests, also with unrelated males.     

Colony sex ratios vary with breeding system but not relatedness asymmetry in the facultatively polygynous ant Pheidole pallidula

Abstract.— We investigated sex allocation in a Mediterranean population of the facultatively polygynous (multiple queen per colony) ant Pheidole pallidula . This species shows a strong split sex ratio, with most colonies producing almost exclusively a single-sex brood. Our genetic (microsatellite) analyses reveal that P. pallidula has an unusual breeding system, with colonies being headed by a single or a few unrelated queens. As expected in such a breeding system, our results show no variation in relatedness asymmetry between monogynous (single queen per colony) and polygynous colonies. Nevertheless, sex allocation was tightly associated with the breeding structure, with monogynous colonies producing a male-biased brood and polygynous colonies almost only females. In addition, sex allocation was closely correlated with colony total sexual productivity. Overall, our data show that when colonies become more productive (and presumably larger) they shift from monogyny to polygyny and from male production to female production, a pattern that has never been reported in social insects.     

Population structure and mating biology of the polygynous ponerine ant Gnamptogenys striatula in Brazil

Gnamptogenys striatula is a polygynous ponerine ant, whose colonies contain either several differentiated queens or several gamergates. Population structure, queen mating frequency and deviation from random mating were investigated in a north-eastern Brazilian population. Eight workers from each of 33 queenright colonies and 17 queens and their progeny (20-40 offspring) were genotyped using eight variable microsatellite markers. Population differentiation tests indicated limited gene flow at the scale of several kilometres, and tests of isolation by distance revealed population viscosity at the scale of a few metres. This population structure, together with the frequent colony migrations and fissions observed in the field, suggest that new nests are founded by budding in G. striatula. Genetic data showed that 13 of our 17 queens were single-mated and four were double-mated. The estimation of the range of maximal frequency of double-mated queens in the population was 0.232-0.259, demonstrating that mating frequency is low in G. striatula. The low estimated mean relatedness between the 17 queens and their mates (-0. 04 +/- 0.49) indicated no evidence of inbreeding in G. striatula.     

Colony kin structure and breeding system in the ant genus Plagiolepis

Relatedness is a central parameter in the evolution of sociality, because kin selection theory assumes that individuals involved in altruistic interactions are related. At least three reproductive characteristics are known to profoundly affect colony kin structure in social insects: the number of reproductive queens per colony, the relatedness among breeding queens and queen mating frequency. Both the occurrence of multiple queens (polygyny) and multiple mating (polyandry) decrease within-colony relatedness, while mating among sibs increases relatedness between the workers and the brood they rear. Using DNA microsatellites, we performed a detailed genetic analysis of the colony kin structure and breeding system in three ant species belonging to the genus Plagiolepis: P. schmitzii, P. taurica and P. maura. Our data show that queens of the three species mate multiply: queens of P. maura mate with 1-2 males, queens of P. taurica with 3-11 males and queens of P. schmitzii may have 1-14 different mates. Moreover, colonies are headed by multiple queens: P. taurica and P. maura are facultatively polygynous, while P. schmitzii is obligately polygynous. Despite polyandry and polygyny, relatedness within colonies remains high because all species are characterized by sib-mating, with a fixation index F(it) = 0.25 in P. taurica, 0.24 in P. schmitzii and 0.26 in P. maura, and because the male mates of a queen are on average closely related.     

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.     

The polygamous mating system of the sea spider Achelia simplissima

Most species of pycnogonids are sexually dimorphic and all have exclusive male care of the offspring, characteristics that make them essential for studies on sex-roles, sexual selection, and parental investment. However, sea spiders have been understudied because of their small size, cryptic coloration, and often patchy distribution, and little is known about their courtship and mating behaviors. The mating habits of both male and female Achelia simplissima (Hilton 1939) were studied experimentally and observationally. This species mates year-round and females commonly initiate courtship by actively ‘pumping’ their bodies near a male. When both nonparental and parental males were present, females mated significantly more often with males that were not carrying egg masses. Each mating event resulted in a single egg mass. Most often, males placed the first egg mass on their right oviger and then alternated between ovigers with subsequent matings. The newest (least developed) egg mass was always placed at the tip of the oviger. Both males and females routinely mated multiple times and had multiple mates; in the field, males were found carrying up to twelve egg masses simultaneously. This is the first experimental study to describe both the male and female mating system of a pycnogonid, and the first observations of courtship and mating for any species with the ammotheid type of ovigers.     

A new interpretation of the social organization and mating system of the Callitrichidae

Tamarins and marmosets are usually described as monogamous, or as living in extended family groups. Field research on a variety of callitrichid species shows, however, that immigration and emigration by adults are common and that groups are likely to be composed largely of unrelated adults of both sexes. Despite the number of adult females present in a group, only a single female is usually reproductively active. This female may mate with more than one male. Care for the young is provided by all group members but principally by adult males. This generally is referred to as a “communal breeding system. ” However, a vertebrate social system in which more than two reproductively active adults participate in infant care is rare and has otherwise been reported only in a small number of avian and canid species. Wild callitrichid groups virtually always include helpers, but the number of adults of each sex is highly variable. We propose that the Callitrichidae tend to live in small multimalemultifemale groups, communally rear the young of one female, and exhibit a mating pattern characterized by female promiscuity but a breeding system that is functionally polyandrous. There is a significant correlation between the number of males and a group and the total number of surviving young. The possible adaptive advantages of this social organization are discussed. An erratum to this article is available at .     

Asymmetric assortative mating and queen polyandry are linked to a supergene controlling ant social organization

Nonrecombining genomic variants underlie spectacular social polymorphisms, from bird mating systems to ant social organization. Because these “social supergenes” affect multiple phenotypic traits linked to survival and reproduction, explaining their persistence remains a substantial challenge. Here, we investigate how large nonrecombining genomic variants relate to colony social organization, mating system and dispersal in the Alpine silver ant, Formica selysi. The species has colonies headed by a single queen (monogynous) and colonies headed by multiple queens (polygynous). We confirmed that a supergene with alternate haplotypes—Sm and Sp—underlies this polymorphism in social structure: Females from mature monogynous colonies had the Sm/Sm genotype, while those from polygynous colonies were Sm/Sp and Sp/Sp. Queens heading monogynous colonies were exclusively mated with Sm males. In contrast, queens heading polygynous colonies were mated with Sp males and Sm males. Sm males, which are only produced by monogynous colonies, accounted for 22.9% of the matings with queens from mature polygynous colonies. This asymmetry between social forms in the degree of assortative mating generates unidirectional male‐mediated gene flow from the monogynous to the polygynous social form. Biased gene flow was confirmed by a significantly higher number of private alleles in the polygynous social form. Moreover, heterozygous queens were three times as likely as homozygous queens to be multiply mated. This study reveals that the supergene variants jointly affect social organization and multiple components of the mating system that alter the transmission of the variants and thus influence the dynamics of the system.     

The role of breeding system on ant ecological dominance: genetic analysis of Ectatomma tuberculatum

Social insects exhibit a great variability in their social organization,and this affects colony kin structure, relatedness among nestmates, and population genetic structure. In the mosaic of arborealants of neotropical habitats, mutually exclusive dominant antspecies occupy different territories, and their nest distributionis spatially aggregated in patches influencing patterns of populationgenetic structure. In this study, we performed an analysis ofthe population and colony genetic structure of the facultativepolygynous ant Ectatomma tuberculatum to investigate how theparticular breeding and social system of this species can explainits ecological dominance in the mosaic. Within-nest geneticanalysis revealed that relatedness between nest mate workerswas significantly greater than zero (r = 0.30) with an effectivenumber of queens per nest of Ne = 2.5–3, indicating thatpolygyny is functional in this species. Moreover, we found thatqueen number was highly variable, probably due to queen adoptionevents, leading to the prevalence of polygyny over monogyny.Finally, the strong population genetic structure and the significantisolation by distance suggested that both budding and polydomytake place in this species. The respective role of secondarypolygyny, budding, and polydomy are then discussed in the contextof the mosaic of arboreal ants, and we propose that this particularsocial organization ensures the ecological dominance of E. tuberculatumby optimizing the colonization of new available nesting sitesand by increasing territory size.     

Breeding system, colony structure, and genetic differentiation in the Camponotus festinatus species complex of carpenter ants

All social insects live in highly organized societies. However, different social insect species display striking variation in social structure. This variation can significantly affect the genetic structure within populations and, consequently, the divergence between species. The purpose of this study was to determine if variation in social structure was associated with species diversification in the Camponotus festinatus desert carpenter ant species complex. We used polymorphic DNA microsatellite markers to dissect the breeding system of these ants and to determine if distinct C. festinatus forms hybridized in their natural range. Our analysis of single-queen colonies established in the laboratory revealed that queens typically mated with only a single male. The genotypes of workers sampled from a field population suggested that multiple, related queens occasionally reproduced within colonies and that colonies inhabited multiple nests. Camponotus festinatus workers derived from colonies of the same form originating at different locales were strongly differentiated, suggesting that gene flow was geographically restricted. Overall, our data indicate that C. festinatus populations are highly structured. Distinct C. festinatus forms possess similar social systems but are genetically isolated. Consequently, our data suggest that diversification in the C. festinatus species complex is not necessarily associated with a shift in social structure.     

Contrasting population genetic structure for workers and queens in the putatively unicolonial ant Formica exsecta

The theory of inclusive fitness provides a powerful explanation for reproductive altruism in social insects, whereby workers gain inclusive fitness benefit by rearing the brood of related queens. Some ant species, however, have unicolonial population structures where multiple nests, each containing numerous queens, are interconnected and individuals move freely between nests. In such cases, nestmate relatedness values may often be indistinguishable from zero, which is problematic for inclusive fitness-based explanations of reproductive altruism. We conducted a detailed population genetic study in the polygynous ant Formica exsecta, which has been suggested to form unicolonial populations in its native habitat. Analyses based on adult workers indeed confirmed a genetic structuring consistent with a unicolonial population structure. However, at the population level the genetic structuring inferred from worker pupae was not consistent with a unicolonial population structure, but rather suggested a multicolonial population structure of extended family-based nests. These contrasting patterns suggest limited queen dispersal and free adult worker dispersal. That workers indeed disperse as adults was confirmed by mark-recapture measures showing consistent worker movement between nests. Together, these findings describe a new form of social organization, which possibly also characterizes other ant species forming unicolonial populations in their native habitats. Moreover, the genetic analyses also revealed that while worker nestmate relatedness was indistinguishable from zero at a small geographical scale, it was significantly positive at the population level. This highlights the need to consider the relevant geographical scale when investigating the role of inclusive fitness as a selective force maintaining reproductive altruism.     

Internest sex-ratio variation and male brood survival in the ant Pheidole pallidula

Sex allocation in social insects has become a general modelin tests of inclusive fitness theory, sex-ratio theory, andparent-offspring conflict. Several studies have shown that colonysex ratios are often bimodally distributed, with some coloniesproducing mainly females and others mainly males. Sex specializationmay result from workers assessing their relatedness to malebrood versus female brood, relative to the average worker-relatednessasymmetry in other colonies of their population. Workers thenadjust the sex ratio in their own interest This hypothesis assumesthat workers can recognize the sex of the brood in their colonyand selectively eliminate males. We compared the primary sexratio (at the egg stage) and secondary sex ratio (reproductivepupae and adults) of colonies in the ant Pheidole pallidula.There was a strong bimodal distribution of secondary sex ratios,with most colonies producing mainly reproductives of one sex.In contrast, there was no evidence of a bimodal distributionof primary sex ratios. The proportion of haploid eggs producedby queens was 0.35 in early spring and decreased to about 0.1in summer. Male eggs also were present in virtually all fieldcolonies sampled in July, although eggs laid at this time ofyear never give rise to males. All male brood is, therefore,selectively eliminated beginning in July and continue to beeliminated through the rest of the year. Finally, the populationsex-ratio investment was female-biased. Together, these resultsare consistent with the hypothesis that workers control thesecondary sex ratio by selectively eliminating male brood inabout half the colonies, perhaps those with high relatednessasymmetry.[Behav Ecol 7: 292–298 (1996)]     

Social and genetic characteristics of geographically isolated populations in the ant Formica cinerea

The ant Formica cinerea in northern Europe has geographically isolated populations that were examined using five microsatellite loci. The populations differ widely regarding the social organization of colonies. Based on genetic relatedness (r) among worker nest mates, the populations were classified as M type with monogynous (single queen) colonies (r > 0.59), as P type with polygynous colonial networks (r < 0.1), or as intermediate with weakly polygynous colonies (0.16 < r < 0.47). The social types showed weak geographical clustering, but the overall distribution indicated that the shift between the social types has occurred several times. The geographically isolated populations had slightly reduced levels of genetic diversity compared to populations from areas where the species is abundant and continuously distributed. Many of the isolated populations consisted of monogynous or weakly polygynous colonies, making their effective population sizes small, and some of them also showed weak bottleneck effects. The overall level of microsatellite diversity within populations was relatively high and differentiation among populations low, indicating recent connections. Isolation of populations may thus be a new phenomenon resulting from reduction of suitable habitats. At the local level, we obtained limited support from a group of nearby subpopulations in southern Finland to the hypothesis that the P type is connected to restricted dispersal. Other P type populations did not, however, show similar elevated levels of differentiation.     

Thin-layer chromatographic isolation of the trall pheromone of the ant Pheidole pallidula

Abstract. Although the presence of small amounts of 3-ethyl-2,5-dimethylpyrazine (EDMP) has been reported in the poison gland of the Pheidole pallidula minor workers, this substance is not the true trail pheromone of this ant. This pyrazine acts as an attractant and a locostimulant. Appropriate solvent extractions and thin-layer chromatography of poison glands, together with trail bioassays, have shown that another substance acts as the trail pheromone. Furthermore, there seems to be an auxiliary pheromone, acting as a synergist; this might be EDMP.     

How brood influences caste aggregation patterns in the dimorphic ant species Pheidole pallidula

Spatial distribution of ant workers and, notably their aggregation/segregation behaviour, is a key-element of the colony social organization contributing to the efficiency of task performance and division of labour. In polymorphic species, specialized worker castes notably differ in their intrinsic aggregation behaviour. In this context, knowing the preponderant role of minors in brood care, we investigate how a stimulus such as brood can influence the spatial patterns of Pheidole pallidula worker castes. In a homogeneous area without brood, it was shown that minors display only a low level of aggregation while majors form large clusters in the central area. Here we find out that these aggregation patterns of both minors and majors can be deeply influenced by the presence of brood. For minors, it nucleates or enhances the formation of a large stable cluster. Such high sensitivity of minors to brood stimuli fits well with their role as main brood tenders in the colony. For majors, interattraction between individuals still remains the prevailing aggregation factor while brood strongly influences the localisation of their cluster. We discuss how the balance between interattraction and sensitivity to environmental stimuli determines the mobility of each worker castes and, consequently, the availability of minors and majors to participate in everyday colony tasks. Moreover, we will evoke the functional value of majors’ cluster location close to the brood, namely with respect to social regulation of the colony caste ratio. Received 30 May 2005; revised 11 January 2006; accepted 13 January 2006.     

Predatory abilities favour the success of the invasive ant Pheidole megacephala in an introduced area

Abstract:  The invasive African big-headed ant, Pheidole megacephala , is a dominant species in the many areas it has invaded. We examined whether one potential reason for its ecological success might be its predatory efficiency. We compared the density of termite nests in an area of Mexico invaded by P. megacephala with an adjacent area where P. megacephala is not present. We also compared the success of P. megacephala in preying on termites with that of 13 native ant species. We found that termite nest density was significantly lower in areas invaded by P. megacephala (0.33 vs. 1.05 nests per 30 m transect). In field trials, we established that P. megacephala workers were significantly more successful at capturing termite workers from termite nest fragments than even the most successful native ant species, Dorymyrmex pyramicus . For both P. megacephala and D. pyramicus , single scouts could trigger the mass recruitment of nestmates, but P. megacephala was able to recruit greater numbers of nestmates. Combined with their aggressiveness towards other ant species, their highly efficient predatory capacities help explain the ecological success of P. megacephala and demonstrate how it can be a major threat to invertebrate biodiversity in the areas it invades.     

Multiple mating and supercoloniality in Cataglyphis desert ants

In social organisms, the breeding system corresponds to the number of breeders in a group, their genetic relationships, and the distribution of reproduction among them. Recent, genetically based studies suggest an amazing array of breeding system and reproductive strategies in desert ants of the genus Cataglyphis. Using highly polymorphic DNA microsatellites, we performed a detailed analysis of the breeding system and population genetic structure of two Cataglyphis species belonging to the same phylogenetic group: C. niger and C. savignyi. Our results show that both species present very different breeding systems. C. savignyi colonies are headed by a single queen and populations are multicolonial. Remarkably, queens show one of the highest mating frequency reported in ants (M_p = 9.25). Workers can reproduce by both arrhenotokous and thelytokous parthenogenesis. By contrast, colonies of C. niger are headed by several, multiply mated queens (M_p = 5.17), and they are organized in supercolonial populations made of numerous interconnected nests. Workers lay arrhenotokous eggs only. These results illustrate the high variability in the socio‐genetic organization that evolved in desert ants of the genus Cataglyphis. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 866–876.