Facultative use of thelytokous parthenogenesis for queen production in the polyandrous ant Cataglyphis cursor

The evolutionary paradox of sex remains one of the major debates in evolutionary biology. The study of species capable of both sexual and asexual reproduction can elucidate factors important in the evolution of sex. One such species is the ant Cataglyphis cursor, where the queen maximizes the transmission of her genes by producing new queens (gynes) asexually while simultaneously maintaining a genetically diverse workforce via the sexual production of workers. We show that the queen can also produce gynes sexually and may do so to offset the costs of asexual reproduction. We genotyped 235 gynes from 18 colonies and found that half were sexually produced. A few colonies contained both sexually and asexually produced gynes. Although workers in this species can also use thelytoky, we found no evidence of worker production of gynes based on genotypes of 471 workers from the six colonies producing sexual gynes. Gynes are thus mainly, and potentially exclusively, produced by the queen. Simulations of gynes inbreeding level following one to ten generations of automictic thelytoky suggest that the queen switches between or combines thelytoky and sex, which may reduce the costs of inbreeding. This is supported by the relatively small size of inbred gynes in one colony, although we found no relationship between the level of inbreeding and immune parameters. Such facultative use of sex and thelytoky by individual queens contrasts with other known forms of parthenogenesis in ants, which are typically characterized by distinct lineages specializing in one strategy or the other.     

Facultative sexual reproduction in the parthenogenetic ant Platythyrea punctata

Summary. In a few, scattered species of social Hymenoptera, unmated workers are capable of producing female offspring from unfertilized eggs through thelytokous parthenogenesis. Regular thelytoky has previously been demonstrated in a number of populations of the neotropical ant Platythyrea punctata. Nevertheless, the finding of males and inseminated queens and workers suggested the sporadic occurrence of sex. In this study we investigated the genetic structure of colonies from Puerto Rico and Costa Rica in order to detect traces of occasional sexual reproduction. Most Puerto Rican colonies had a clonal structure with all nestmates sharing the same multilocus genotype, indicating that thelytoky is the predominant mode of reproduction. Genetic variability was detected in six of 18 colonies and might have arisen from adoption of alien workers in one colony and from the adoption of alien workers, recombination during parthenogenesis, or sexual reproduction in the other colonies. The reproductive of one of these latter colonies was found to be an inseminated worker (gamergate), and the genotypes of its nestmates definitively suggested recombination and sexual reproduction. Three gamergates were found in a single colony collected in Costa Rica, and all produced offspring from fertilized eggs, while uninseminated workers were apparently incapable of reproducing by thelytoky.Received 10 August 2004; revised 20 October 2004; accepted 3 November 2004.     

Nutritional versus genetic correlates of caste differentiation in a desert ant

1. In many ant species, caste differentiation stems from trophic differences at the larval stage. Adult workers that feed larvae have great control over the allocation of colony resources to growth (production of workers) versus reproduction (production of queens). However, larval caste fate may also be constrained very early on through direct genetic effects or non‐genetic maternal effects. 2. Here, we combined isotopic and genetic analyses to study the developmental origin of queens and workers in a desert‐dwelling ant, Cataglyphis tartessica (Amor & Ortega, 2014). Queens do not found new colonies alone but rather disperse with workers. As the latter are always wingless, selection pressures on specific queen traits such as flight ability have become relaxed. Though the phylogenetically related species, C. emmae (Forel, 1909) only produces winged queens much larger than workers, C. tartessica produces two types of small queens relative to workers: brachypterous (short‐winged) queens and permanently apterous ergatoid (wingless and worker‐like) queens. 3. Upon emergence, workers and ergatoids have similar δ15N isotopic values, which were lower than those of brachypters, suggesting the latter are fed more protein as larvae. Microsatellite analyses indicated that: (i) colonies are mostly monogynous and monandrous; (ii) both ergatoids and brachypters are equally related to workers; and (iii) in the few polyandrous colonies, patrilines were evenly represented across workers, brachypters and ergatoids. 4. Overall, there was no evidence of genetic caste determination. We suggest that, in contrast to brachypters, ergatoids are selfish individuals that escape the nutritional castration carried out by workers and develop into queens in spite of the colony's collective interests.     

Mechanism of facultative parthenogenesis in the ant <Emphasis Type="Italic">Platythyrea punctata</Emphasis>

Thelytokous parthenogenesis, the production of diploid female offspring from unfertilized eggs, can be caused by several cytological mechanisms, which have a different impact on the genetic variation on the offspring. The ponerine ant Platythyrea punctata is widely distributed throughout the Caribbean Islands and Central America and exhibits facultative parthenogenesis. Workers in many field colonies from the Caribbean Islands have identical multilocus genotypes and are thus probably clonal, but the occurrence of males makes an ameiotic mechanism of thelytoky unlikely. To clarify the details of thelytoky in this species we compared the multilocus genotypes of mothers and their offspring in experimental colonies and analyzed the genotypes of haploid and diploid males. Additionally, we screened a large number of field colonies from thelytokous populations for the occurrence of recombination events. According to these data, automixis with central fusion and a reduced recombination rate is the most likely mechanism of thelytoky, as in the Cape honeybee and the ant Cataglyphis cursor.     

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.     

Variation in patriline reproductive success during queen production in orphaned colonies of the thelytokous ant Cataglyphis cursor

In genetically diverse insect societies (polygynous or polyandrous queens), the production of new queens can set the ground for competition among lineages. This competition can be very intense when workers can reproduce using thelytoky as worker lineages that manage to produce new queens gain a huge benefit. Selection at the individual level might then lead to the evolution of cheating genotypes, i.e. genotypes that reproduce more than their fair share. We studied the variation in reproductive success among worker patrilines in the thelytokous and highly polyandrous ant Cataglyphis cursor. Workers produce new queens by thelytoky in orphaned colonies. The reproductive success of each patriline was assessed in 13 orphaned colonies using genetic analysis of 433 workers and 326 worker-produced queens. Our results show that patrilines contributed unequally to queen production in half of the colonies, and the success of patrilines was function of their frequencies in workers. However, over all colonies, we observed a significant difference in the distribution of patrilines between workers and worker-produced queens, and this difference was significant in three of 13 colonies. In addition, six colonies contained a low percentage of foreign workers (drifters), and in one colony, they produced a disproportionably high number of queens. Hence, we found some evidence for the occurrence of rare cheating genotypes. Nevertheless, cheating appears to be less pronounced than in the Cape Honey bee, a species with a similar reproductive system. We argue that worker reproduction by parthenogenesis might not be common in natural populations of C. cursor.     

Sex at the margins: parthenogenesis vs. facultative and obligate sex in a Neotropical ant

Geographic parthenogenesis is a distribution pattern, in which parthenogenetic populations tend to live in marginal habitats, at higher latitudes and altitudes and island‐like habitats compared with the sexual forms. The facultatively parthenogenetic ant Platythyrea punctata is thought to exhibit this general pattern throughout its wide range in Central America and the Caribbean Islands. Workers of P. punctata from the Caribbean produce diploid female offspring from unfertilized eggs by thelytokous parthenogenesis, and mated females and males are rare. In contrast, workers in one colony from Costa Rica were incapable of thelytoky; instead mated workers produced all female offspring. Because sample sizes were very low in former studies, we here use microsatellite markers and explicit tests of thelytoky to examine the population genetic structure of ancestral and derived populations of P. punctata throughout the Caribbean and Central America. Populations from the Caribbean islands were fully capable of parthenogenesis, and population genetic signatures indicate that this is the predominant mode of reproduction, although males are occasionally produced. In contrast, the northernmost population on the mainland (Texas) showed signatures of sexual reproduction, and individuals were incapable of reproduction by thelytoky. Contrary to expectations from a geographic parthenogenesis distribution pattern, most parts of the mainland populations were found to be facultatively thelytokous, with population genetic signatures of both sexual and parthenogenetic reproduction.     

An unusual ant diet:Cataglyphis floricola feeding on petals

Summary C. floricola is an endemic species from the southern Iberian Peninsula which collects large amounts ofHalimium halimifolium petals. Laboratory and field observations confirm that both workers and larvae feed on these petals, which represent an important food resource forC. floricola colonies. This petal consumption is a very unusual ant diet.     

Nest-moving by the polydomous ant <Emphasis Type="Italic">Cataglyphis iberica</Emphasis>

In this paper we analyze emigration from nests by the polydomous ant Cataglyphis iberica. Social carrying of workers of this species between different nests of the colony is frequent. In Bellaterra (Barcelona, NE Spain), we monitored field emigration of C. iberica by noting for each nest the migratory behavior of C. iberica workers and, when the nests were attacked by another ant species, Camponotus foreli, we noted the number of C. foreli workers involved in the attacks. Emigration of C. iberica from nests was highly variable. We suggest the main factor determining emigration by this species was attack by workers of C. foreli, so emigration from C. iberica nests was much faster when harassment by C. foreli increased. The system of multiple nests of C. iberica enables this species to abandon attacked nests and to reinstall their population in other nests of the same colony. This reduces risk to the colonies because the route between the different nests is well known by transporter workers.     

Hybridogenesis through thelytokous parthenogenesis in two Cataglyphis desert ants

Hybridogenesis is a sexual reproductive system, whereby parents from different genetic origin hybridize. Both the maternal and paternal genomes are expressed in somatic tissues, but the paternal genome is systematically excluded from the germ line, which is therefore purely maternal. Recently, a unique case of hybridogenesis at a social level was reported in the desert ant Cataglyphis hispanica. All workers are sexually produced hybridogens, whereas sexual forms (new queens and males) are produced by queens through parthenogenesis. Thus, only maternal genes are perpetuated across generations. Here, we show that such an unusual reproductive strategy also evolved in two other species of Cataglyphis belonging to the same phylogenetic group, Cataglyphis velox and Cataglyphis mauritanica. In both species, queens mate exclusively with males originating from a different genetic lineage than their own to produce hybrid workers, while they use parthenogenesis to produce the male and female reproductive castes. In contrast to single‐queen colonies of C. hispanica, colonies of C. velox and C. mauritanica are headed by several queens. Most queens within colonies share the same multilocus genotype and never transmit their mates' alleles to the reproductive castes. Social hybridogenesis in the desert ants has direct consequences on the genetic variability of populations and on caste determination. We also discuss the maintenance of this reproductive strategy within the genus Cataglyphis.     

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.     

Sexual and asexual colony foundation and the mechanism of facultative parthenogenesis in the termite <Emphasis Type="Italic">Reticulitermes speratus</Emphasis> (Isoptera,Rhinotermitidae)

Summary. Facultative parthenogenesis has great adaptive significance, especially with regard to low pairing efficiency. In the termite Reticulitermes speratus, females that fail to mate with males reproduce parthenogenetically and found colonies cooperatively with partner females or even alone. Comparison of colony foundation success at 400 days between colonies founded by single females (F), female-female pairs (FF), and male-female pairs (FM) showed that female-female cooperation promoted colony survivorship over monogamous foundation. We report here for the first time the mode of parthenogenesis in Isoptera. Combining chromosome observations and genetic analysis using microsatellites, we show that the mode of parthenogenesis is diploid thelytoky and that the restoration of ploidy is most likely accomplished by terminal fusion. Parthenogens show a higher mortality and a longer egg-development time than sexually produced offspring, probably due to reduced heterozygosity. In addition Wolbachia bacteria were detected in R. speratus. However, since Wolbachia was also detected in non-parthenogenetic R. flavipes, it is unlikely that Wolbachia is the cause of parthenogenesis in R. speratus.Received 30 October 2003; revised 4 March 2004; accepted 17 March 2004.     

Local resource competition and sex ratio in the ant Cataglyphis cursor

The local resource competition (LRC) hypothesis predicts thatwherever philopatric offspring compete for resources with theirmothers, offspring sex ratios should be biased in favor of thedispersing sex. In ants, LRC is typically found in polygynous(multiple queen) species where foundation of new nests occursby budding, which results in a strong population structure anda male-biased population-wide sex ratio. However, under polygyny,the effect of LRC on sex allocation is often blurred by theeffect of lowered relatedness asymmetries among colony members.Moreover, environmental factors, such as the availability ofresources, have also been shown to deeply influence sex ratioin ants. We investigated sex allocation in the monogynous (singlequeen) ant Cataglyphis cursor, a species where colonies reproduceby budding and both male and female sexuals are produced throughparthenogenesis, so that between-colony variations in relatednessasymmetries should be reduced. Our results show that sex allocationin C. cursor is highly male biased both at the colony and populationlevels. Genetic analyses indicate a significant isolation-by-distancein the study population, consistent with limited dispersal offemales. As expected from asexual reproduction, only weak variationsin relatedness asymmetry of workers toward sexual offspringoccur across colonies, and they are not associated with colonysex ratio. Inconsistent with the predictions of the resourceavailability hypothesis, the male bias significantly increaseswith colony size, and investment in males, but not in females,is positively correlated with total investment in sexuals. Overall,our results are consistent with the predictions of the LRC hypothesisto account for sex ratio variation in this species.     

Thelytokous parthenogenesis in the exotic dacetine ant Strumigenys rogeri (Hymenoptera: Formicidae) in Taiwan

Only recently has it become clear that several species of eusocial hymenopterans regularly reproduce by thelytokous parthenogenesis, that is, the production of diploid female offspring by unmated females. This phenomenon suggests that parthenogenetic reproduction might be advantageous to organisms under certain environmental conditions. Here the occurrence of asexual reproduction is reported for the first time in the dacetine ant, Strumigenys rogeri, at least for the focal populations in Taiwan. Virgin queens of S. rogeri maintained with several workers produced both workers and young queens from unfertilized eggs under laboratory conditions in as short as 39 days, whereas workers were strictly sterile as no spermatheca was discovered after dissection. Combined with additional evidence (i.e. absence of males in field colonies), queen thelytoky is confirmed. Such a reproductive mode and short development time may jointly help explain the success of this tramp ant species in Taiwan and elsewhere.     

Social Organization of Cataglyphis cursor Ant Colonies (Hymenoptera,Formicidae): Inter-, and Intraspecific Comparisons

The social organization of several colonies of the ant Cataglyphis cursor with different compositions has been studied by means of individual marking of workers and later treatment of data with correspondence analysis. There are always three main poles or groups of tasks: inactivity, unspecific tasks in the nest and outside activities. From them, three groups of workers are separated: inactives, which stay immobile in the nest a great part of their time; interiors, which perform various tasks in the nest; and foragers, that are engaged in activities outside the nest. Several factors, such as the presence of the queen, the colony size or the season of the year influence the social structure of C. cursor colonies and originate important inter-, and intracolonial variations.     

Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits

In the Cape honeybee, Apis mellifera capensis, workers lay diploid(female) eggs via thelytoky. In other A. mellifera subspecies,workers lay haploid (male) eggs via arrhenotoky. When thelytokousworker reproduction occurs, worker policing has no relatednessbenefit because workers are equally related to their sisterworkers' clonal offspring and their mother queen's female offspring.We studied worker policing in A. m. capensis and in the arrhenotokousAfrican honeybee A. m. scutellata by quantifying the removalrates of worker-laid and queen-laid eggs. Discriminator coloniesof both subspecies policed worker-laid eggs of both their ownand the other subspecies. The occurrence of worker policing,despite the lack of relatedness benefit, in A. m. capensis stronglysuggests that worker reproduction is costly to the colony andthat policing is maintained because it enhances colony efficiency.In addition, because both subspecies policed each others eggs,it is probable that the mechanism used in thelytokous A. m.capensis to discriminate between queen-laid and worker-laideggs is the same as in arrhenotokous A. m. scutellata.     

Evolution of hybridogenetic lineages in Cataglyphis ants

In most social Hymenoptera, a diploid egg develops into either a queen or a worker depending on environmental conditions. Hybridogenetic Cataglyphis ants display a bizarre genetic system, where queen‐worker caste determination is primarily determined by genetic factors. In hybridogenetic populations, all workers are F1 hybrids of two distinct lineages, whereas new queens are nearly always pure‐lineage individuals produced by clonal reproduction. The distribution and evolutionary history of these hybridogenetic populations have not yet been thoroughly analysed. Here, we studied the phylogeographic distribution of hybridogenetic populations in two closely related Spanish species: Cataglyphis humeya and Cataglyphis velox. Hybridogenesis has been previously documented in a locality of C. velox, but whether this system occurs elsewhere within the range of the two species was yet unknown. Queens and workers from 66 localities sampled across the range of the species were genotyped at 18 microsatellite markers to determine whether queens were produced by parthenogenesis and whether workers were hybrids of divergent lineages. Populations with F1 hybrid workers were identified by combining genetic, geographical and mating assortments data. In most populations of C. velox, workers were found to be hybrids of two divergent lineages. Workers were however produced via random mating in two marginal populations of C. velox, and in all populations studied of its sister species C. humeya. High‐throughput sequencing data were obtained to confirm inferences based on microsatellites and to characterize relationships between populations. Our results revealed a complicated history of reticulate evolution that may account for the origin of hybridogenetic lineages in Cataglyphis.     

Mating system and population structure in the desert ant Cataglyphis livida

We investigated population genetic structure, mating system, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis livida. Pedigree analyses at polymorphic microsatellite loci show that colonies are headed by a single queen, and that queens are mated with two to eight males. No inbreeding was found in the population sampled. Colonies are genetically differentiated and exhibit no isolation-by-distance pattern, consistent with independent foundation of new colonies. Workers do reproduce and lay haploid (arrhenotokous) eggs in queenless colonies; conversely, we found no evidence of worker reproduction in queenright nests. In contrast with C. cursor, where new queens are produced by thelytokous parthenogenesis, female sexuals and workers of C. livida arise from classical sexual reproduction. We discuss the parallels and contrasts between the mating system and population structure in C. livida and the other Cataglyphis species studied so far.     

Queen–worker caste ratio depends on colony size in the pharaoh ant (<Emphasis Type="Italic">Monomorium pharaonis</Emphasis>)

The success of an ant colony depends on the simultaneous presence of reproducing queens and non-reproducing workers in a ratio that will maximize colony growth and reproduction. Despite its presumably crucial role, queen–worker caste ratios (the ratio of adult queens to workers) and the factors affecting this variable remain scarcely studied. Maintaining polygynous pharaoh ant (Monomorium pharaonis) colonies in the laboratory has provided us with the opportunity to experimentally manipulate colony size, one of the key factors that can be expected to affect colony level queen–worker caste ratios and body size of eclosing workers, gynes and males. We found that smaller colonies produced more new queens relative to workers, and that these queens and workers both tended to be larger. However, colony size had no effect on the size of males or on the sex ratio of the individuals reared. Furthermore, for the first time in a social insect, we confirmed the general life history prediction by Smith and Fretwell (Am Nat 108:499–506, 1974) that offspring number varies more than offspring size. Our findings document a high level of plasticity in energy allocation toward female castes and suggest that polygynous species with budding colonies may adaptively adjust caste ratios to ensure rapid growth.     

Inheritance of thelytoky in the honey bee Apis mellifera capensis

Asexual reproduction via thelytokous parthenogenesis is widespread in the Hymenoptera, but its genetic underpinnings have been described only twice. In the wasp Lysiphlebus fabarum and the Cape honey bee Apis mellifera capensis the origin of thelytoky have each been traced to a single recessive locus. In the Cape honey bee it has been argued that thelytoky (th) controls the thelytoky phenotype and that a deletion of 9 bp in the flanking intron downstream of exon 5 (tae) of the gemini gene switches parthenogenesis from arrhenotoky to thelytoky. To further explore the mode of inheritance of thelytoky, we generated reciprocal backcrosses between thelytokous A. m. capensis and the arrhenotokous A. m. scutellata. Ten genetic markers were used to identify 108 thelytokously produced offspring and 225 arrhenotokously produced offspring from 14 colonies. Patterns of appearance of thelytokous parthenogenesis were inconsistent with a single locus, either th or tae, controlling thelytoky. We further show that the 9 bp deletion is present in the arrhenotokous A. m. scutellata population in South Africa, in A. m. intermissa in Morocco and in Africanized bees from Brazil and Texas, USA, where thelytoky has not been reported. Thus the 9 bp deletion cannot be the cause of thelytoky. Further, we found two novel tae alleles. One contains the previously described 9 bp deletion and an additional deletion of 7 bp nearby. The second carries a single base insertion with respect to the wild type. Our data are consistent with the putative th locus increasing reproductive capacity.