Colony demographics of rare soldier-polymorphic worker caste systems in <Emphasis Type="Italic">Pheidole</Emphasis> ants (Hymenoptera,Formicidae)

Nearly all species in the ant genus Pheidole have dimorphic workers, with distinct small minors and larger soldiers. The size range of both castes is typically narrow. Just seven described species are soldier-polymorphic, with a broad soldier size range. Here, we characterize worker caste allocation and demography in the soldier-polymorphic P. obtusospinosa, P. rhea, and P. tepicana, and the dimorphic P. spadonia for comparison. The head allometry of soldiers in soldier-polymorphic species is strongly positive and that of dimorphic species is negative. Among soldier-polymorphic species, the soldier castes differ from each other in the degree of positive allometry. In addition, they differ in the number of size modes: P. obtusospinosa and P. rhea have two and P. tepicana has one. During colony ontogeny, P. obtusospinosa first has one mode and develops the second mode much later, while P. rhea produces multiple modes throughout. We also characterize worker caste systems based on the biomass allocation. For all three soldier-polymorphic species, the majority of soldiers are small soldiers. Pheidole obtusospinosa and P. rhea allocate roughly equal biomass to the two soldier classes, while P. tepicana allocates little to supersoldiers based on both biomass and caste ratio. These findings illustrate the interplay among caste ratios, biomass allocation, size frequency distributions, and allometry in the evolution of different worker caste systems. We conclude that soldier-polymorphic species may have evolved convergently in response to broad-scale factors, but differences among them suggest selection pressures in small-scale environments have been different.     

Skewed soldier sex ratio in termites: testing the size-threshold hypothesis

Social insect colonies contain multiple phenotypes, i.e. castes, and this caste polyphenism is often linked to sexual dimorphism. Unlike social hymenopterans, both termite sexes are diploid and contribute to helper-type tasks within the colony. Nonetheless, a biased sex ratio is frequently observed in termites, especially in soldiers. To explain this bias in soldier sex ratio, Matsuura (Evol. Ecol. 20: 565–574, 2006) postulated the existence of a size threshold for workers molting into soldiers. Under the influence of sexual size dimorphism (SSD), such a threshold was considered to indirectly favor one sex. We conducted a literature survey of sex ratio among termite soldiers and tested this size-threshold hypothesis using data for 67 termite species from a variety of termite lineages. We demonstrated the existence of a size threshold for individuals molting into soldiers, resulting in the acquisition of soldiers of only one sex in species exhibiting strong SSD. In species exhibiting weak SSD, the size threshold skews the sex ratio of soldiers, but does not necessarily cause the loss of one sex. Finally, we observed a prevalence of single-sex soldiers in the Termitidae, regardless of SSD, suggesting that the ancestral developmental mechanisms that constrain soldier differentiation from one sex are maintained in certain extant species.     

Correlates of ecological dominance within Pheidole ants (Hymenoptera: Formicidae)

1. In any group of organisms, one can almost invariably find some species that are ecologically dominant (i.e. disproportionately more abundant and widespread), whereas others are comparatively less prevalent. Understanding of the causes of variation in ecological dominance has been elusive, particularly given that dominant and subordinate species often lack obvious features that could predict their abundance in nature. 2. In this study, physiological, behavioural, morphological, and phylogenetic information is integrated in an effort to understand the mechanisms underlying ecological dominance in ants using the hyperdiverse ant genus Pheidole (Formicidae: Myrmicinae) as a model system. Field estimates of the relative abundance of 10 Pheidole species were compared with potential correlates, which included behavioural (walking velocity), physiological (tolerance to high and low temperatures and desiccation), and morphological traits (body size and degree of dimorphism in the worker caste). A molecular phylogeny of the tested species was also generated to account for potential confounding effects of phylogenetic non‐independence. 3. Dominant Pheidole species were characterised by higher environmental tolerance with respect to temperature and humidity, as well as faster walking speeds. On the other hand, no morphological correlates of ecological dominance were detected. Interestingly, subordinate species showed no evidence of trade‐off in performance, being both more fragile to environmental challenges and slower in their walking speeds. 4. These results provide important insights into the mechanisms involved in local species coexistence in Pheidole.     

The Effect of Diet and Opponent Size on Aggressive Interactions Involving Caribbean Crazy Ants (Nylanderia fulva)

Biotic interactions are often important in the establishment and spread of invasive species. In particular, competition between introduced and native species can strongly influence the distribution and spread of exotic species and in some cases competition among introduced species can be important. The Caribbean crazy ant, Nylanderia fulva, was recently introduced to the Gulf Coast of Texas, and appears to be spreading inland. It has been hypothesized that competition with the red imported fire ant, Solenopsis invicta, may be an important factor in the spread of crazy ants. We investigated the potential of interspecific competition among these two introduced ants by measuring interspecific aggression between Caribbean crazy ant workers and workers of Solenopsis invicta. Specifically, we examined the effect of body size and diet on individual-level aggressive interactions among crazy ant workers and fire ants. We found that differences in diet did not alter interactions between crazy ant workers from different nests, but carbohydrate level did play an important role in antagonistic interactions with fire ants: crazy ants on low sugar diets were more aggressive and less likely to be killed in aggressive encounters with fire ants. We found that large fire ants engaged in fewer fights with crazy ants than small fire ants, but fire ant size affected neither fire ant nor crazy ant mortality. Overall, crazy ants experienced higher mortality than fire ants after aggressive encounters. Our findings suggest that fire ant workers might outcompete crazy ant workers on an individual level, providing some biotic resistance to crazy ant range expansion. However, this resistance may be overcome by crazy ants that have a restricted sugar intake, which may occur when crazy ants are excluded from resources by fire ants.     

Division of labor in the hyperdiverse ant genus Pheidole is associated with distinct subcaste- and age-related patterns of worker brain organization

The evolutionary success of ants and other social insects is considered to be intrinsically linked to division of labor among workers. The role of the brains of individual ants in generating division of labor, however, is poorly understood, as is the degree to which interspecific variation in worker social phenotypes is underscored by functional neurobiological differentiation. Here we demonstrate that dimorphic minor and major workers of different ages from three ecotypical species of the hyperdiverse ant genus Pheidole have distinct patterns of neuropil size variation. Brain subregions involved in sensory input (optic and antennal lobes), sensory integration, learning and memory (mushroom bodies), and motor functions (central body and subesophageal ganglion) vary significantly in relative size, reflecting differential investment in neuropils that likely regulate subcaste- and age-correlated task performance. Worker groups differ in brain size and display patterns of altered isometric and allometric subregion scaling that affect brain architecture independently of brain size variation. In particular, mushroom body size was positively correlated with task plasticity in the context of both age- and subcaste-related polyethism, providing strong, novel support that greater investment in this neuropil increases behavioral flexibility. Our findings reveal striking levels of developmental plasticity and evolutionary flexibility in Pheidole worker neuroanatomy, supporting the hypothesis that mosaic alterations of brain composition contribute to adaptive colony structure and interspecific variation in social organization.     

Community-level interactions and functional ecology of major workers in the hyperdiverse ground-foraging Pheidole (Hymenoptera, Formicidae) of Amazonian Ecuador

Ants of the genus Pheidole are abundant and hyperdiverse, particularly in Neotropical rainforests. Very little is known, however, about the degree of ecological and behavioral differentiation of coexisting species comprising Pheidole communities. Additionally, the ecological role of the major worker subcaste, thought to be significant to the diversification of Pheidole, is poorly understood. We investigated the ecology and behavior of a ground-foraging Pheidole community of at least 56 species in Amazonian Ecuador. Pheidole species differed strongly in tolerance to flooding, nest site usage, foraging range, major worker foraging, and control of baits, but not in daily activity or ability to discover baits. A molecular phylogeny based on mitochondrial DNA was characterized by poorly resolved basal relationships and long terminal branches, suggesting an ancient diversification of many Pheidole lineages. Comparison of well-supported sister species suggests that both phylogenetic history and ecologically induced differentiation contribute to interspecific variation in Amazonian Pheidole. Ground-nesting species had larger major workers than twig-nesting species, whereas dominant species with stronger recruitment had a higher proportional abundance of major workers at baits. Variation among species suggests the presence of behavioral groups within the Amazonian Pheidole community that appear to segregate according to nest site usage and/or tolerance to flooding disturbance. Our results suggest an important role for major worker differentiation in the diversification of Pheidole.     

Male or female soldiers? An evaluation of several factors which may influence soldier sex ratio in lower termites

In termites, the soldiers’ sex ratio is often biased toward one sex. Unlike in the Hymenoptera, this bias cannot easily be explained by relatedness asymmetries because termites are diploid. Matsuura proposed that when large body size is adaptive for colony defence (e.g. in case of phragmotic defence) then the larger sex (given sexual size dimorphism exists) should be more likely to reach a threshold size and develop into soldiers. This would explain biased sex ratios. Matsuura validated his hypothesis for four Reticulitermes species. Here, we tested his hypothesis for two species of Cryptotermes with phragmotic defence. These drywood termites have a life type that is thought to be ancestral in termite’s evolution, thus giving us potential insights into the evolution of the soldier caste. In one of these species, the sex ratio of soldiers was highly female biased, but we could not support Matsuura’s hypothesis. Both species lacked sexual size dimorphism in all castes. Additionally, in both species, the sex ratio of helpers and sexuals did not deviate from a 1:1 ratio, and hence can also not account for the bias observed in soldiers. However, this study showed that there were behavioural differences between the sexes in both species, which could shed some light on biased sex ratio in soldiers. Our findings also indicate that the developmental pathway taken by individuals reflects a ‘decision’ at the colony level. The discovery of behavioural differences between sexes in termites should open the way to similar studies in other taxa with helpers/ workers of both sexes, as it might reveal more task partitioning in colonies than previously thought and it raises questions concerning the selective pressures that acted on caste evolution in termites. Received 30 October 2007; revised 17 January and 27 February; accepted 4 March 2008.     

Storage function and ultrastructure of the adult fat body in workers of the ant Camponotus festinatus (Buckley) (Hymenoptera : Formicidae)

The presence of storage proteins in ants is perhaps most remarkable in its abundance in some species in the adult stage. The ultrastructure of fat body in workers of Camponotus festinatus (Hymenoptera : Formicidae) confirms that they do indeed store large quantities of protein, as well as lipid and carbohydrate, under some conditions. Rounded electron-dense granules, which are abundant in workers maintained in groups isolated from the parent colony, probably contain an arylphorin-like protein. Irregularly shaped electron-dense granules present in all workers regardless of age, caste or social environment, resemble primarily lysosomes, but lack acid phosphatase activity. Peroxisomes were also identified but were not associated with either type of dense granule. Lipid analysis showed that lipid storage followed similar patterns to protein storage, with isolated workers, especially soldiers, accumulating huge quantities of triglycerides. The relationship between storage of nutrient reserves and the presence of larvae suggests that the stores may function in regulating seasonal brood production.     

Alarm-recruitment behaviour in Pheidole militicida (Hymenoptera: Formicidae)

ABSTRACT.

• 1 Pheidole militicida Wheeler, a seed-harvesting species of the southwestern United States, possesses a major worker caste (soldiers) with unusually large heads. Previous work suggested that these large major workers are specialized defenders against large seed-harvesting species in the genus Pogonomyrmex.
• 2 Experimental introductions of Pogonomyrmex maricopa Wheeler and the omnivorous fire ant, Solenopsis xyloni McCook, demonstrate that P. militicida colonies alarm-recruit major workers against S.xyloni workers but not against the larger Pogonomyrmex workers.
• 3 P.militicida is the second species in which enemy-specific defence against Solenopsis fire ants has been detected. I suggest that the special role of Solenopsis as both competitor and predator in ant communities frequently favours major worker specialization against this genus.
• 4 Major workers of P.militicida and Pheidole dentata Mayr, the other species with enemy-specific defence against Solenopsis, are morphologically very different from one another. It is suggested that interspecific variation in major worker morphology is not necessarily associated with variation in behavioural specialization.

     

Morphological differences between extranidal and intranidal workers in the ant Temnothorax rugatulus,but no effect of body size on foraging distance

Most ant genera are thought to have monomorphic workers, indicating perhaps a high degree of flexibility in task allocation, and the well-studied genus Temnothorax is an example of this. However, considerable size variation may exist between individuals. In addition, though workers can show flexible behavior, it has been shown that individuals may consistently differ in their task profiles. Here we test whether body size variation among workers affects foraging behavior. Two main hypotheses were tested: first, whether larger ants forage at greater distance from the nest, and second, whether larger individuals show a higher propensity to work outside of the nest. Our results showed that ant body size does not significantly affect foraging distance. However, larger ants were more likely to be found outside the nest. Though Temnothorax ants are a common model system, this is the first study demonstrating task allocation based on body size, which is fixed in adults. Our study suggests that particularly small species may have to be examined carefully for body size variation before concluding that body size is uniform and therefore irrelevant for task allocation.     

Bigger Helpers in the Ant Cataglyphis bombycina: Increased Worker Polymorphism or Novel Soldier Caste?

Introduction

The mechanisms by which development favors or constrains the evolution of new phenotypes are incompletely understood. Polyphenic species may benefit from developmental plasticity not only regarding ecological advantages, but also potential for evolutionary diversification. For instance, the repeated evolution of novel castes in ants may have been facilitated by the existence of alternative queen and worker castes and their respective developmental programs.

Material and Methods

Cataglyphis bombycina is exceptional in its genus because winged queens and size-polymorphic workers occur together with bigger individuals having saber-shaped mandibles. We measured seven body parts in more than 150 individuals to perform a morphometric analysis and assess the developmental origin of this novel phenotype.

Results

Adults with saber-shaped mandibles differ from both workers and queens regarding the size of most body parts. Their relative growth rates are identical to workers for some pairs of body parts, and identical to queens for other pairs of body parts; critical sizes differ in all cases.

Conclusions

Big individuals are a third caste, i.e. soldiers, not major workers. Novel traits such as elongated mandibles are combined with a mix of queen and worker growth rates. We also reveal the existence of a dimorphism in the queen caste (microgynes and macrogynes). We discuss how novel phenotypes can evolve more readily in the context of an existing polyphenism. Both morphological traits and growth rules from existing queen and worker castes can be recombined, hence mosaic phenotypes are more likely to be viable. In C. bombycina, such a mosaic phenotype appears to function both for defense (saber-shaped mandibles) and fat storage (big abdomen). Recycling of developmental programs may have contributed to the morphological diversity and ecological success of ants.     

A novel hypothesis for the origin of the sexual division of labor in termites: which sex should be soldiers?

Sexual specialization and skewed sex ratios of the altruistic castes, especially soldiers, are common in many termite taxa. However, no theoretical or empirical studies have explained the origin of the sexual division of labor in termites. In most termite species, female alates are larger than male alates, and mature queens are much larger than kings, with females under consistent selection for high fertility. Therefore, females usually have the potential to be larger than males. Here, I present a novel preadaptation hypothesis that potential sexual differences in the suitability for the caste give rise to the sexual division of labor, and I provide the first evidence in support of this hypothesis in termites. Defense in Reticulitermes is typically performed by soldiers via mandibular and phragmotic defense in which soldiers with pluglike heads block openings, thus preventing enemies from invading the nest. Phragmotic defense requires that soldiers have heads wide enough to plug nest openings. Therefore, a size threshold for workers that develop into soldiers is a likely adaptation for effective defense. I show that sexual size dimorphism (SSD) and a size threshold for soldiers promote skewed sex ratios. A female-biased soldier sex ratio was observed in species with SSD, whereas there was no bias in soldier sex ratio in species without SSD. Thus, SSD and soldier sex ratio data from several Reticulitermes species support the preadaptation hypothesis.     

A social ethogram of the neotropical arboreal ant Zacryptocerus varians (Fr. Smith)

An ethogram is presented of Zacryptocerus varians, a morphologically advanced member of the ‘turtle ants’ comprising the neotropical ant tribe Cephalotini. The species displays unusual and in one or two cases possibly even unique social behaviours, including the consumption and sharing of infrabuccal pellets, the apparent absence of adult transport, a primarily or exclusively mechanical form of colony defence, and a remarkable form of abdominal trophallaxis. All of these specializations seem to be associated with more primary adaptations by the species to arboreal nesting and scavenging. Among the additional results is the demonstration that the major worker is more specialized as a defensive caste than is the case in certain species of Camponotus and Pheidole.     

Flight muscle breakdown in the soldier caste of the gall-inducing thrips species, Kladothrips intermedius Bagnall

Within the gall-inducing thrips of Australia, genus Kladothrips, is a single origin of a soldier caste. A subsequent radiation has led to at least seven social species, and two species that are likely to have independently lost the soldier caste. Both losses of soldiers are connected to a shift in the insects’ host plant. A third inferred host shift is correlated with life history changes in a species with soldiers, K. intermedius, which might suggest this defensive caste may be in transition. The soldiers of this species have variable wing lengths that overlap with that of the flight-capable dispersers. Our study was designed to assess the possibility that some soldiers in this species retain the ability to disperse by wing. A morphological assessment shows that a proportion of soldiers have body dimensions and wing lengths that fall within the range of dispersers, with males more so than females. However, longer wing length in soldiers (sample of primarily females) did not correspond with a disperser like walking behaviour. Furthermore, histological sections suggest that wing muscles of soldiers are deteriorated or absent, which is similar to what was observed in their foundress mothers. The presence of long wings did not correspond with being flight capable in this caste.     

Save your host,save yourself? Caste‐ratio adjustment in a parasite with division of labor and snail host survival following shell damage

Shell damage and parasitic infections are frequent in gastropods, influencing key snail host life‐history traits such as survival, growth, and reproduction. However, their interactions and potential effects on hosts and parasites have never been tested. Host–parasite interactions are particularly interesting in the context of the recently discovered division of labor in trematodes infecting marine snails. Some species have colonies consisting of two different castes present at varying ratios; reproductive members and nonreproductive soldiers specialized in defending the colony. We assessed snail host survival, growth, and shell regeneration in interaction with infections by two trematode species, Philophthalmus sp. and Maritrema novaezealandense, following damage to the shell in the New Zealand mud snail Zeacumantus subcarinatus. We concomitantly assessed caste‐ratio adjustment between nonreproductive soldiers and reproductive members in colonies of the trematode Philophthalmus sp. in response to interspecific competition and shell damage to its snail host. Shell damage, but not parasitic infection, significantly increased snail mortality, likely due to secondary infections by pathogens. However, trematode infection and shell damage did not negatively affect shell regeneration or growth in Z. subcarinatus; infected snails actually produced more new shell than their uninfected counterparts. Both interspecific competition and shell damage to the snail host induced caste‐ratio adjustment in Philophthalmus sp. colonies. The proportion of nonreproductive soldiers increased in response to interspecific competition and host shell damage, likely to defend the parasite colony and potentially the snail host against increasing threats. These results indicate that secondary infections by pathogens following shell damage to snails both significantly increased snail mortality and induced caste‐ratio adjustments in parasites. This is the first evidence that parasites with a division of labor may be able to produce nonreproductive soldiers according to environmental factors other than interspecific competition with other parasites.     

Introduced Pheidole of the world: taxonomy,biology and distribution

The objective of this study is to provide a detailed taxonomic resource for identifying and studying ants in the genus Pheidole that have established beyond their native ranges. There is an increasing need for systematists to study taxa of specific concern to 21^st century environmental, food security and public health challenges. Systematics has an important role to play in both the theoretical and applied disciplines of invasion biology. Few invaders impact terrestrial ecosystems more than ants. Among the world’s 100 worst invasive species is the cosmopolitan and highly destructive Pheidole megacephala (Fabricius). Accurate identification of Pheidole megacephala is imperative for the success of screening, management and eradication programs designed to protect native ecosystems from the impacts of this destructive species. However, accurate identification of Pheidole species is difficult because of their taxonomic diversity, dimorphic worker caste and lack of taxonomic resources. Illustrated keys are included, along with the taxonomic history, taxonomic diagnoses, biological notes and risk statements for the 14 most invasive members of the genus. Global distribution maps based on over 14,000 specimen and literature records are presented for each species. These results of this work will facilitate identification of pest species, determination of climatic and habitat requirements, discovery of pest origins, horizon scanning and assessment of invasion pathways. The following new synonym is proposed, with the senior synonym listed first and the junior synonyms in parentheses: Pheidole indica Mayr (= Pheidole teneriffana Forel, and its synonyms Pheidole taina Aguayo and Pheidole voeltzkowii Forel). Pheidole navigans Forel, stat. rev., stat. n. is removed from synonymy and elevated to species rank. It is proposed that records of Pheidole moerens Forel outside of the Mesoamerica and the Caribbean refer instead to Pheidole navigans or other heterospecific taxa in the Pheidole flavens species complex. We propose that the names Pheidole anastasii Emery and Pheidole floridana Emery have been widely misapplied to North American outdoor records of Pheidole bilimeki Mayr. It is suggested that the synonymy of Pheidole lauta Wheeler be transferred from Pheidole floridana Emery to Pheidole bilimeki Mayr.     

Subcaste‐specific evolution of head size in the ant genus Pheidole

An organism's morphology is constrained by its evolutionary history and the need to meet a variety of potentially competing functions. The ant genus Pheidole is the most species‐rich ant genus and almost every species has a dimorphic worker caste (a few are trimorphic). This separation of workers into two developmentally distinct subcastes (smaller minors and larger majors with distinctively large heads) may partially release individuals from functional constraints on morphology, making Pheidole an ideal genus for addressing questions on the evolution of morphology in relation to ecological specialization. Major workers can perform a variety of tasks, although they are usually specialized for defence, as well as food retrieval and processing. Pheidole species vary in their diet, although many species gather seeds. The major workers mill the seeds using large jaws powered by mandible closer muscles that occupy a large proportion of the head cavity. In the present study, we examined the relationship between seed‐harvesting and morphology in Pheidole, hypothesizing that majors of seed‐harvesting species would have larger heads relative to non‐seed‐harvesters to accommodate the powerful mandibular muscles needed to mill seeds. By taking a phylogenetically controlled comparative approach, we found that majors of seed‐associated Pheidole did not have larger heads (width and length) than majors of non‐seed‐harvesting species. However, the head length of minors (and to a lesser extent head width) was smaller in seed‐harvesters. Additionally, we found the difference in head size between majors and minors was greater in seed‐harvesting species. These morphological differences in diet, however, were not related to changes in the rate of evolution in either seed‐harvesting or non‐seed‐harvesting lineages. These findings suggest that the morphologies of worker subcastes can evolve independently of each other, allowing colonies with polymorphic workers to specialize on new resources or tasks in ways not possible in monomorphic species.     

Sociogenetic organisation of two desert ants

Desert ants of the genus Cataglyphis evolved a remarkable diversity in their reproductive strategies. In Cataglyphis species where social organisation was described so far, colonies are headed by one or multiple queens, queens being singly or multiply mated, and workers and/or queens possess the ability to reproduce asexually via thelytokous parthenogenesis. Here, we investigate the social organisation of C. bombycina (group bombycinus) and C. theryi (group albicans) using highly polymorphic microsatellite markers. Our results show that both species are characterized by monogynous colonies and multiply mated queens, supporting the idea that polyandry is an ancestral trait of the genus. No evidence for parthenogenetic reproduction by queens was found. One distinctive feature of the species C. bombycina among the genus is the presence of a morphologically distinct soldier caste, with highly developed scythe blades jaws. In the only colony where a significant number of soldiers have been sampled, the distribution of patrilines is fundamentally different between the soldier and the worker caste. This result suggests a genetic contribution to worker caste determination in this species, and certainly awaits further investigation.     

Old soldiers never die ....

An ancestral supersoldier phenotype of Pheidole ants can be recovered when selection for supersoldiers re-emerges, indicating that the developmental potential for caste pathways is retained.     

Reactions by army ant workers to nestmates having had contact with sympatric ant species

It was recently shown that Pheidole megacephala colonies (an invasive species originating from Africa) counterattack when raided by the army ant, Eciton burchellii. The subsequent contact permits Pheidole cuticular compounds (that constitute the “colony odour”) to be transferred onto the raiding Eciton, which are then not recognised by their colony-mates and killed. Using a simple method for transferring cuticular compounds, we tested if this phenomenon occurs for Neotropical ants. Eciton workers rubbed with ants from four sympatric species were released among their colony-mates. Individuals rubbed with Solenopsis saevissima or Camponotus blandus workers were attacked, but not those rubbed with Atta sexdens, Pheidole fallax or with colony-mates (control lot). So, the chemicals of certain sympatric ant species, but not others, trigger intra-colonial aggressiveness in Eciton. We conclude that prey-ant chemicals might have played a role in the evolution of army ant predatory behaviour, likely influencing prey specialization in certain cases.