Seasonality, division of labor, and dynamics of colony-level nutrient storage in the ant Pheidole morrisi

Nutritional provisioning is a critical component of life history strategies, and of particular interest in social insect colonies because of the role that division of labor plays in resource allocation. To explore the mechanisms that underlie colony nutritional strategies, I examined three populations of the ant Pheidole morrisi across a gradient of overwinter food scarcity over two seasons. P. morrisi colonies were found to employ amixed strategy of fat storage with regard to a longer overwinter period: members of both worker castes increase their percent-fat in a graded manner, while the proportion of a specialized subcaste of majors known as “repletes”, also increased within the colony. Geographic variation in other colony traits such as mean colony size, mean worker size, and minor/major caste ratio were also found, although not always in a manner clearly relating to fat storage. These results indicate that colony demography responds to seasonal fluctuations in food availability through behavioral alterations (increased fat stores and recruitment of replete workers) rather than physical alterations (changes in lean body sizes or caste ratio). The findings illustrate the dynamic role division of labor plays in the success of insect colonies confronting environmental variability. Received 9 May 2006; revised 19 July 2006; accepted 24 July 2006.     

Differential regulations of wing and ovarian development and heterochronic changes of embryogenesis between morphs in wing polyphenism of the vetch aphid

SUMMARY In wing polyphenisms that produced alternative wing morphs depending on environmental conditions, the developmental regulations to balance between flight and reproductive abilities should be important. Many species of aphids exhibit wing polyphenisms, and the development of wing and flight muscles is thought to incur costs of reproductive ability. To evaluate the relationship between flight and reproduction, the fecundity and the wing- and ovarian development in the parthenogenetic generations were compared between winged and wingless aphids in the vetch aphid Megoura crassicauda . Although no differences in offspring number and size were detected, the onset of larviposition after imaginal molt was delayed in winged adults. The comparison of growth in flight apparatus revealed that, after the second-instar nymphs, the flight-apparatus primordia of presumptive wingless aphids were degenerated while those of winged nymphs rapidly developed. In the ovaries of winged line, the embryo size was smaller and the embryonic stages were delayed from third to fifth instars, although these differences had disappeared by the time of larviposition. It is therefore likely that the delay in larviposition in winged aphids is due to the slower embryonic development. The correlation between embryo size and developmental stage suggests that the embryos of winged aphids are better developed than similarly sized embryos in wingless aphids. These heterochronic shifts would facilitate the rapid onset of larviposition after the dispersal flight. This developmental regulation of embryogenesis in the aphid wing polyphenism is suggested to be an adaptation that compensates the delay of reproduction caused by the wing development.     

Physiological condition and wing pigmentation expression in a damselfly with seasonal polyphenism

Secondary sexual traits can be indicators of individual condition that may present seasonal polyphenism as a result of the differential costs of expression along the season. Wing spots in male damselflies of the Calopterygidae family are secondary sexual traits associated with intrasexual competition and mate choice. Hetaerina titia Drury is a calopterygid damselfly where males show red and black wing spots, contrasting with other species of the genus whose males only express a red wing spot. In the present study, we evaluate the seasonal variation of the expression of male's red and black wing spots and their allometric patterns. Additionally, we measure male condition in the form of proteins, lipids, soluble carbohydrates and glycogen in early and late seasons. Black wing spots present higher variation than red wing spots and males of the late season are more pigmented. Allometry is positive for wing red spot in the early season and for black spot in the late season. Males of the late season present a higher concentration of proteins, soluble carbohydrates and glycogen, although there is no variation in the lipid content. The results of the present study suggest that, in H. titia males, black pigmentation replaces the function of the red pigmentation to signal condition. Both traits, however, may be heavily affected by environmental situations (e.g. food availability).     

Nest relocation in the ant Pheidole dentata

We studied nest relocation in the ant Pheidole dentata, a common species in the southern US, by following colonies for 6 weeks. We correlated probability of relocation with several abiotic and biotic environmental factors, such as air temperature, humidity, leaf litter depth (LLD), nest type and presence of phorid fly parasitoids. Colonies moved often, on average every 16.2 days. By the end of our study, fewer than 5 % of colonies marked at the start remained in their original nests. Only 3.1 % of colonies returned to a previously used nest. The mean distance of relocation was 0.76 ± 0.73 m. Colonies nested in a variety of locations, such as in the ground, by tree trunks, under rocks and inside wood. Several factors affected probability of relocation. Higher LLD and vapor pressure deficit (VPD) increased probability of relocation. Probability of relocation varied by nest type, by plot and week of study. We found no evidence that surface cover or rain affected relocation behavior. Colonies appear to avoid nests that become dry by nesting against tree trunks. Phorid fly abundance correlated negatively with VPD, yet it had no effect on colonies’ likelihood of relocation. We discuss other implications of frequent nest relocations.     

Cooperation during prey digestion between workers and larvae in the ant, Pheidole spadonia

Digestion and distribution of nutrients are central to the growth and reproduction of social insect colonies, just as they are to individual organisms. In the case of eusocial insect species, different components of food handling and processing can be distributed among castes. This paper reports on an ant species, Pheidole spadonia, in which the adult workers butcher prey and 4^th instar larvae dissolve prey for distribution among other colony members including workers, larvae and queens. To characterize the process, six groups, each composed of twenty-five workers and thirty larvae, were provisioned with a fruit fly carcass, and then video-taped continuously for 24 hours. On average, five adult workers and twenty-two 4^th instar larvae invested 12.8 labor hours into butchering and predigesting one fly carcass. Workers contributed a mean total of 3.3 labor hours to butcher the carcass into small fragments. Fourth instar larvae contributed a mean total of 9.5 labor hours to pre-orally dissolve the solid fragments. Surprisingly, larvae did not ingest during the dissolving process. Instead, workers ingested the dissolved prey tissue into their crops and then regurgitated it to colony members, larvae and workers, that solicited for feedings. The cooperative interactions reported here between workers and larvae extend the mechanistic and evolutionary explanations for eusociality. Received 13 January 2005; revised 22 April 2005; accepted 25 April 2005.     

Chromosome polymorphism in the ant,Pheidole nodus

A survey of chromosome polymorphism was made in populations of Pheidole nodus (Hymenoptera, Formicidae). A total of 1,666 males were collected from 11 localities in Japn. Four polymorphic karyotypes were observed: (1) n = 17 with 4 metacentrics (abbreviated as 4M), (2) n = 18(3M), (3) n = 19(2M) and (4) n = 20(1M). These differences are due to the Robertsonian type rearrangement. The karyotype 18(3M) is found in all the populations examined, but the others are more or less localized in their distribution. The 17(4M) appears mainly in Shikoku and the northern Kyushu populations, 19(2M) along the Pacific coast of Honshu, Shikoku and Kyushu, and 20(1M) in the eastern part of Honshu and Shikoku. This distribution pattern indicates that 18(3M) is the oldest, 19(2M) and 20(1M) are derived from 18(3M) by centric fission, and 17(4M) by centric fusion. The most probable mechanism of karyotype evolution in this species is considered to be the centric fission.     

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.     

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

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

Antibiotics, primary symbionts and wing polyphenism in three aphid species

The possible role of the primary Buchnera symbionts in wing polyphenism is examined in three aphid species. Presumptive winged aphids were fed on antibiotic-treated beans to destroy these symbionts. As previously reported, this leads to inhibited growth and low/zero fecundity. When such treatment is applied to the short-day-induced gynoparae (the winged autumn migrant) of the black bean aphid, Aphis fabae, it also causes many insects to develop as wingless or winged/wingless intermediate adult forms (apterisation). However, whilst antibiotic treatment of crowd-induced, long-day winged forms of the pea aphid, Acyrthosiphon pisum (a green and a pink clone) and the vetch aphid, Megoura viciae has similar effects on size and fecundity, it does not affect wing development. Food deprivation also promotes apterisation in A. fabae gynoparae but not in the crowd-induced winged morphs of the other two species. Thus, it appears that apterisation in A. fabae is not a direct effect of antibiotic treatment or a novel role for symbionts but is most likely related to impaired nutrition induced by the loss of the symbiont population.     

Sex ratio determination by queens and workers in the ant Pheidole desertorum

Because workers in colonies of eusocial Hymenoptera are more closely related to sisters than to brothers, theory predicts workers should bias investment in reproductive broods to favour reproductive females over males. However, conflict between queens and workers is predicted. Queens are equally related to daughters and sons, and should act to prevent workers from biasing investment. Previous study of the ant Pheidole desertorum showed that workers are nearly three times more closely related to reproductive females than males; however, the investment sex ratio is very near equal, consistent with substantial queen control of workers. Near-equal investment is produced by an equal frequency of colonies whose reproductive broods consist of only females (female specialists) and colonies whose reproductive broods consist of only males or whose sex ratios are extremely male biased (male specialists). Because natural selection should act on P. desertorum workers to bias investment in favour of reproductive females, why do workers in male-specialist colonies rear only (or mostly) males? We tested the hypothesis that queens prevent workers from rearing reproductive females by experimentally providing workers with immature reproductive broods of both sexes. Workers reared available reproductive females, while failing to rear available males. Worker preference for rearing reproductive females is consistent with queens preventing their occurrence in colonies of male specialists. These results provide evidence that queens and workers will act in opposition to determine the sex ratio, a fundamental prediction of queen-worker conflict theory. Copyright 2000 The Association for the Study of Animal Behaviour.     

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)]     

Kin recognition and the paradoxical patterns of aggression between colonies of a Mojave desert Pheidole ant

Populations of the desert seed-harvesting ant Pheidole xerophylla are often characterized by high nest density leading to competitive interactions between foragers from different nests. We investigated the inter-nest aggression, spatial distribution and genetic structure of a P. xerophylla population of the Mojave Desert in Southern California. Inter-nest aggression was quantified by standardized staged encounters in a neutral arena. Genetic relatedness within nests and relatedness between nests were calculated using allelic frequencies at four microsatellite-DNA loci. We found a bimodal distribution of inter-colony aggression levels with a first mode at low aggression levels and another mode at much higher aggression levels. Inter-colony aggression levels were largely non-transitive. No effect of geographical distance on inter-nest aggression levels was detected. Despite high amounts of variation in inter-colony relatedness ( − 0.24 to 0.37) this variable did not correlate with the level of aggression between nests. Intra-nest relatedness ranged from 0.40 to 0.75 and close inspection of worker genotypes within colonies revealed a high proportion of polygynous colonies or a mixture of polygyny and polyandry. Aggression levels among nests was found to decrease with increasing intra-nest relatedness. These results do not support the idea that aggression is modulated by a nestmate recognition mechanism based on overall genetic similarity. Instead, the absence of transitivity found in inter-colony aggression and bimodal distribution of aggression levels are compatible with a common label acceptance model of nestmate recognition and suggest that label diversity may be encoded by a limited number of loci. Received 29 March 2005; revised 8 September 2005; accepted 27 September 2005.     

The dynamics of developmental system drift in the gene network underlying wing polyphenism in ants: a mathematical model

SUMMARY Understanding the complex interaction between genotype and phenotype is a major challenge of Evolutionary Developmental Biology. One important facet of this complex interaction has been called "Developmental System Drift" (DSD). DSD occurs when a similar phenotype, which is homologous across a group of related species, is produced by different genes or gene expression patterns in each of these related species. We constructed a mathematical model to explore the developmental and evolutionary dynamics of DSD in the gene network underlying wing polyphenism in ants. Wing polyphenism in ants is the ability of an embryo to develop into a winged queen or a wingless worker in response to an environmental cue. Although wing polyphenism is homologous across all ants, the gene network that underlies wing polyphenism has evolved. In winged ant castes, our simulations reproduced the conserved gene expression patterns observed in the network that controls wing development in holometabolous insects. In wingless ant castes, we simulated the suppression of wings by interrupting (up- or downregulating) the expression of genes in the network. Our simulations uncovered the existence of four groups of genes that have similar effects on target gene expression and growth. Although each group is comprised of genes occupying different positions in the network, their interruption produces vestigial discs that are similar in size and shape. The implications of our results for understanding the origin, evolution, and dissociation of the gene network underlying wing polyphenism in ants are discussed.     

Interspecific competition between Solenopsis invicta and two native ant species, Pheidole fervens and Monomorium chinense

This study was designed to understand the effects of the interspecific competition between red imported fire ant, Solenopsis invicta Buren and two native ant species, Pheidole fervens Smith and Monomorium chinense Santschi, by conducting colony interference and individual confrontation tests under laboratory conditions. The colony interference test showed that both native ant species, owing to their numerical advantage, killed the Solenopsis invicta virus-1 (SINV-1)-infected or healthy queens of S. invicta. Significantly less time was required for M. chinense to kill all SINV-1-infected S. invicta compared with the time required to kill the healthy S. invicta. Compared with healthy S. invicta, SINV-1-infected S. invicta spent a longer time eliminating the P. fervens colonies. In confrontation tests, M. chinense killed a significantly higher number of infected S. invicta minors than they did healthy minors, but the number of S. invicta majors (either infected or healthy) killed was substantially less. This study found that the viral infection weakened the competitive ability of S. invicta and made them prone to be eliminated by M. chinense but not by P. fervens.     

Initiation of flight muscle apoptosis and wing casting in the red imported fire ant Solenopsis invicta

Abstract Newly‐mated Solenopsis invicta flight queens cast (shed) their wings within 24 h. An examination of their flight muscle cells reveals numerous apoptotic (terminal deoxynucleotidyl transferase mediated dUTP nick end labelling positive) nuclei. By contrast, flight muscle cells of mature alate virgin (MAV) females removed 24 h earlier from a managed laboratory colony exhibit neither wing casting nor the presence of apoptotic nuclei. Using MAV‐females, the initiation of flight muscle apoptosis and wing casting is compared with artificial mating using seminal fluid with sperm, seminal fluid with no sperm, saline as a negative control, the mating flight as simulated in the laboratory, elevated CO₂ exposure, application of methoprene (a juvenile hormone analogue), or injection of 20‐hydroxyecdysone. Numerous apoptotic nuclei are revealed in the flight muscle cells of mated dealate females 24 h after a natural mating flight but not in MAV‐females controls. Only artificial mating of MAV‐females reveals a similar pattern of apoptotic nuclei flight muscle 24 h after insemination. None of the other factors tested induces flight muscle cell apoptosis in MAV‐females. Methoprene dissolved in methyl ethyl ketone, at a concentration of 0.44 ng per μL per ant, stimulates 90% of MAV‐females to shed their wings within 24 h, as opposed to 10% or less wing shedding for the methyl ethyl ketone control and all other treatments.     

Genetics, behaviour and chemical recognition of the invading ant Pheidole megacephala

Introduced species often become ecologically dominant, displacing native species and posing a serious threat to ecosystem function and global biodiversity. Ants are among the most widespread and damaging alien species; introductions are often accompanied by population-level behavioural and genetic changes contributing to their success. We investigated the genetic structure, chemical profile and nestmate recognition in introduced populations of the invasive big-headed ant, Pheidole megacephala, in Australia. Behavioural analyses show that workers are not aggressive towards conspecifics from different nests, even at large geographical scales (up to 3000 km) and between populations encompassing a wide range of environmental conditions. By contrast, interactions with workers of other species invariably result in agonistic behaviours. Genetic analyses reveal that populations have low genetic diversity. No genetic differentiation occurs among nests of the same population; differentiation between populations, though significant, remains weak. Chemical analyses indicate that cuticular lipids are similar between colonies of a population, and that differentiation between populations is low. Altogether, these results indicate that the big-headed ant P. megacephala forms a large unicolonial population across northern/eastern Australia.