Global phylogenetic structure of the hyperdiverse ant genus Pheidole reveals the repeated evolution of macroecological patterns

Adaptive radiations are of particular interest owing to what they reveal about the ecological and evolutionary regulation of biodiversity. This applies to localized island radiations such as Darwin''s finches, and also to rapid radiations occurring on a global scale. Here we analyse the macroevolution and macroecology of Pheidole, a famously hyperdiverse and ecologically dominant ant genus. We generate and analyse four novel datasets: (i) a robust global phylogeny including 285 Pheidole species, (ii) a global database on regional Pheidole richness in 365 political areas summarizing over 97 000 individual records from more than 6500 studies, (iii) a global database of Pheidole richness from 3796 local communities and (iv) a database of Pheidole body sizes across species. Analysis of the potential climate drivers of richness revealed that the patterns are statistically very similar across different biogeographic regions, with both regional and local richness associated with the same coefficients of temperature and precipitation. This similarity occurs even though phylogenetic analysis shows that Pheidole reached dominance in communities through serial localized radiations into different biomes within different continents and islands. Pheidole body size distributions have likewise converged across geographical regions. We propose these cases of convergence indicate that the global radiation of Pheidole is structured by deterministic factors regulating diversification and diversity.     

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.     

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.     

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.     

Infant growth restriction is associated with distinct patterns of DNA methylation in human placentas

The placenta acts not only as a conduit of nutrient and waste exchange between mother and developing fetus, but also functions as a regulator of the intrauterine environment. Recent work has identified changes in the expression of candidate genes, often through epigenetic alteration, which alter the placenta's function and impact fetal growth. In this study, we used the Illumina Infinium HumanMethylation27 BeadChip array to examine genome-wide DNA methylation patterns in 206 term human placentas. Semi-supervised recursively partitioned mixture modeling was implemented to identify specific patterns of placental DNA methylation that could differentially classify intrauterine growth restriction (IUGR) and small for gestational age (SGA) placentas from appropriate for gestational age (AGA) placentas, and these associations were validated in a masked testing series of samples. Our work demonstrates that patterns of DNA methylation in human placenta are reliably and significantly associated with infant growth and serve as a proof of principle that methylation status in the human term placenta can function as a marker for the intrauterine environment, and could potentially play a critical functional role in fetal development.     

Cell cycle progression is associated with distinct patterns of phosphorylation of Op18.

Op18 is a highly conserved major cytosolic phosphoprotein which has been implicated in signal transduction in a wide variety of cell types. Freshly isolated peripheral blood lymphocytes (PBL) constitutively express low levels of mostly unphosphorylated Op18. Following mitogenic stimulation of PBL, Op18 synthesis is induced at a time when cells are entering S-phase. In this study we have characterized Op18 phosphorylation during progression of freshly isolated PBL through the cell cycle. Transition from G0 to G1 following activation with OKT3 was associated with an increase in a phosphorylated form designated Op18c. Progression of cells through G1 into S resulted in an increase in phosphorylated Op18 forms, designated Op18a and Op18b, which paralleled new Op18 synthesis. Transition of cells into G2 + M resulted in the appearance of the more acidic phosphorylated forms Op18d and Op18e. Calphostin C, a specific inhibitor of protein kinase C, dramatically decreased all forms of phosphorylated Op18 in OKT3 treated Jurkat cells. Our results suggest that Op18 phosphorylation is mediated in part by PKC activation as well as by other kinases yielding different phosphorylated forms at specific stages of the cell cycle.     

Division of labour and seasonality in the ant Leptothorax albipennis: worker corpulence and its influence on behaviour

We address the organization of workers in social insect societies. We distinguish between changes in behavioural role over the nurse to forager role sequence, which may depend on changes in physiology, and potentially more rapid changes of task within role. We investigated the association between role and nutrient status in the ant Leptothorax albipennis. Worker lipid stores were quantified using a new body size-controlled method, and were related to worker behaviour. Worker lipid stores were evenly distributed amongst colony members at the end of winter, splitting rapidly into two distinct modes (replete nurses and lean foragers) in spring. The proportion of lean foragers increased throughout spring and summer, until most colonies contained only workers of this type. Callow workers then eclosed with intermediate lipid stores. We developed a computer vision system that tracks all nest ants to extract detailed behaviour of individuals of known lipid stores. Lipid storage was negatively correlated with a worker's foraging propensity, and with measures of spatial occupation in the nest and of activity. Different colonies showed a similar quantitative correlation between lipid stores and behavioural role, suggesting that lipid stores were not only correlated with the relative organization of individuals within each nest, but may also have influenced their absolute role. We reviewed the literature and found evidence that nutrient status influences role predisposition in social insect workers. We conclude that the distribution of worker roles may be linked to the balance between foraging income and energetic consumption within the colony directly via worker nutrient status. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

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.     

Species-level phylogeography and evolutionary history of the hyperdiverse marine gastropod genus Conus

Phylogenetic and paleontological analyses are combined to reveal patterns of species origination and divergence and to define the significance of potential and actual barriers to dispersal in Conus, a species-rich genus of predatory gastropods distributed throughout the world's tropical oceans. Species-level phylogenetic hypotheses are based on nucleotide sequences from the nuclear calmodulin and mitochondrial 16S rRNA genes of 138 Conus species from the Indo-Pacific, eastern Pacific, and Atlantic Ocean regions. Results indicate that extant species descend from two major lineages that diverged at least 33 mya. Their geographic distributions suggest that one clade originated in the Indo-Pacific and the other in the eastern Pacific + western Atlantic. Impediments to dispersal between the western Atlantic and Indian Oceans and the central and eastern Pacific Ocean may have promoted this early separation of Indo-Pacific and eastern Pacific + western Atlantic lineages of Conus. However, because both clades contain both Indo-Pacific and eastern Pacific + western Atlantic species, migrations must have occurred between these regions; at least four migration events took place between regions at different times. In at least three cases, incursions between regions appear to have crossed the East Pacific Barrier. The paleontological record illustrates that distinct sets of Conus species inhabited the Indo-Pacific, eastern Pacific + western Atlantic, and eastern Atlantic + former Tethys Realm in the Tertiary, as is the case today. The ranges of <1% of fossil species (N=841) spanned more than one of these regions throughout the evolutionary history of this group.     

Isolation and characterization of microsatellite loci from the invasive ant Pheidole megacephala

We report the characterization of eight microsatellite markers in the big-headed ant Pheidole megacephala, a pest ant registered in the list of '100 of the world's worst invasive alien species'. An enrichment protocol was used to isolate microsatellite loci, and polymorphism was explored with 36 individuals collected in an invasive population from Australia and 20 individuals collected in a population from the native mainland location in South Africa. These primers showed a number of alleles per locus ranging from two to 10, and expected heterozygosities ranging from 0.083 to 0.826. Moreover, results of cross-species amplification are reported in five other Pheidole species and in seven other ants of the subfamily Myrmicinae.     

Functional groups and patterns of organization in North American ant communities: a comparison with Australia

Ant distribution and behavioural dominance is examined at nine sites along an elevational gradient (1400–2600 m) in south eastern Arizona, in order to classify North American species according to a functional group scheme used extensively in Australia. The functional groups are then used as a basis for determining patterns of community structure along the environmental gradient, and for comparing community structure between Australia and North America. Quantitative information on species com- position was obtained from pitfall traps, and patterns of ant abundance at tuna baits were used to determine relative behavioural dominance among taxa. A total of eighty-three species from twenty-eight genera was recorded along the elevational gradient, with site species richness ranging from four (high elevation Douglas fir forest) to thirty-three (mid elevation oak–juniper woodland). There was a strong correlation between ant abundance and richness, which was not an artefact of sampling intensity. The most common ants were species of Forelius, Monomorium, Crematogaster and Pheidole at the three desert sites, species of Formica, Pheidole and Crematogaster at the three woodland sites, and species of Prenolepis and Formica at one forest site. No species were abundant at two other forest sites. The most common species in traps also tended to be the most common species at baits. In terms of behavioural dominance, highly competitive ants included species of Solenopsis, Forelius, Monomorium and Liometopum. Species of Pheidole and Crematogaster tended to be moderately competitive, whereas species of Dory- myrmex, Myrmica, Camponotus and Formica (fusca gp) had low competitive ability. On the basis of these results and on published records of other taxa, North American ants were assigned to functional groups as follows (major taxa only given here): Dominant Dolichoderinae—Forelius, Liome- topum; Subordinate Camponotini—Camponotus; Hot Climate Specialists—Pogonomyrmex, Myrmecocystus; Cold Climate Specialists—Formica (rufa, exsecta and microgyna groups), Leptothorax, Stenamma, Lasius, Prenolepis; Cryptic Species—Smithistruma, Solenopsis (subgenus Diplorhop- trum), Acanthomyops; Opportunists—Formica (fusca group), Myrmica, Paratrechina, Dorymyrmex; Generalized Myr- micinae—Pheidole, Crematogaster, Monomorium; Specialist Predators—no major taxa. Functional group composition varied systematically along the elevation gradient: Dominant Dolichoderinae, Generalized Myrà micinae and Hot Climate Specialists were predominant at desert sites; Generalized Myrmicinae and Opportunists were predominant at woodland sites; and Opportunists and Cold Climate Specialists were predominant at forest sites. These patterns are consistent with published studies from elsewhere in North America. Almost all North American taxa can be matched with what appear to be ecologically equivalent taxa in Australia, and biogeographic patterns of functional group composition are broadly similar across the two continents. The major differences are that Australian ant communities are far richer in species, and are almost always dominated by dolichoderines, particularly species of Iridomyrmex. Generalized myrmicines are subdominant to dolichoderines in Australia, but are the behaviourally dominant ants throughout the warmer parts of North America. In cool-temperate North America, species of Formica (especially rufa and exsecta groups) are behaviourally dominant, as they are throughout the Palearctic. Some major features of the North American fauna can be linked to its poor representation of Dominant Dolichoderinae, including (1) the relatively low degree of physiological, morphological and behavioural specialization of Hot Climate Specialists; (2) behavioural dominance by formicines in cool-temperate habitats; and (3) the susceptibility to invasion by behaviourally dominant species such as the imported fire ant Solenopsis invicta and the Argentine ant Linepithema humile.     

Changes in brain amine levels associated with the morphological and behavioural development of the worker honeybee

Summary Changes in biogenic amine levels associated with the morphological and behavioural development of the worker honeybee are examined.A significant increase in amine levels in the head of the honeybee is associated with transition from the larval to pupal stage. Adult emergence is also accompanied by a significant increase in 5-HT levels in the brain, but no significant change in brain dopamine (DA) levels. NADA (N-acetyldopamine) levels increase during larval and pupal development, but in contrast to both DA and 5-HT, drop significantly during the transition from pupa to adult.Levels of DA in the brain of nectar and pollen forager bees, presumed to be among the oldest adults sampled, were found to be significantly higher than in nurses, undertakers or food storers. These results suggest that an age-dependent change in amine levels occurs in the brain of the worker bee. In the optic lobes, levels of DA and 5-HT were found to be significantly higher in pollen forager bees than in all other behavioural groups. Significant differences in amine levels in the optic lobes of nectar foragers and pollen foragers indicate that some differences in amine levels occur independent of worker age. The functional significance of differences in brain amine levels and whether or not biogenic amines play a direct role in the control of honeybee behaviour has yet to be established.Abbreviations DA dopamine - 5-HT 5-hydroxytryptamine or serotonin - NADA N-acetyldopamine     

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.     

A new data of worker polymorphism in the ant genus Dorylus (Hymenoptera: Formicidae: Dorylinae)

Recently, in southern and central Vietnam, foraging columns of D. orientalis which contained not only “typical” workers but also a few “atypical” workers were collected. The atypical worker mentioned above is characterized by a set of the following features: (1) head narrowed anteriorly, (2) median portion of clypeus strongly projecting anteriad, and (3) antenna 8-segmented. Sequences of the 658-base standard mitochondrial DNA barcoding region were completely identical between typical and atypical workers. Therefore, the condition observed was a case of worker polymorphism within a colony. The mode of polymorphism observed has the following interesting aspects: (1) workers are clearly subdivided into two series by a set of qualitative characters; (2) the “typical series” is numerically much more dominant than the “atypical series” (the latter occupied less than 1% of the whole of the workers collected); (3) a wider size variation was observed in the former (HW, 0.48–1.41 mm; ML, 0.42–1.12 mm) than in the latter (HW, 0.44–1.13 mm; ML, 0.35–0.79 mm); and (4) within the atypical series, smaller workers are numerically much dominant. Rareness of the workers belonging to the atypical series in foraging column as well as morphological differences between the two series suggests a certain possibility that the atypical series does not adapt to foraging but to other tasks in the colony's life history.