Energy use and allocation in the Florida harvester ant, Pogonomyrmex badius: are stored seeds a buffer?

Limitation of a necessary resource can affect an organism’s investment into growth and reproduction. Pogonomyrmex harvester ants store vast quantities of seeds in their nests that are thought to buffer the ants when external resources are not available. This research uses externally controlled food availability to examine how resource shortage affects colony investment, resource use, and resource distribution within the nest. Colonies were either starved or supplemented with resources for 2 months, beginning at the onset of reproductive investment and ending immediately before nuptial flights. Fed colonies invested more in overall production, proportionally more in reproduction relative to growth and in female reproductives relative to males. Stored seeds in starved colonies did not buffer production in this study. However, worker fat reserves were depleted in starved colonies, indicating that fat reserves fuel the spring bout of production. In starved colonies, worker fat reserves were depleted evenly throughout the nest, distributing the burden of starvation on all workers regardless of caste and age. A reallocation of diploid eggs into female workers rather than reproductives best explains the observed change in sex ratio investment between treatments. The redistribution of resources into growth relative to reproduction in starved colonies is consistent with life history theory for long-lived organisms, switching from current to future reproduction when resources are scarce.     

Brood production and lineage discrimination in the red harvester ant (Pogonomyrmex barbatus)

In contrast to the system of caste determination in most social insects, reproductive caste determination in some populations of Pogonomyrmex barbatus has a genetic basis. Populations that exhibit genetic caste determination are segregated into two distinct, genetic lineages. Same-lineage matings result in female reproductives, while inter-lineage matings result in workers. To investigate whether founding P. barbatus queens lay eggs of reproductive genotype, and to determine the fate of those eggs, we genotyped eggs, larvae, and pupae produced by naturally inseminated, laboratory-raised queens. We show that founding dependent lineage queens do lay eggs of reproductive genotype, and that the proportion of reproductive genotypes decreases over the course of development from eggs to larvae to pupae. Because queens must mate with a male of each lineage to produce both workers and female reproductives, it would benefit queens to be able to distinguish males of the two lineages. Here we show that P. barbatus males from the two genetic lineages differ in their cuticular hydrocarbon profiles. Queens could use male cuticular hydrocarbons as cues to assess the lineage of males at the mating aggregation, and possibly keep mating until they have mated with males of both lineages.     

Extremely high mating frequency in the Florida harvester ant (<Emphasis Type="Italic">Pogonomyrmex badius</Emphasis>)

High effective multiple queen mating is a rare but taxonomically widespread phenomenon in eusocial Hymenoptera that has arisen convergently in several taxa. In ants, high effective mating frequencies have been confirmed in only two clades: the higher leaf-cutters (Atta, Acromyrmex) and the Pogonomyrmex seed harvesters. We analysed polyandry in Pogonomyrmex badius, which has a life-history unique within the genus, and report the highest numerical mating frequencies thus far recorded in ants. We also show that P. badius is characterized by one of the highest effective mating frequencies hitherto found in ants. It is now clear that all major sub-clades of Pogonomyrmex sensu stricto exhibit high levels of polyandry. Therefore, multiple mating must have arisen early in the evolution of the genus, and may have constituted a mechanism to increase offspring variability for queens that were confronted with increasingly complex levels of organization. Too few congeners have been investigated by the same method to be certain that polyandry in P. badius is really higher than in the rest of the genus. If so, research should concentrate on a possible link between high queen mating frequency and the distinct caste system found in P. badius.Communicated by L. Keller     

Energetic and time costs of foraging in harvester ants,Pogonomyrmex occidentalis

Summary Western harvester ants, Pogonomyrmex occidentalis, preferentially utilize low vegetational cover pathways. Energetic costs for foraging ants were less than 0.1% of caloric rewards of harvested seeds, suggesting that reduction of energetic cost is not a major benefit of this preference. Walking speed was significantly faster on lower cover routes, increasing net return rates from equidistant artificial food sources. Undisturbed foragers on low cover routes traveled farther, increasing their total foraging area without increasing foraging time. These results suggest that in animals with low costs of locomotion relative to energetic rewards, time costs are more important than direct energetic costs in influencing foraging decisions. In baited experiments with equidistant food sources, preferential use of low cover routes resulted in a large increase in net energetic gain rate, but only a slight increase in energetic efficiency. Under natural conditions, net energetic gain rates were constant for foragers using low and high vegetational cover routes, but foragers using low cover paths had lower efficiencies. This suggests that net energetic gain rate is a more important currency than energetic efficiency for foraging harvester ants.     

Behavioral differences between Pogonomyrmex rugosus and dependent lineage (H1/H2) harvester ants

The discovery of genetic caste determination (GCD) in populations of Pogonomyrmex harvester ants raises many questions about the evolution and persistence of such populations. The genetic caste determination arises from the existence of two distinct, but mutually dependent, genetic lineages within a population. Workers always develop from a combination of the two lineages, but their sister queens develop from within-lineage matings. Maintaining genetic caste determination appears to be costly because many queen-destined eggs are wasted when a colony is not in the reproductive stage, yet these populations appear to be widespread. We investigated whether inter-lineage workers have novel traits that give GCD colonies a selective advantage in certain environments. In particular, we compared ecologically relevant behavioral characteristics of inter-lineage workers in H-lineage colonies with co-occurring normal colonies of P. rugosus. First, we measured colony defensive response toward a simulated vertebrate predator. Second, we set up direct competitive foraging and recruitment experiments between dependent lineage and P. rugosus colonies. Last, we measured individual aggressive response to foreign inter-lineage and P. rugosus workers. We found that H1/H2 inter-lineage workers explored objects on the nest more thoroughly and responded much more aggressively to simulated predator disturbance than the P. rugosus colonies. In individual encounters, H1/H2 inter-lineage and P. rugosus workers were equally aggressive toward foreign ants, but both worker types could discriminate P. rugosus from inter-lineage intruders and were more aggressive toward ants of the alternate type to themselves. When competing directly for resources, however, P. rugosus colonies consistently dominated seed piles. In summary, H1/H2 GCD colonies show distinct behavioral differences, but there is no clear ecological advantage from the traits we examined.     

Low queen mating frequency in the seed-harvester ant Pogonomyrmex (Ephebomyrmex) pima: implications for the evolution of polyandry

The evolution of polyandry is a central problem in the study of insect mating systems, and both material and genetic benefits have been proposed to offset the presumed costs of multiple mating. Although most eusocial Hymenoptera queens mate with just one or occasionally two males, high levels of polyandry are exhibited by several taxa, including seed-harvester ants of the genus Pogonomyrmex. Previous studies of queen mating frequency in Pogonomyrmex have focused on monogynous (one queen per colony) species in the subgenus Pogonomyrmex. We performed a genetic mother–offspring analysis of mating frequency in Pogonomyrmex (Ephebomyrmex) pima, a queen-dimorphic species with dealate and intermorph queens that differ in colony structure (intermorph colonies contain multiple queens). Our results demonstrate that both dealate and intermorph queens of P. (E.) pima are typically single maters, unlike their congeners analyzed thus far. Polyandry appears to be a derived trait in Pogonomyrmex, but comparative tests between P. (E.) pima queen morphs and across the genus provide no evidence that it evolved as an adaptation to increase genetic diversity within colonies or to obtain more sperm, respectively.     

Division of labor and the evolution of task sharing in queen associations of the harvester ant<Emphasis Type="Italic"> Pogonomyrmex californicus</Emphasis>

Division of labor is a key factor in the ecological success of social groups. Recent work suggests that division of labor can emerge even without specific adaptations for task specialization and that it can appear in incipient social groups as a self-organizational property. We investigated experimentally how selection and self-organization may interact during the evolution of division of labor by examining task performance in groups of normally solitary versus normally social ant queens. We created social pairs of colony-founding queens from two populations of the ant Pogonomyrmex californicus, one in which queens are normally solitary and one in which queens form foundress groups, and observed their behavior during nest excavation. In both populations, one of the two queens usually performed most of the excavation, becoming the excavation specialist. We could predict which queen would become the specialist based on their relative propensities to perform the task in other contexts, consistent with a variance-based model of task specialization. The occurrence of specialization even when group members were not adapted to social life suggests that division of labor may well have been present in incipient queen groups. However, division of labor can result in cost skew among group members, and thus, paradoxically, within-group selection may constrain or even reduce specialization. Consistent with this effect, pairs of normally solitary queens were significantly more asymmetrical in their task performance than normally social pairs, in which both queens nearly always performed the behavior to some degree.Communicated by J. Heinze     

Sex allocation ratios in the facultatively polygynous ant, Leptothorax acervorum

We investigated sex allocation in a central European population of the facultatively polygynous ant Leptothorax acervorum. The population-wide sex ratio was found to be quite balanced, with a proportional investment in female sexuals of 0.49. Sex allocation varied considerably between colonies, resulting in split sex ratios. The productivity of colonies was negatively correlated with queen number and positively with colony size. In contrast, the sex ratio (proportional investment in female sexuals) was neither correlated with queen number, colony size, nor total sexual production, but with worker relatedness. The uncoupling of the genetic colony structure and queen number presumably results from frequent queen turnover and colony splitting.     

Parasitic flies (Diptera: Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant,Atta cephalotes (Hymenoptera: Formicidae)

Summary Three lines of evidence, including interspecific comparisons, temporal division of foraging between size castes, and experimental manipulations, suggest that the diurnal parasitoid Neodohrniphora curvinervis (Diptera: Phoridae) influences both the caste sizes and numbers of leaf-cutter ants (Atta cephalotes) that leave their underground nests to collect leaves. At Parque Nacional Corcovado in Costa Rica, A. cephalotes was attacked by Neodohrniphora during the daytime, and foraged less during the day than at night; a closely related ant at the same site, A. colombica, had no phorid parasites and foraged exclusively during the day. Most daytime foragers of A. cephalotes were smaller than the lower size threshold for attack by Neodohrniphora, while nocturnal foragers, active when parasitoids were absent, were both larger than this threshold and within the energetically optimal size range for foraging. When I supplied artificial lighting to allow phorids to hunt at A. cephalotes colonies past dusk, ants foraged less than when light was provided but flies were removed. The influence of Neodohrniphora on the foraging activity of A. cephalotes may explain why investigations focusing on abiotic factors have largely failed to discover what drives this ant's daily foraging cycles, and suggests that forager sizes are influenced not only by energetic efficiency, but also by the threat of parasitism.     

The relation between caste ratios and division of labor in the ant genus Pheidole (Hymenoptera: Formicidae)

Summary Ten species of Pheidole, representing as many species groups from various localities in North and South America, Asia, and Africa, were analyzed to probe for possible relationships between caste ratios and division of labor.Minor workers are behaviorally almost uniform among the species, but major workers vary in repertory from 4 to 19 behavioral acts (Table 1, Fig. 2). The major repertory size increases significantly across the species with the percentage of majors in the worker force (Fig. 3). This trend is consistent with the basic prediction of ergonomic optimization models under an assumption of colony-level selection. There is also a trend toward reduction of behavioral repertory with increase of size in the major relative to the minor, a second relation expected from theory, but the data are not sufficient to reach statistical significance.When the minor:major ratio was lowered to below 1:1 (from the usual 3:1 to 20:1, according to species), in three widely different species (guilelmimuelleri, megacephala, pubiventris), the repertory size increased by 1.4–4.5X and the rate of activity by 15–30X (Table 1, Figs. 4–6). The change occurred within 1 h of the ratio change and was reversed in comparably short time when the original ratio was restored.This abrupt and important shift in behavior permitted the major workers to serve as an emergency stand-by caste, available to be summoned to a nearly full repertory when the minor worker caste was depleted. The majors also restored 75% or more of the missing minor workers' activity rate under laboratory conditions. Their transformation allowed continued oviposition by the queen and the rearing of larvae to the adult stage.In line with these findings, a distinction is made between programmed elasticity in the repertory of individual workers and castes and the resiliency of the colony as a whole, which depends upon the pattern of caste-specific elasticity.     

Polydomy and sexual allocation ratios in the ant Myrmica punctiventris

Summary Colony structure and reproductive investment were studied in a population of Myrmica punctiventris. This species undergoes a seasonal cycle of polydomy. A colony overwinters in entirety but fractionates into two or more nest sites during the active season and then coalesces in the fall. Colony boundaries were determined by integrating data on spatial pattern, behavioral compatability, and genetic relatedness as revealed by protein electrophoresis. Colonies contained at most one queen. Consequently, a colony consisted of one queenright nest and one or more queenless nests. Furthermore, estimates of relatedness were fully consistent, with queens being single mated. M. punctiventris therefore has a colony genetic structure that conforms to the classical explanation of the maintenance of worker sterility by kin selection. Kin selection theory predicts that workers would favor a female-biased allocation ratio while selection on queens would favor equal investment in males and females. We predicted that in polydomous populations, queenless nests would rear more female reproductives from diploid larvae than queenright nests. There was a significant difference between queenright and queenless nests in sexual allocation; queenless nests allocated energy to reproductive females whereas queenright nests did not. At neither the nest nor colony levels did worker number limit sexual production. We also found that nests tended to rear either males or females but when colony reproduction was summed over nests, the sexes were more equally represented. The difference in allocation ratios between queenless and queenright nests was attributed solely to queen presence/absence. Our work shows that polydomy provides an opportunity for workers to evade queen control and thereby to sexualize brood.Offprint requests to: L.E. Snyder at the current address     

Parentage and sex allocation in the facultatively polygynous ant Myrmicatahoensis

Most social groups have the potential for reproductive conflict among group members. Within insect societies, reproduction can be divided among multiple fertile individuals, leading to potential conflicts between these individuals over the parentage of sexual offspring. Colonies of the facultatively polygynous ant Myrmicatahoensis contain from one to several mated queens. In this species, female sexuals were produced almost exclusively by one queen. The parentage of male sexuals was more complex. In accordance with predictions based on worker sex-allocation preferences, male-producing colonies tended to have low levels of genetic relatedness (i.e., high queen numbers). Correspondingly, males were often reared from the eggs of two or more queens in the nest. Further, over half of the males produced appeared to be the progeny of fertile workers, not of queens. Overall investment ratios were substantially more male biased than those predicted by genetic relatedness, suggesting hidden costs associated with the production of female sexuals. These costs are likely to include local resource competition among females, most notably when these individuals are adopted by their maternal nest. Received: 3 March 1998 / Accepted after revision: 20 June 1998     

Between-caste aversion as a basis for division of labor in the ant Pheidole pubiventris (Hymenoptera: Formicidae)

Summary When deprived of minor workers under expermental conditions, major workers of the ant Pheidble pubiventris dramatically increase their repertory and rate of activity, and the change is due in good part to the greater attention they pay the brood. When minor workers are reinstated in appropriate numbers, the majors reduce their attention to the immature stages to the ordinary, low levels. Their response consists of the active avoidance of minors while in the vicinity of the immature stages. However, majors do not turn from other majors near the brood as much as they do from the minors, and they do not avoid minors at all while in other parts of the nest. In addition, minors do not avoid either minors or majors anywhere in the nest. The result is a striking division of labor with reference to brood care.