Harvester Ant Pogonomyrmex Californicus Research Articles

Genome assembly and annotation of the California harvester ant Pogonomyrmex californicus.

The harvester ant genus Pogonomyrmex is endemic to arid and semiarid habitats and deserts of North and South America. The California harvester ant Pogonomyrmex californicus is the most widely distributed Pogonomyrmex species in North America. Pogonomyrmex californicus colonies are usually monogynous, i.e. a colony has one queen. However, in a few populations in California, primary polygyny evolved, i.e. several queens cooperate in colony founding after their mating flights and continue to coexist in mature colonies. Here, we present a genome assembly and annotation of P. californicus. The size of the assembly is 241 Mb, which is in agreement with the previously estimated genome size. We were able to annotate 17,889 genes in total, including 15,688 protein-coding ones with BUSCO (Benchmarking Universal Single-Copy Orthologs) completeness at a 95% level. The presented P. californicus genome assembly will pave the way for investigations of the genomic underpinnings of social polymorphism in the number of queens, regulation of aggression, and the evolution of adaptations to dry habitats.

The foundress’s dilemma: group selection for cooperation among queens of the harvester ant, Pogonomyrmex californicus

The evolution of cooperation is a fundamental problem in biology, especially for non-relatives, where indirect fitness benefits cannot counter within-group inequalities. Multilevel selection models show how cooperation can evolve if it generates a group-level advantage, even when cooperators are disadvantaged within their group. This allows the possibility of group selection, but few examples have been described in nature. Here we show that group selection can explain the evolution of cooperative nest founding in the harvester ant Pogonomyrmex californicus. Through most of this species’ range, colonies are founded by single queens, but in some populations nests are instead founded by cooperative groups of unrelated queens. In mixed groups of cooperative and single-founding queens, we found that aggressive individuals had a survival advantage within their nest, but foundress groups with such non-cooperators died out more often than those with only cooperative members. An agent-based model shows that the between-group advantage of the cooperative phenotype drives it to fixation, despite its within-group disadvantage, but only when population density is high enough to make between-group competition intense. Field data show higher nest density in a population where cooperative founding is common, consistent with greater density driving the evolution of cooperative foundation through group selection.

Distribution and origin of intraspecific social variation in the California harvester ant Pogonomyrmex californicus

The California seed harvester ant Pogonomyrmex californicus exhibits striking differences in queen behavior and colony organization throughout its range. Most populations show the likely ancestral condition of single-queen colonies (monogyny). However, in one known population, cooperation between queens during colony founding (pleometrosis) occurs, and is suspected to persist to the mature colony stage (primary polygyny). To better understand this variation in social phenotype, we estimate relatedness among co-foundresses, measure the frequency of polygyny in adult colonies across three focal populations, and assess population genetic structure between populations. We additionally measure queen mating frequency (polyandry) across focal populations. With few possible exceptions, queens within pleometrotic associations are unrelated. We demonstrate a correlation between pleometrosis in incipient colonies and polygyny in adult colonies at the population level. Nuclear microsatellites and mtDNA barcoding indicate significant structure between focal populations. Queens from all three focal populations engage in relatively high levels of polyandry. These findings, when examined with previous data demonstrating that pleometrosis leads to polygynous colonies in the laboratory, strongly suggest that the same occurs in nature. However, the possibility of additional queen adoption in adult colonies (secondary polygyny) is not excluded. Thus, polygynous P. californicus colonies potentially represent long-term associations of unrelated family groups, containing multiple unrelated queens and their mixed-paternity offspring. Due to its pronounced variation in social behavior, P. californicus provides a unique opportunity to examine the evolutionary history and genetic underpinnings of cooperation among non-relatives, a strategy of intense interest in behavioral ecology.

Gene expression and variation in social aggression by queens of the harvester ant Pogonomyrmex californicus.

A key requirement for social cooperation is the mitigation and/or social regulation of aggression towards other group members. Populations of the harvester ant Pogonomyrmex californicus show the alternate social phenotypes of queens founding nests alone (haplometrosis) or in groups of unrelated yet cooperative individuals (pleometrosis). Pleometrotic queens display an associated reduction in aggression. To understand the proximate drivers behind this variation, we placed foundresses of the two populations into social environments with queens from the same or the alternate population, and measured their behaviour and head gene expression profiles. A proportion of queens from both populations behaved aggressively, but haplometrotic queens were significantly more likely to perform aggressive acts, and conflict escalated more frequently in pairs of haplometrotic queens. Whole-head RNA sequencing revealed variation in gene expression patterns, with the two populations showing moderate differentiation in overall transcriptional profile, suggesting that genetic differences underlie the two founding strategies. The largest detected difference, however, was associated with aggression, regardless of queen founding type. Several modules of coregulated genes, involved in metabolism, immune system and neuronal function, were found to be upregulated in highly aggressive queens. Conversely, nonaggressive queens exhibited a striking pattern of upregulation in chemosensory genes. Our results highlight that the social phenotypes of cooperative vs. solitary nest founding tap into a set of gene regulatory networks that seem to govern aggression level. We also present a number of highly connected hub genes associated with aggression, providing opportunity to further study the genetic underpinnings of social conflict and tolerance.

Behavioral transitions with the evolution of cooperative nest founding by harvester ant queens

Research on the evolution of cooperative groups tends to explore the costs and benefits of cooperation, with less focus on the proximate behavioral changes necessary for the transition from solitary to cooperative living. However, understanding what proximate changes must occur, as well as those pre-conditions already in place, is critical to understand- ing the origins and evolution of sociality. The California harvester ant Pogonomyrmex californicus demonstrates population-level variation in colony founding over a close geographic range. In adjacent populations, queens either found nests as single individuals (haplometrosis) or form cooperative groups of nonrelatives (pleometrosis). We com- pared aggregation, aggression, and tolerance of queens from one pleometrotic and two haplometrotic populations during nest initiation, to determine which behaviors show an evolu- tionary shift and which are present at the transition to pleometrosis. Surprisingly, within-nest aggregative behavior was equally present among all populations. In nesting boxes with multiple available brood-rearing sites, both queen types readily formed and clustered around a single common brood pile, suggesting that innate attraction to brood (offspring) facilitates the transition to social aggregation. In contrast, queens from the three populations differed in their probabili- ties of attraction on the ground to nest sites occupied by other queens and in levels of aggression. Our results suggest that

Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus

Colony size is a fundamental attribute of insect societies that appears to play an important role in their organization of work. In the harvester ant Pogonomyrmex californicus, division of labor increases with colony size during colony ontogeny and among unmanipulated colonies of the same age. However, the mechanism(s) integrating individual task specialization and colony size is unknown. To test whether the scaling of division of labor is an emergent epiphenomenon, as predicted by self-organizational models of task performance, we manipulated colony size in P. californicus and quantified short-term behavioral responses of individuals and colonies. Variation in colony size failed to elicit a change in division of labor, suggesting that colony-size effects on task specialization are mediated by slower developmental processes and/or correlates of colony size that were missing from our experiment. In contrast, the proportional allocation of workers to tasks shifted with colony size, suggesting that task needs or priorities depend, in part, on colony size alone. Finally, although task allocation was flexible, colony members differed consistently in task performance and spatial tendency across colony size treatments. Sources of interindividual behavioral variability include worker age and genotype (matriline).

Division of labor increases with colony size in the harvester ant Pogonomyrmex californicus

Size has profound consequences for the structure and function of biological systems, across levels of organization from cells to social groups. As tightly integrated units that vary greatly in size, eusocial insect colonies, in particular, are expected to exhibit social scaling relations. To address the question of how social organization scales with colony size, we quantified task performance in variably sized colonies of the harvester ant Pogonomyrmex californicus. We found a positive scaling relationship between colony size and division of labor in 2 different contexts. First, individual workers were more specialized in older, larger colonies. Second, division of labor increased with colony size, independently of colony age. Moreover, the proportional allocation of workers to tasks shifted during colony ontogeny—older, larger colonies performed relatively less brood care—but did not vary with colony size among same-aged colonies. There were no colony-size effects on per capita activity or the distribution of activity across workers. Size-related changes in task performance were correlated with changes in the rate of encounter between nest mates. These results highlight the importance of colony size for the organization of work in insect societies and raise broader questions about the role of size in sociobiology.

Endocrine physiology of the division of labour in Pogonomyrmex californicus founding queens

The proximate controls of a behaviour in extant species can inform us about the evolutionary route towards that behavioural phenotype. In social insects, different behavioural phenotypes often correlate with divergent hormone levels, and, in honeybees ( Apis mellifera ), this insight has lead to the hypothesis that behavioural biases, or division of labour, emerged via co-option of endocrine regulatory systems that paced behavioural change during the reproductive cycle of solitary ancestors. Founding queens of the California harvester ant Pogonomyrmex californicus show discrete behavioural changes during colony founding, with a dichotomy between nest-biased behaviour and field-biased behaviour. Additionally, a division of labour can develop if queens found nests together, with one queen being nest-biased and another being field-biased. To determine whether behavioural diphenism can be associated with reproductive endocrine regulators in an ant, we measured ecdysteroid and juvenile hormone (JH) content in (1) single-founding queens showing normal behavioural progression and (2) cofounding queens showing a division of labour. We found that ecdysteroid levels did not correlate with behaviour. JH titres, on the other hand, were elevated during the foraging life stage of single-founding queens as well as in the cofounding queens with a behavioural bias towards foraging. Our results suggest that JH affects the propensity for foraging task replication in P. californicus , and provide evidence for a common evolutionary route towards social behaviour in ants and bees.

Influence of the social context on division of labor in ant foundress associations

Previous studies indicate that division of labor can arise spontaneously in social groups. The comparison between normally social populations and forced associations of solitary individuals allows us to dissect the mechanisms by which tasks are distributed within a group and to ask how selection acts on division of labor during the incipient stages of sociality. In some ant species, newly mated queens form cooperative associations during nest initiation, in which individuals specialize on different tasks. The harvester ant Pogonomyrmex californicus shows geographical variation across populations in colony-founding strategies: solitary founding (haplometrosis) and group founding (pleometrosis). This system provides a unique opportunity to investigate how social context affects division of labor during social evolution. We created groups containing normally solitary, normally group founding, or mixed groups of solitary and social queens to examine how social phenotype affects division of labor. We also examined how group size affects task specialization by comparing pairs of queens with groups of 6 queens. Division of labor arose consistently across all associations. Groups of haplometrotic or pleometrotic queens differentiated into an excavation and a brood care specialist. In mixed groups, the haplometrotic queens took the role of excavator whereas the pleometrotic queens mainly tended brood. Our data also show that the intensity of specialization was greater in larger associations, consistent with current models of group size and division of labor. We discuss these data in the context of how emergence and selection act on the evolution of division of labor within incipient social groups.

Division of labor and the evolution of task sharing in queen associations of the harvester ant Pogonomyrmex californicus

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.

Switching of metabolic-rate scaling between allometry and isometry in colonial ascidians.

The metabolic rate and its scaling relationship to colony size were studied in the colonial ascidian Botrylloides simodensis. The colonial metabolic rate, measured by the oxygen consumption rate (V(O2) in millilitres of O(2) per hour) and the colony mass (wet weight M(w) in grams) showed the allometric relationship (V(O2) = 0.0412 M(w)(0.799). The power coefficient was statistically not different from 0.75, the value for unitary organisms. The size of the zooids and the tunic volume fraction in a colony were kept constant irrespective of the colonial size. These results, together with the two-dimensional colonial shape, excluded shape factors and colonial composition as possible causes of allometry. Botryllid ascidians show a takeover state in which all the zooids of the parent generation in a colony degenerate and zooids of a new generation develop in unison. The media for connection between zooids such as a common drainage system and connecting vessels to the common vascular system experienced reconstruction. The metabolic rate during the takeover state was halved and was directly proportional to the colonial mass. The scaling thus changed from being allometric to isometric. The alteration in the scaling that was associated with the loss of the connection between the zooids strongly support the hypothesis that the allometry was derived from mutual interaction among the zooids. The applicability of this hypothesis to unitary organisms is discussed.

Reproductive conflicts in cooperative associations of fire ant queens (Solenopsis invicta)

In ants, unrelated queens frequently associate to initiate a colony cooperatively. The joint reproductive effort of the cofoundresses increases growth and survival of the incipient colony. However, such associations are unstable. Soon after emergence of the first workers, queen-queen and queen-worker fights lead to the death or expulsion of all but one cofoundress. Because no sexual offspring are produced in incipient colonies the surviving queen monopolizes the entire future reproductive success of the colony. Two factors, the queens9 relative fighting ability and their relative contribution to worker production (assuming that workers can recognize and selectively favour their mother) have been proposed to influence the survival prospects of individual queens within associations. The effect of these two factors was tested in the fire ant Solenopsis invicta. Initial size differences, a potential measure of the queens9 fighting ability, affected the outcome of the conflicts, so that the initially heavier queen was more likely to survive. Differential loss of mass by initially equal nestmates also affected survival, with the queen losing more body mass being more likely to die. The manipulation of the queens9 relative contribution to the worker brood did not significantly affect the queens9 survival probability, suggesting that workers are unable to favour their mother.

Mechanisms of Interference and Foraging Among Colonies of the Harvester ant Pogonomyrmex Californicus in the Mojave Desert

This report examines patterns of competition and foraging dynamics among colonies of the harvester ant Pogonomyrmex californicus. Two components of harvesting efficiency are defined: total harvesting efficiency (i.e., all food items considered) and seed harvesting efficiency (only seeds considered). Throughout the summer, total harvesting efficiency remained constant, whereas seed—harvesting efficiency exhibited an increase as a result of changes in the relative availability of the dominant seed crop, Erodium cicutarium. Several aspects of interference were studied. Colonies were uniformly spaced, and nest relocations significantly increased nearest—neighbor distance. Of encounters between ants from different colonies, 81% resulted in some form of aggression and 7% were fatal to one or both foragers. In a particular study, forager mortality rate was estimated at 0.06 deaths per ant foraging hour, thus indicating that such aggression may have a substantial impact on colony size. Furthermore, following an encounter involving physical struggle, ants returned to and remained in their nests for an extended period of time, thereby reducing seed input to the colony. The above—mentioned components of interference are examined to their potential effects on colony density, distribution, and size.