The ontogeny of selection on genetic diversity in harvester ants.

Selection may favour traits throughout an individual's lifetime or at a particular life stage. In many species of social insects, established colonies that are more genetically diverse outperform less diverse colonies with respect to a variety of traits that contribute to fitness, but whether selection favours high diversity in small colonies is unknown. We tested the hypothesis that selection favours genetically diverse colonies during the juvenile period using a multi-year field experiment with the harvester ant, Pogonomyrmex occidentalis. We used controlled matings to generate colonies that varied in genetic diversity and transplanted them into the field. We monitored their survival for seven (the 2015 cohort, n = 149) and six (the 2016 cohort, n = 157) years. Genetically more diverse colonies had greater survival, resulting in significant viability selection. However, in both cohorts survival was not influenced by genetic diversity until colonies were three years old. We suggest that changes in their internal organization enabled colonies to use the benefits of multiple genotypes, and discuss possible mechanisms that can generate this pattern.

The benefits of being big and diverse: early colony survival in harvester ants.

In sessile organisms such as plants and benthic invertebrates, founding propagules typically suffer extremely high rates of mortality due to both extrinsic and intrinsic factors. Many social insect species share similarities with these groups, but factors influencing early colony survival are relatively unstudied. We used a field experiment to measure the importance of environmental quality relative to intrinsic colony properties in the harvester ant, Pogonomyrmex occidentalis, by monitoring the survival of 584 experimental colonies. We measured survival of transplanted colonies over four months in each of three years (2014-2016) at a site in western Colorado. Colony survival was primarily determined by colony features. Multiple mating by the queen and larger colony size at the time of transplant increased survival, but queen size, maternal lineage and the composition of plant species in the vicinity of the colony did not. Food supplementation increased survival significantly when natural food was scarce, but was not consistently beneficial, in contrast to predictions. Our results emphasize the general importance of rapid growth and early attainment of large size in the survival of sessile species. However, attributes specific to ants that are a consequence of their sociality also strongly affected survival. Colonies with multiply-mated queens were more likely to survive over a wide range of circumstances, highlighting the importance of this trait even at the early stages of colony life.

Comparative advantage and caste evolution.

Most of the theory for the evolution of caste specialization in social insects assumes that increased efficiency in worker labor leads to specialization and increased worker efficiency gives colonies with behavioral specialists an advantage. However, there are an increasing number of studies that show that the task specialists within social insect colonies do not have the highest efficiency. Indeed, some studies show that some groups of workers are uniformly better than all other groups at every task. In this note, I adapt the principle of comparative advantage from economics to show that, rather than maximizing the payoff, specialization is advantageous when minimizing opportunity costs. This leads to the prediction that caste specialization should be associated with reduced opportunity costs rather than increased task efficiency.

Offspring Size and Reproductive Allocation in Harvester Ants.

A fundamental decision that an organism must make is how to allocate resources to offspring, with respect to both size and number. The two major theoretical approaches to this problem, optimal offspring size and optimistic brood size models, make different predictions that may be reconciled by including how offspring fitness is related to size. We extended the reasoning of Trivers and Willard (1973) to derive a general model of how parents should allocate additional resources with respect to the number of males and females produced, and among individuals of each sex, based on the fitness payoffs of each. We then predicted how harvester ant colonies should invest additional resources and tested three hypotheses derived from our model, using data from 3 years of food supplementation bracketed by 6 years without food addition. All major results were predicted by our model: food supplementation increased the number of reproductives produced. Male, but not female, size increased with food addition; the greatest increases in male size occurred in colonies that made small females. We discuss how use of a fitness landscape improves quantitative predictions about allocation decisions. When parents can invest differentially in offspring of different types, the best strategy will depend on parental state as well as the effect of investment on offspring fitness.

Inclusive fitness theory and eusociality.

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Patriline shifting leads to apparent genetic caste determination in harvester ants.

The harvester ant, Pogonomyrmex occidentalis, is characterized by high levels of intracolonial genetic diversity resulting from multiple mating by the queen. Within reproductively mature colonies, the relative frequency of different male genotypes (patrilines) is not stable. The difference between samples increases with time, nearing an asymptote after a year. Patriline distributions in gynes and workers display similar patterns of change. A consequence of changing patriline distributions is that workers and gynes appear to have different fathers. However, apparent genetic differences between castes are caused by changing paternity among all females. Temporal variation in the relative frequency of patrilines may be a consequence of processes that reflect sexual conflict, such as sperm clumping. Recent work documenting genotype differences between physical castes (workers and gynes; major and minor workers) in several species of ants has been interpreted as evidence of genetic caste determination. Reanalysis of these studies found little support for this hypothesis. Apparent caste determination may result from temporal variation in sperm use, rather than from fertilization bias among male ejaculates.

Dioecy and the evolution of sex ratios in ants.

Split sex ratios, when some colonies produce only male and others only female reproductives, is a common feature of social insects, especially ants. The most widely accepted explanation for split sex ratios was proposed by Boomsma and Grafen, and is driven by conflicts of interest among colonies that vary in relatedness. The predictions of the Boomsma-Grafen model have been confirmed in many cases, but contradicted in several others. We adapt a model for the evolution of dioecy in plants to make predictions about the evolution of split sex ratios in social insects. Reproductive specialization results from the instability of the evolutionarily stable strategy (ESS) sex ratio, and is independent of variation in relatedness. We test predictions of the model with data from a long-term study of harvester ants, and show that it correctly predicts the intermediate sex ratios we observe in our study species. The dioecy model provides a comprehensive framework for sex allocation that is based on the pay-offs to the colony via production of males and females, and is independent of the genetic variation among colonies. However, in populations where the conditions for the Boomsma-Grafen model hold, kin selection will still lead to an association between sex ratio and relatedness.

Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis.

Multiple mating by females characterizes most insect species, but is relatively uncommon in social insects. Females may mate with multiple mates because they experience the direct benefits of increased survival or fecundity, to acquire high quality mates, or to lower the risk of reduced fecundity by mating with incompatible males. We used the extensive natural variation in mating frequency in the western harvester ant, Pogonomyrmex occidentalis, to test the hypothesis that increased mating by the queen leads to an increase in colony performance. Colonies with greater genetic diversity began to forage earlier in the day and foraged for longer time periods. The workers which initiated foraging were a nonrandom subset of the genotypes present in the colony. We used a statistical approach to correctly predict the direction and magnitude of the correlation between genetic diversity and colony foraging activity.

Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis.

Using four highly polymorphic microsatellite markers (12-28 alleles), we gentoyped workers from 63 colonies of Pogonomyrmex occidentalis. Colonies have a single, multiply mated queen, and an average number of 6.3 patrilines per colony. Colony growth was measured over an 8-year period in the study population. Intracolonial relatedness and colony growth are correlated negatively, indicating a substantial fitness benefit to multiple mating.

Queen size mediates queen survival and colony fitness in harvester ants.

We examined the effect of queen size on the probability of new colony establishment in the ant Pogonomyrmex occidentalis. Large queens are significantly more likely to survive than small queens through the initial stages of colony founding. These differences in individual fitness correlates have corresponding effects on colony fitness. In species in which individual queens vary in fitness, sexual allocation ratios should incorporate the individual fitness functions.

Evolution of self-organized systems.

In this paper I ask questions about the evolution of self-organized activity cycles that are found in some ant colonies. I use a computer model that generates periodic activity patterns in interacting subunits and explore the parameters of this model using a genetic algorithm in which selecting on one aspect of the system produces the distinctive self-organized pattern. The general point that I explore, using the example of activity cycles, is that the observation of a self-organized pattern does not mean that the pattern is an adaptation. Self-organized patterns can represent nonadaptive correlated responses to selection, exaptations or even selectively disadvantageous traits. Evolution of self-organized patterns requires genetic feedback between the self-organized output and the subunits that produce the pattern. Without this necessary feedback, a self-organized system does not evolve.

Recruitment in the harvester ant, Pogonomyrmex occidentalis: effects of experimental removal.

We examined the importance of experimental removal of mature colonies on colony recruitment in the western harvester ant Pogonomyrmex occidentalis. To test the common assumption that established colonies suppress the establishment of new colonies we removed all colonies in ten 0.25 ha plots in 1996 and an additional five plots in 1997 and measured new colony recruitment in 1997, 1998, and 1999. Using a blocked, paired plot design we found that removal of colonies increased new colony recruitment in some areas of the site, but not others. Spatial variation in the importance of established colonies to recruitment was consistent across years; blocks in which density dependence was important in one year exhibited density dependent recruitment in following years. We estimated that in the blocks where recruitment was affected by established colonies, they accounted for less than 10% of the mortality of foundress queens. The increase in the number of new recruits (on average two additional new colonies) was considerably less than the number of colonies removed; average colony density in the removal plots was 14 colonies per 0.25 ha plot. The consistent lack of importance of established colonies to recruitment in one block and the relatively small response to colony removal in the other blocks suggests that the number of new colonies in a year may not be equivalent to the number of deaths of established colonies in that year. Space limitation is an important influence on recruitment in P. occidentalis, but the magnitude of the limitation varies spatially.

SEXUAL SELECTION ON BODY SIZE AND SHAPE IN THE WESTERN HARVESTER ANT, POGONOMYRMEX OCCIDENTALIS CRESSON.

Mating in social insects has generally been studied in relation to reproductive allocation and relatedness. Despite the tremendous morphological diversity in social insects, little is known about how individual morphology affects mating success. We examined the correlation of male size and shape with mating success in the western harvester ant, Pogonomyrmex occidentalis. Larger males had significantly higher mating success in two independent collections of males at mating aggregations. We also detected significant linear and nonlinear selection on aspects of male shape that were consistent across years. These shape components are independent of size, suggesting that male mating success is a complex function of size and shape. Successful males had elongate thoraxes and short mandibles relative to males collected at random at the lek. Overall, mated males also had longer postpetioles relative to body size, but there was also evidence of nonlinear selection on relative postpetiole length in both years. We found no evidence of assortative mating based on size or multivariate shape measures in either year, but in one year we found weak assortative mating based on some univariate traits.