1. Introduction

Ant queens and workers usually belong to the reproductive or non-reproductive caste. However, ants can also switch from one caste to the other, resulting in the occurrence of many degrees of reproduction. A number of reproductive strategies may occur within a colony, such as monogyny and polygyny, or single or multiple inseminations of queens. Moreover, colony productivity can be influenced by many factors, such as the relatedness between queens and workers, and the rate of production of new workers. Social structure and the life history of ant colonies are very complex; yet, we suggest that the rate of production of eggs is a key feature.

The objective of this review is to assess the impact of egg laying on overall colony functionality and survival. We address this question by two main methodologies: first, we compile different studies on specific aspects of egg production. We aim to confirm the key idea of the importance of egg production by critically examining these studies. Second, we develop our observations using a current model on the allocation of work in insect societies to support the idea of the central position of egg laying in ant societies. We conclude that fecundity is a key feature, with many consequences on a colony’s functionality and dynamics. In ant societies, both the queen and the workers can be involved in producing eggs. The assessment of the consequences of egg production by the queen and workers may help us to understand the various roles played by eggs.

2. Ant Reproduction and Colony Structure

Ants are highly structured in terms of the roles that members of a colony fulfill, and many ant species’ colonies are headed by a reproductive queen. There is generally a reproductive division of labor within the ant societies, with potential egg producers (queens) typically engaging less in work performed by infertile female-only workers. However, worker-only reproductive strategies also exist. In some species, worker-produced individuals may bear genetic similarity to the workers performing the care. The species-specific reproductive behavior often represents a trade-off between high investment in one’s own reproduction to secure genetic representation in future generations and low investment in reproduction to help maintain colony survival. Colonies of ants are characterized by a complex social organization. They may not feature a single reproductive individual within the reproductive division of labor; one (or more) egg-laying queen dominates the egg production and, as a result, the reproductive offspring in a colony. Various terms have been defined to describe different forms of multifemale social structure and reproduction in social Hymenoptera. Ants conform to the definition of elementary societies in which the socioeconomic ratio of individuals is advanced by groups of females working together, rearing brood, and orchestrating foraging, defense, and reproduction. In most post-emergence eusocial Hymenoptera (typified by ants, bees, and wasps), the reproductive female (usually a single mother queen) has precedence over reproduction and can, in the absence of a queen, affect the reproduction of her fellow workers. This involves repeating a fraction of the total workload carried out by workers that differ phenotypically and in terms of reproductive physiology from the queen. In some societies, the ‘queen’ behavior is expressed facultatively through reproductive dominance, while in others it is fixed via irreversible changes prohibiting reproduction by the workers. Effective communication among colony members via long-term pheromones enhances colony regulation and contemporary nest-mate recognition, which balances reproductive unit contribution while reducing conflicts as well as production, and intra-specific and inter-specific host exploitation. Going into the reproductive season, proper anticipation of individual contribution to queen replacement can be identified through the ovarian development of workers with regressed sugar glands.

2.1. Queen Ants

Queen ants are specialized for reproduction and egg-laying. Many adult ants in a colony are sterile female workers who forage for food, care for brood (eggs, larvae, and pupae), and maintain the nest. The production of male ants and future queens is the queen’s responsibility. In addition to her reproductive status, the fecundity of a queen often sets her apart from other adult females in a colony. Queens are equipped with a spermatheca that receives and stores sperm after mating, and she uses this sperm during her lifetime to fertilize eggs. Queens can lay both male and female eggs to produce male and female ants, or singly lay unfertilized eggs that will develop into haploid males.

Following a single period of mating, queens of many ant, bee, and wasp species are able to lay eggs for much or all of their remaining lives. As with any reproductive organ, the spermatheca has an upper limit on how much sperm it can store, and the number of fertilizations in the queen’s lifetime may vary among species. Egg-laying by an ant queen may decrease over time; however, in part because stores of sperm in the queen’s spermatheca become depleted. Because a majority of the queen’s offspring are by definition female workers, the remaining fertilizations in the queen’s lifetime often involve male-producing eggs. All else equal, more fertile queens are expected to produce more worker-destined eggs, increasing a colony’s workforce. In addition, maintaining a high number of workers is advantageous because a larger worker force may be better able to find and hoard new nest sites should the need arise.

2.2. Worker Ants

Due to the strict life history rules that define ant colonies, worker ants are of reproductive significance, allowing for many subsidiary effects of reproduction in animal societies. Their reproductive value can be shown from an indirect angle by analyzing the tasks workers perform that shape the reproductive output of a colony. In a natural colony, the majority of tasks consist of brood care, foraging, and housekeeping, all of which directly or indirectly affect reproduction. As such, nest construction and maintenance facilitate egg laying, and patrolling of the nest surroundings and foraging primarily provide an income of resources to rear brood and directly or indirectly to feed queens. The basic capability of workers to eventually produce eggs is demonstrated by cases of worker reproduction from laying worker colonies where no queen is present, triggering social closure. Thus, worker egg laying seems a natural consequence if queens die or decay in ant colonies.

Their egg-laying ability is not the most important aspect of worker reproduction, as it is quickly perceived and sanctioned by workers. Instead, evidence from macrogynes shows that worker initiation, i.e., the performance of tasks by workers that prepare egg-laying by the gamergyne, plays an important role in maintaining colony cohesion. This signifies how the tasks are of more reproductive importance than the egg-laying ability itself. Here again, the importance is in a flexible adaptation to the peculiar ecology, where worker tasks include ground patrolling, leading foraging trails, and, most importantly, assuming a central task in brood rearing.

3. Egg Laying Behavior

Ants exhibit a variety of behaviors at high egg development rates. First of all, they must oviposit more to produce more eggs early in life. They may suppress ovarian development at first to focus on brood care, maintaining high egg-laying levels in subsequent seasons. Ant egg-laying rates may be synchronized by cues such as rainfall, day length, temperature, and food availability, and changes may occur in response to declining food availability. One common pattern in temperate ant species is that workers oviposit few egg cells in the spring, as food is of moderate availability; more egg cells are deposited in the summer when food is more available. As the reproduction season ends in the late summer and autumn, as worker numbers decline, fewer egg cells are produced.

In ant colonies with a single queen, worker reproduction is lower than normal. If the queen is lost or the single queen is divided into several mated brothers, workers often reproduce and produce eggs. The presence of a potential reproduction-inhibiting queen may therefore suppress worker egg laying. In environments with moderate to high reproduction, ant colonies are more likely to lay eggs and produce new workers than colonies with low reproduction. If egg laying is costly, then food-rich colonies are more prone to lay eggs, and pairs of workers produce more eggs than poor food colonies. Egg laying should also be most profitable for longer-lived ants, since there is a greater chance that they will oviposit. In the case of social ants, we can quantify the range at which responses to these various environmental and social cues might impact reproduction in species with known bicolony characters, and therefore intrinsic colony size.

4. Egg Development and Life Cycle

In ants, like other holometabolous insects, the egg is the only stage that develops within the body of reproductives (queens). Eggs are laid directly into brood chambers, and the external environment around them plays a crucial role in the developmental process. In most species, a single unfertilized egg develops into a haploid male, whereas fertilized eggs develop into diploid females that can also become queens depending on the caste determination system of the species. Egg laying and all the subsequent stages in the life cycle are well integrated because the yield of new colony members is crucial to the success and maintenance of a colony. In part due to the fact that reproductive success and dynamics of life cycles can vary greatly between species, the number and quality of brood room construction and utilization strategies are extremely variable.

The fertilized ant egg is produced within a queen’s body and laid only after being fertilized by a male. In most species, she produces eggs through a process called meiosis, which allows eggs to receive a copy of each parent’s chromosomes, resulting in a fertilized diploid egg. The first zygotic events, or formation of a new and distinct nuclei and distribution of allotment of non-identical chromosomes, occur during initial egg development. Over time, the egg undergoes rapid developmental events that transform its molecular state from a totipotent cell to a differentiating cell and finally, within the female worker body, to a fully phenotypically female or male ant. The embryonic period may take days, but can also be postponed by the queen in search of optimal external conditions. The ant egg becomes a larva when the first external differences are visible. A larva is an immobile feeding and growth phase, and when the full-sized ant forms and hardens, it becomes a pupa. Its entire development can range from days in some species to weeks or months in others. In most non-social insects, nutritional differences are fundamentally responsible for establishing cast differences, first during larval growth and again post-metamorphosis. In ant colonies, interactions among colony members are also essentially necessary for differentiation into fertile queens and infertile workers. The time spent as an egg, larva, and pupa is critical in the development of a full worker or mother (queen) ant. Organogenesis and differentiation take place mainly during the egg and larval phase, respectively, and post-pupa stages consist mainly of growth and some organ reorganization. At the end of pre-adult periods, the gaster and cuticle expand and harden in the pupa’s last soft stage. A bivoltine cycle, in which a majority of brood develops two envelopes over several generations, is characteristic of temperate Pharaoh ants. These life cycle preferences are likely ultimately set by queen physiology and food availability, and food opportunities appear to be largely constant because both forage outside the nest. Queen rearing is the best way for a colony to grow and replace and likely impacts other primary brood room activities due to resource limitation at the nest site.

5. Impacts of Egg Production on Colony Success

Egg production is considered to be of major importance for the success of ant colonies. The number of eggs produced by a colony is typically strongly correlated with the total number of inhabitants and the intrinsic rate of increase, pointing to the prime importance of egg output for colony success. Egg production rates are expected to be influenced by environmental factors, above all food availability, which affects the resources available for the production of eggs and for the survival of the workers responsible for brood care. Another potentially important factor is the intensity of competition among colonies, as strong intraspecific competition may lead to overpopulation of the environment and increased environmental stress. Pioneering colonies and ecological opportunists typically show high numbers of eggs available, whereas eggs are rare in established, longer-lasting colonies. Two major consequences of increased egg production can be distinguished: First, the ability to re-expand after a decline in colony size is indeed the result of egg-laying workers. Second, the production of many eggs can contribute to increased colony success and a demographic drive due to a high intrinsic rate of increase.

In turn, the factors which cause eggs to be rare in established, longer-lasting colonies include environmental factors such as food shortage or drought. Eggs are the most valuable and delicate individuals in a colony, for they are an investment in the future, and a strategy leading to the production of relatively high numbers of eggs will lead to a prevalence of eggs and young larvae. The original function of eggs may be to increase the viability of the colony in the long term, by contributing to increased colony resilience against environmental stressors. In fact, when conditions become too severe, older workers will voluntarily or ‘altruistically’ stop laying eggs.