The Adaptive Evolution of Ants

Introduction

Picnickers are very familiar with ants. It seems that within 20 minutes or less after sitting down to a snack in virtually any city park around the world, these insects begin to swarm one’s blanket with ever-greater numbers. It has been estimated that ants represent a far greater proportion of the biomass in New York’s Central Park than do humans. In fact, ants alone constitute more than 20 percent of the terrestrial biomass in Brazil’s amazon rainforests, a region famous for its incredible diversity of life (Wilson 1978, p.13).

Ants don’t just affect humans. Red Imported Fire Ant, Solonopsis invicta, first was introduced to the United States in about 1929 at Mobile, Alabama. This species has since spread north to Tennessee, west to Texas, and East to Florida and the Carolinas (Vinson 1997). In the process, nearly all other species of native ants have been driven away (Morris 1993). These ants have become the dominant predators of invertebrates in areas in which they are entrenched, and significantly lower species diversity. They have also been known to attack turtles, chameleons, snakes, newborn birds, and small mammals (Vinson 1997). Water-bird nesting success has been reported to be down 34% in areas infested with S. invicta (Dickinson 1995).

Ants (Hymenoptera: Formicidae) are one of the most dominant families of organisms on the planet. How did ants evolve? Why, from an evolutionary point of view, do worker and soldier ants give their lives to protect the colony and its queen(s)? Do individuals of other social species behave in a similar way for similar reasons?

Truly social, or eusocial, animals were defined by E. O. Wilson (1975) as having three defining characteristics: "(1) individuals of the same species cooperate in caring for the young; (2) there is a reproductive division of labor, with more or less sterile individuals working on behalf of fecund nestmates; (3) and there is an overlap of at least two generations in life stages capable of contributing to colony labor, such that offspring assist parents during some period of their life." Though some debate surrounds this definition due to parallels found in colonial breeding mammals and birds (e.g. Crespi and Yanega 1995; Sherman et al. 1995), it is clear that ants fall within this category: (1) Ant colonies feature nurses, typically recently emerged individuals, which care for eggs, larvae, and the queen (Vinson 1997). (2) Mature ant colonies, in general, feature one queen who is mother to the sterile caste of wingless workers, as well as to a winged reproductive caste, the alates, which are produced during mating season (Vinson 1997). The worker caste itself typically consists of various sized individuals, the largest of which are called soldiers, as their primary function is protection of the nest from assault (Futuyma 1998). (3) Ants are holometabolous, going through a series of larval stages prior to metamorphosing into an adult. These larval stages are not necessarily passive, however. Fourth instar fire ant larvae are essential to the colony, as they are responsible for the extraoral digestion of proteins, which are then fed to the workers and queen (Vinson 1997). Larvae of weaver ants (Oecophylla) are manipulated by workers to produce silk, which is then used to bind leaves together when forming a nest (Futuyma 1998). Adult workers also go through stages of development. Newly emerged workers, as mentioned above, usually become nurses. They soon graduate, typically within three weeks, to reserves, which are responsible for colony sanitation and defense. Finally, some workers will then graduate into foragers. These individuals leave the nest in search of food sources for the colony.

Richard Dawkins argues in his book The Selfish Gene (1989) that evolution can be reduced to competition among macromolecules, namely polynucleotides, for replication substrates. Organisms as we know them, such as plants, animals, or bacteria, are really nothing more than "machines" to transport, protect, and ultimately replicate DNA. Therefore, it is not surprising to see instances in which animals behave selfishly toward members of their own species, perhaps even killing conspecifics, if that behavior adds to the reproductive success of the individual. For example, when a male lion overthrows another male for control of a pride, infanticide is common. By killing off the cubs of the previous dominant male, the pride will no longer be encumbered with the costs of raising offspring that are not related to the new alpha male. Only his offspring will share his genome, and thus the male acts "selfishly" to prevent spending resources on unrelated offspring.

The more surprising cases, in fact, are those in which animals behave altruistically. Ants are prime examples of altruism. Everything the workers do, even to the point of sacrificing their lives, is for the good of the colony. Workers do not even reproduce. Why are they willing to give their lives, and thus end their "personal" lineage, for the good of other workers and the queen?

The answer seems to lie in the theory of inclusive fitness, which is credited to W. D. Hamilton (1964). His paper is primarily based on the coefficient of relationship, which had previously been used to illustrate the relationship between parents and offspring. He used mathematical models to illustrate that siblings, cousins, and neighbors also had a coefficient of relationship. Therefore, altruistic behavior toward relatives can be explained as an effort to conserve one’s own genome. This process of perpetuation of one’s own genome by helping one’s relatives has come to be called "kin selection."

Hamilton then applied his theory of inclusive fitness to Hymenopteran societies. As sterile worker caste members do not reproduce, the only method of transmission of their genome is to support the queen, even if it means personal sacrifice. In this way, workers literally do serve for the good of the colony, and in doing so, provide for the only possible method of transmission of their genome to future generations. Indeed, ants may be more disposed to kin selection than normal, due to their genetical method of sex determination. Typically among diploid organisms, offspring receive one of each pair of chromosomes from each parent. Therefore, each sibling has a relation coefficient of ½ to one another. Hymenopterans, however, are unique in that they have evolved a haplodiploidy sex determination mechanism, in which males are haploid and females are diploid. Therefore, all female offspring of a mated pair, which includes the female worker caste, will receive the same genetic information from their father, and thus each daughter shares a ¾ relation coefficient with the other – a closer relationship than they share with their mother. Therefore, haplodiploid individuals that become part of a social caste specialized for the rearing of sisters would experience a selective advantage, as their genes would have a greater prevalence in the gene pool due to this close relationship with their true sisters (Wilson 1978; Queller et al. 1993).

In nature, however, things get a little more complicated. In many species of ants, foundresses, females who have completed their mating flights, team up in foundress associations. They live within the same colony and all produce offspring. It has been hypothesized that, because of the high mortality rate among new queens (99%; Vinson 1997), there is a selective advantage to foundress associations as these new colonies will be able to defend themselves against raiders more quickly due to increased reproductive output (Pamilo et al. 1997). As the colony matures, however, the workers eventually rebel, killing all but one of the queens. Though typically the lone survivor is the most prolific egg laying queen, this is not always the case. More than likely, the queen is chosen by other traits, such as body size or physical condition. One can see that the strongest queen is also likely to be the most successful egg layer, and thus this behavioral trait of queen assassination could evolve through selective advantage.

Some species of ants have evolved polygyne colonies, in which several, frequently unrelated queens share a colony (Pamilo et al. 1997). One common example of polygyne colonies can be seen in the introduced strain of S. invicta in the United States. Interestingly, this social trait was very uncommon back in Argentina, the ancestral range of S. invicta (Ross et al. 1996a), and queens of monogyne colonies have a specific genetic difference, the Pgm-3a allele, when compared to queens of polygyne colonies (Keller and Ross 1993; Ross et al. 1996b). Queens of polygyne colonies typically produce fewer offspring than do queens in monogyne colonies. However, the sum total of their efforts produces an enormous colony very quickly – but also a colony with different matrilines (Vinson 1997). How can their cooperative efforts be explained by the inclusive fitness theory if the workers are not even related?

One possibility is that the current social conditions in colonies do not reflect those that would be found at the "dawn of sociality" (Pamilo et al. 1997). When ants evolved from wasps, probably in very small populations, monogyne colonies may have been the norm, and workers in those colonies would have all been full sisters (coefficient of relationship = ¾). Once eusociality was established in the ants, certain behavioral traits evolved that conveyed further selective advantage on the population. For example, Liersch and Schmid-Hempel (1998) found in field studies that colonies of bumble bees made up of closely related individuals have higher parasite loads than colonies with more distantly related members. This could convey a selective advantage on more heterogeneous colonies that work together in a eusocial manner. O’Donnell (1997) has proposed that some parasites may even act directly to promote social behavior by "parasitically castrating" individuals within a population. If the parasite had low intra-populational transmission rates, it is possible that individuals rendered sterile by the parasite would experience a selective advantage, via kin selection theory, by promoting the reproduction of a relative.

Brood raids, as seen in S. invicta (Vinson 1997), could also be one of these adaptive behavioral traits. Young colonies will send workers on brood raids to bring back the larvae of a neighboring colony. These raids, when successful, allow a young colony to build up its supply of workers very quickly. The "captured" workers serve the colony as if it were their own, not because they are enslaved, but because they don’t know any better. The workers do not calculate the coefficient of relationship between themselves and their peers, but instead behave as they have been selectively molded to act – they live to serve the colony, whether such an action increases their inclusive fitness or not (Ratnieks and Reeve 1992).

As evidence for the inclusive fitness theory explanation, it would be expected that in colonies in which workers are highly related to one another (typically monogyne colonies), the proportion of female to male offspring would typically be about 3:1 (¾ female). However, in colonies with multiple queens, and thus multiple matrilines, proportions of males to females would be expected to drift towards 1:1, as worker females would not be as closely related to one another, and thus would not select female larvae as strongly. Indeed, this is exactly what was found in a survey by Seger (1991) of 49 species of ants (Futuyma 1998).

While the inclusive fitness theory provides an evolutionary framework for the viability of eusociality, it does not explain the dominance of social insects, particularly the ants. Two theories have been offered to explain this phenomenon. Oster and Wilson (1978) proposed that this could be due to the efficient task organization that is evident in these species. Indeed, as described above, individuals of different sizes and different ages perform very different tasks, all of which are necessary for a strong and stable colony.

Queller (1994) proposes that another factor may be the extended parental care evident in eusocial organisms. Parental care allows large numbers of individuals to be turned out with high efficiency. Indeed, when one observes nurse worker ants tending to larvae in an ant colony, one cannot help but be struck by the parallels to the assembly lines of the manufacturing industry. Both allow massive productivity and high efficiency, which, in turn, lead to dominance in their respective competitive environments.

While kin selection offers a very parsimonious theory by which eusociality can evolve, several other hypotheses have been proposed that do have some experimental backing and thus may also play a role (Futuyma 1998). Alexander (1974) proposed that the queens suppress the reproduction of some of their offspring so those individuals will assist in rearing other, more fertile, offspring. It seems reasonable to believe that this process could begin in a small population where a limited number of individuals were, by disease or defect, sterile at birth. There could be a strong selective advantage for those individuals to assist relatives in the rearing of young, provided, of course, some stimulus could evolve to signal an individual ant that she is not fertile.

A third hypothesis offered by West-Eberhard (1978) suggests that eusociality may be maintained by mutualism. Workers may be what she terms "cryptic reproductives" or "hopeful reproductives," and thus may achieve greater "personal" reproductive success by assisting the colony (Futuyma 1998).

Other Supporting Examples and Parallels

Many other species of insects are considered eusocial, including certain species of aphids, weevils, and thrips, as well the entire order Isoptera and many families of Hymenoptera, which include the ants (formicidae; Sherman et al. 1995). While only members of Hymenoptera possess haplodiploid sex determination, inclusive fitness theory provides a selective mechanism for the evolution of these "societies" as well.

Insects are not the only group of organisms that are eusocial. The naked mole rat, a rodent, is by all accounts a eusocial organism, complete with social castes and a queen in each colony. Many other species of mammals and birds come very close to eusociality during communal nesting. For example, the Florida Scrub Jay, Aphelocoma coerulescens, is a cooperative breeder, in which nonbreeders (typically younger birds) "help" older birds by protecting a mutual territory, gathering food, and (occasionally) feeding the young (Burt and Peterson 1993).

The behavior of our own species may also have been influenced by kin selection. E. O. Wilson (1978) has proposed that the high prevalence of homosexuality in human cultures around the world may be the result of some selective advantage early in the evolution of humans. Perhaps they served as a "helper caste," to the small closely related tribes of early humans. If the presence of homosexuals in a tribe relieved some of the burden of rearing children from close relatives, homosexuality could have been a selected trait. Interestingly, even though Western culture shuns homosexuality, more "primitive" cultures, such as Native Americans, hold them in great respect. Many become the Shaman of tribes, the medicine man, a position of great importance.

Ants are one of the most dominant terrestrial animals, and have a highly organized social system involving sterile worker castes that serve the colony so that the numerically smaller reproductive caste may reproduce. This seems, at first glance, to violate one of the most fundamentally important "rules" in biology: that the most important reason for eating, avoiding predators, and courting a mate (in sexually reproducing organisms) is to reproduce, thus passing on one’s genes to the next generation. However, Hamilton’s inclusive fitness theory, also known as the theory of kin selection, helps to understand this dilemma. By assisting close relatives to survive and reproduce, one can increase one’s own reproductive output indirectly. Haplodiplody makes such pressures even greater in Hymenoptera, of which ants are a large family. Female ants have a coefficient of relationship of ¾ with their true sisters, and therefore experience strong selective advantages when behaving in an altruistic manner that allows more sisters to be produced. Eusociality, which evolved through kin selection, provided the social framework in which an enormous host of very complex behaviors could evolve, such as the farming of aphids for dewdrops or sewing together of leaves to form arboreal nests. Amazingly, all these complex, cooperative behaviors are accomplished by selfish individual ants that act for one overriding purpose – the continued perpetuation of their own genes.

Copyright © 1999 Justin W. Merry All Rights Reserved

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