The obligate slave-maker Polyergus breviceps (red ants) are readily distinguished from its host Formica argentea (black ants).
Polyergus breviceps workers returning from a slave raid.
¿Cómo funcionan las colonias de hormigas esclavizadoras?
Es imposible abordar la totalidad del comportamiento de toma de esclavos entre las hormigas siguiendo el desarrollo de una hormiga. Más bien, para comprender su sistema de trabajo, vamos a describir la ontogenia de un enjambre esclavizador.
Una colonia de Polyergus breviceps comienza como todas las otras colonias de hormigas lo hacen, con una sola reina apareándose e iniciando su vuelo nupcial .
La reina entrará en colonia objetivo de esclavizamiento, matará y sustituirá a la antigua reina. Una vez que ella ha asumido el poder, las hormigas de esta colonia la aceptarán como la nueva reina. Ella comenzará a poner sus propios huevos, que las trabajadoras cuidarán y para cuando las antiguas trabajadoras comienzan a morir, múltiples crías de su propia especie habrán desarrollado plenamente. En este punto, comienzan a asaltar las colonias cercanas de sus víctimas preferidas, las Formica argentea. Las larvas que capturan y traen de vuelta serán criadas por esclavas que quedan en su colmena para ser la próxima generación de trabajadoras. Este proceso continúa durante toda la vida de la colonia, ya que producen más reinas vírgenes que proceden a establecer colonias propias de la misma manera.
How do slavemaking colonies work?
It's impossible to address the entire behavior of slave making in ants through following the development of one ant. Rather, to understand the systems at work, we'll describe the ontogeny of a slave-making hive.
A Polyergus breviceps colony starts out as all ant colonies do, with a single queen mating and making her nuptial flight . The P. breviceps queen will enter the host colony, kill and replace the old queen. Once she has assumed the position of power, the ants of this colony will accept her as the new queen. She will start laying her own eggs, which the workers will tend to and by the time the old workers start dying off, multiple broods of her own P. breviceps will be fully grown. At this point, they start raiding nearby colonies of their preferred host, Formica argentea (19. Wild, A. 2010). The larvae they bring back will by raised by any remaining slaves in their hive to be the next generation of workers. This process continues for the lifetime of the colony as it makes more virgin queens that proceed to establish colonies of their own in the same manner.
En 1810 el naturalista suizo Pierre Huber publicó un libro fundamental en la historia de la mirmecología, la Historia de las hormigas. Entre otros descubrimientos, narró las razias o incursiones que realizan las obreras de Polyergus rufescens sobre los nidos de Formica fusca, de donde sacan innumerables pupas que trasladan al hormiguero. Estas pupas se convertirán en adultos que convivirán con la especie raptora, constituyéndose así una colonia mixta con reparto de funciones.A este comportamiento se le ha denominado, desde entonces, esclavismo. El impacto de este descubrimiento ha impulsado multitud de investigaciones y publicaciones, y su influencia se ha dejado sentir más allá del campo reducido de la mirmecología. El empleo del término “esclavismo” para referirse a esta conducta de las hormigas ha conllevado, en muchos casos, su asociación con la esclavitud humana, al extremo de utilizarse para justificar esta última.
Slave raids and colony takeovers
Polyergus workers will emerge from their nest (a mixed nest where Formica workers are already enslaved) and forage for a suitable raid target. If one is found, the scoutswill return to the nest, rally the other Polyergus, and head out in a raiding column. If it was a Formica nest, the Polyergus incite a "panic-flee" response from the Formica by releasing formic acid and take the Formica pupae back to their nest to be slaves. Occasionally, a new queen will embark on a raiding column with the other Polyergus. She will then, after mating, leave the column and forage for a suitable Formicanest. Howard Topoff did a considerable amount of work in evaluating how the queen then takes over the colony. After finding a Formica nest, she finds an entrance and is immediately attacked byFormica worker. The queen responds by biting with her sharp mandibles and releasing a pheromone from her enlargedDufour's gland that, unlike many other parasitic ants, has a pacifying effect. The queen quickly searches for and locates theFormica queen and, with her adapted mandibles, proceeds to bite and lick various parts the Formica queen for an average of 25 minutes. "Within seconds of the host queens death, the nest undergoes a most remarkable transformation". TheFormica workers cease to be aggressive to the intruder and start to groom the Polyergus queen as if it were their own.The takeover now complete, the Polyergus queen gains not only a nest, but a worker caste as well. She then lays her eggs and the cycle continues.
Nearly all slave making ants have mandibular adaptations that help them attack others; Polyergus is no different.
Specific to Polyergus, when the queen first enters a Formica nest she releases a pheromone from her enlarged Dufour’s gland. Topoff did experiments to show that this pheromone has an important facilitative effect in colony usurpation; it reduces the aggression of the defending Formica workers. The researchers took the Dufour’s, pygidial, and poison glands from freshly mated Polyergus queens, using water as a negative control. These were crushed in distilled water to make a solution containing their extracts. Because it was impossible to prevent a Polyergus queen from secreting their own pheromones during a live encounter, they used the harvester ant Pogonomyrmex occidentalis (naturally attacked byFormica) as the subject. These ants were dipped in the above solutions, one ant/solution/test at a time, and placed in a petri dish with three Formica occulta "attackers". They were observed for three minutes to see for how long the Pogonomyrmexwas attacked. The results were as follows: "the mean duration of aggression by the Dufour’s gland treatment was 53.3 seconds...The mean duration of aggression for the water, pygidial gland, and poison gland controls were: 143.5 seconds, and 137.2 seconds and 132.2 seconds respectively". Apparently, at some time, Polyergus queens evolved the capacity to passively facilitate colony takeovers.
Topoff and Ellen Zimmerli also did experiments to prove that the Polyergus queen "tricks" the Formica colony by obtaining chemicals from the Formica queen in the process of killing her. In one test, the Formica queen was killed (by flash freezing then thawing) prior to Polyergus contact. Even though it was already dead, the Polyergus queen bit, stabbed, and licked the queen just as if it were alive: and the Polyergus was consequently accepted by the colony. Another test showed that if noFormica queen was present, then Polyergus had little chance of a successful takeover. Clearly, the Formica queen is providing some sort of chemical(s) to the Polyergus queen, however unintentionally. That takeover can occur even if the host queen is dead, but not if she is not present, proves that chemical absorption is important. The Polyergus queen needs only kill one host queen to be accepted. If the colony was polygynistic, the Polyergus queen can take her time finding the other queens. "Hour by hour, day by day, she methodically locates and kills every Formica queen, sometimes taking several weeks to clear out all remnants of opposition".
Considerable work has been published on the evolution of ant dulosis and almost all of it has at least some empirical evidence to defend its positions. Notably, that nearly all raiding ant species have is an adaptation of their mandibles that make them big or piercing or both. It makes sense that the very thing that enables an ant to be a better raider causes that same ant to become dependent on others; the parasite loses the use of its mandibles for actual work. On this and other evidence, it has been proposed that predation is the precursor to slavery. It has also been suggested that colony multiplication by adoption and budding followed by temporary parasitism can lead to dulosis. While observations indicate that colony multiplication can lead to temporary parasitism, it is apparently very questionable that temporary parasitism leads to dulosis.
In addition, about 100 years ago, Carlo Emery observed that "the slave-making temporarily and permanently parasitic ants originate from closely related forms which serve them as host". Jurgen Heinze did a series of experiments that prove this observation, known today as Emery's Rule. Rather than just relying solely on morphological cues, he used enzyme gelelectrophoresis assays to create a detailed phylogenetic picture of host and parasite connections. His experimental results support a loose version of Emery’s rule. On one end of the spectrum, they saw near identical electromorphs between species in most host and parasite pairs studied. However, it also appears that at least one example does not support Emery’s rule in that (Leptothorax paraxenus) differed from its host in several electromorphs. The selective forces involved in the evolution of social parasitism are not fully understood, and it is unlikely that one model will fit all relationships.
"Any hypothesis explaining the evolution of slavery in Polyergus must account both for the origin of group raiding with brood capture, and for non-independent colony foundation by queens". Topoff gives an adequate hypothesis to the evolution ofPolyergus by integrating three processes: queen takeover, olfactory imprinting, and territorial fighting. Here are his main points. A free-living ancestor of Polyergus, that is a scavenger, would band together with others for intraspecific contest. Occasionally a queen would invade colonies of Formica. Initially the queen would drive off the Formica queen and workers and appropriated the Formica pupae (he gives as example the queens of Formica wheeleri that do this now). The killing of the Formica queen and adoption by the workers would evolve from this. His previous work (which was presented earlier) shows what would have evolved for adaptation to occur: "(1) sharp mandibles for killing the Formica queen, (2) a pheromone that reduces aggression from resident workers, (3) a tendency to hold onto the dead Formica queen long enough to absorb her odors...". The next step would be olfactory imprinting between the two species, a consequence of living one’s life from start to finish in the presence of both species. Polyergus’ ancestor then forages and encounters a colony of the same species. Again, they recruit nestmates to a territorial raid. In a brilliant insight, Topoff suggest this trait explains the raiding behavior. The Polyergus worker, raised by Formica as conspecifics, "identifies individual of Formica as belonging to its own species, another territorial raid is incited. Thus from the standpoint of Polyergus... slave raids are equivalent to territorial raids". The captured brood is imprinted as well and they become workers in the original nest. As time went on "Our ancestral Polyergus could easily slide in the direction of facultative parasitism". Eventually, Polyergus ancestors lost the ability to take care of themselves and become the inquiline Polyergus we see today.