Dulosis

Dulosis (from the Ancient Greek doûlos, meaning "slave" or "bondsman"; also termed brood raiding or pirate ant parasitism) is a specialized form of intraspecific or interspecific social parasitism in ants (family Formicidae, order Hymenoptera) studied within myrmecology and entomology in which workers of a parasitic colony conduct organized raids on neighboring ant nests, seize their immature brood (larvae and pupae), and transport them back to the parasite's nest (Hölldobler & Wilson, 1990; Buschinger, 2009). Although a proportion of the captured brood may be consumed as trophic prey, the surviving pupae eclose inside the parasite's nest, imprint olfactorily on the mixed colony odor within the first hours of adult life, and thereafter perform all routine colony labor—foraging for nectar and insect prey, excavating nest galleries, regurgitating liquid food via stomodeal trophallaxis, and grooming the parasitic queen and her offspring—as an integrated subordinate workforce (Alloway, 1979; D'Ettorre & Heinze, 2001). Having evolved independently at least ten times across the subfamilies Formicinae (most notably in the Nearctic and Palearctic amazon ants of the genus Polyergus, the sanguinary ants Formica subgenus Raptiformica, and Rossomyrmex) and Myrmicinae (including Harpagoxenus, Protomognathus, Temnothorax duloticus, and Strongylognathus), dulotic lineages consistently obey Emery's rule, parasitizing host species to which they are closely related phylogenetically (Emery, 1909; Buschinger, 2009).

Intraspecific Brood Raiding, Facultative Dulosis, and Obligate Amazon Ants

Comparative behavioral and phylogenomic reconstructions demonstrate that obligate interspecific dulosis evolved via gradual escalation from two ancestral ant behaviors: territorial competition among neighboring colonies and temporary social parasitism during dependent colony foundation (Wilson, 1971; Topoff, 1990; Pollock & Rissing, 1989):

1. Intraspecific Brood Raiding in Founding Colonies: In desert seed-harvester ants (Veromessor pergandei), red imported fire ants (Solenopsis invicta), and honeypot ants (Myrmecocystus mimicus), pleometrotic founding nests clustered in dense aggregations raid adjacent conspecific incipient colonies and steal their worker pupae to accelerate workforce growth and win territorial tournaments.
2. Facultative Interspecific Dulosis (Formica subgenus Raptiformica): In the Holarctic sanguinary ant Formica sanguinea and its North American relatives (Formica subintegra, Formica pergandei), the workers retain generalized mandibles capable of nest excavation, foraging, and brood nursing. Colonies of F. sanguinea can survive autonomously in the laboratory without hosts, yet in nature they conduct seasonal summer raids against colonies of the Formica fusca species group (Serviformica), incorporating captured host pupae so that 20% to 80% of the mixed nest consists of Serviformica workers.
3. Obligate Dulosis and Morphological Specialization (Polyergus, Harpagoxenus, Strongylognathus): In obligate dulotic genera such as the amazon ants (Polyergus rufescens, Polyergus breviceps, Polyergus lucidus) and the myrmicine Strongylognathus, the evolution of sickle-shaped, toothless falcate mandibles specialized for piercing the armored head capsules and thoraces of defending host workers has rendered the parasitic workers incapable of chewing solid food, excavating soil, or opening cocoons. Deprived of their Formica or Tetramorium host workers, an isolated cohort of Polyergus workers starves to death even when surrounded by abundant honey and dead prey (Topoff, 1990; Hölldobler & Wilson, 1990).

Comparative Biology of Major Dulotic Ant Lineages

Scout Navigation, Recruitment Trails, and Polarized-Light Homing

In Polyergus rufescens and Polyergus breviceps, raiding is restricted to warm afternoons during mid- to late summer when host Formica colonies contain abundant late-instar worker pupae (Topoff, 1990). Earlier in the afternoon, a small caste of older scout workers leaves the mixed nest and searches up to 50–100 meters away. Upon discovering a target Formica nest entrance, the scout inspects its perimeter without provoking combat and returns home in a straight trajectory guided by polarized-light e-vector detectors in the dorsal rim ommatidia feeding into the central complex path integrator, while depositing a recruitment trail pheromone from its rectal bladder and Dufour's gland.

Within minutes of the scout's return, 500 to 4,000 Polyergus raiders surge out of the nest in a dense phalanx (10–20 cm wide and several meters long), arriving at the target Formica mound and penetrating its subterranean brood chambers within seconds.

Propaganda Allomones and Queen Regicide Followed by Odor Absorption

Rather than engaging in prolonged attrition warfare against thousands of defending Formica or Temnothorax workers, dulotic raiders deploy specialized exocrine allomones that disrupt the host colony's alarm communication system (Regnier & Wilson, 1971; Lenoir et al., 2001):

1. Dufour's Gland Acetate Propaganda Substances: In Formica subintegra and Formica pergandei, the abdominal Dufour's gland is hypertrophied to nearly 20% of the gaster's volume and filled with up to 700 micrograms of volatile decyl acetate, dodecyl acetate, and tetradecyl acetate. Sprayed onto defending Formica subsericea workers during a raid, these esters act as high-amplitude propaganda allomones: they bind odorant sensilla projecting to the antennal lobe of the defenders, inducing immediate panic flight and dispersal of the hosts while simultaneously serving as an attractant beacon for conspecific raiders (Regnier & Wilson, 1971).
2. Assassin-like Queen Usurpation and Cuticular Hydrocarbon Transfer: During solitary colony foundation, a newly mated Polyergus breviceps or Polyergus rufescens queen penetrates a host Formica nest alone, calmed initially by appeasement esters (such as decyl butyrate) secreted from her enlarged Dufour's gland. Once she locates the resident Formica queen, the Polyergus queen pierces the host queen's head and thorax with her falcate mandibles and then spends 15 to 30 minutes grooming and licking the dying queen's insect cuticle. Gas chromatography–mass spectrometry confirms that this behavior transfers the host queen's cuticular hydrocarbon (CHC) signature (synthesized by subepidermal oenocytes) directly onto the usurper's epicuticle, causing the orphaned Formica workers to adopt their mother's assassin within minutes (Topoff, 1990; Johnson et al., 2001).

How are captured host workers tricked into serving a foreign species in the absence of physical coercion? Classic cross-fostering experiments by Pierre Jaisson and Patrizia D'Ettorre demonstrated that newly eclosed callow ants lack an innate genetic template of their own species' colony odor; instead, during a sensitive post-eclosion window (the first 24 to 72 hours after emerging from the pupal cuticle), each callow worker learns the blended cuticular hydrocarbon Gestalt of its nestmates and the brood it tends as the reference template for nestmate recognition (Jaisson, 1975; D'Ettorre & Heinze, 2001).

Nevertheless, the evolutionary conflict between dulotic parasites and their hosts is not one-sided. In the North American micro-ant system of Protomognathus americanus parasitizing Temnothorax longispinosus and Temnothorax curvispinosus inside hollow acorns, Pamminger, Foitzik, and Achenbach discovered that enslaved Temnothorax nursing workers execute adaptive "slave rebellion": although the host nurses faithfully feed the parasitic Protomognathus larvae through pupation, once the pupae differentiate and reveal their species-specific cuticular hydrocarbon profiles, the enslaved Temnothorax nurses selectively tear open and kill 60% to 80% of the female (worker and queen) Protomognathus pupae, substantially reducing the future raiding pressure on neighboring free-living Temnothorax relatives via indirect kin selection (Achenbach & Foitzik, 2009).

1. Regnier, F. E., & Wilson, E. O. (1971). Chemical communication and "propaganda" in slave-maker ants. Science, 172(3980), 267–269. https://doi.org/10.1126/science.172.3980.267
2. Topoff, H. (1990). Slave-making ants. American Scientist, 78(6), 520–528. https://doi.org/10.1126/science.240.4855.1072
3. D'Ettorre, P., & Heinze, J. (2001). Sociobiology of slave-making ants. Acta Ethologica, 3(2), 67–82. https://doi.org/10.1007/s102110100038
4. Achenbach, A., & Foitzik, S. (2009). First evidence for slave rebellion: Enslaved ant workers systematically kill the brood of their social parasite Protomognathus americanus. Evolution, 63(4), 1068–1075. https://doi.org/10.1111/j.1558-5646.2009.00591.x