Dynamics of chemical mimicry in the social parasite wasp Polistes semenowi (Hymenoptera: Vespidae)

Chemical cues are so important in the recognition mechanism of social insects that most social parasites (which rely on hosts to rear their brood) have been documented as overcoming the mechanism by which colony residents recognize non-nestmates, by mimicking the odour of the usurped colony. We simulated in the laboratory the process by which the obligate social parasite, Polistes semenowi, invades nests of the host species, Polistes dominulus, in the field and analysed the epicuticular lipid layer before and after host nest usurpation. The experiment documents that P. semenowi social parasites have an epicuticular hydrocarbon pattern which is very similar to that of their host but, after entering host colonies, parasites mimic the odour of the colonies they invade, to the point that they perfectly match the hydrocarbon profile peculiar to the colony they entered. However, both before and after host nest invasion, parasites show a tendency to possess diluted recognition cues with respect to their hosts.

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Invasion of the Nest of Polistes dominulus by the Social Parasite Sulcopolistes sulcifer (Hymenoptera, Vespidae)1

Ethology ◽

10.1111/j.1439-0310.1990.tb00784.x ◽

2010 ◽

Vol 84 (1) ◽

pp. 47-59 ◽

Cited By ~ 33

Author(s):

S. Turillazzi ◽

R. Cervo ◽

I. Cavallari

Keyword(s):

Social Parasite ◽

Polistes Dominulus ◽

The Social

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The possible role of ant larvae in the defence against social parasites

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.2867 ◽

2019 ◽

Vol 286 (1898) ◽

pp. 20182867 ◽

Cited By ~ 2

Author(s):

Unni Pulliainen ◽

Heikki Helanterä ◽

Liselotte Sundström ◽

Eva Schultner

Keyword(s):

Host Species ◽

Social Parasitism ◽

Social Parasite ◽

Social Parasites ◽

Nest Mate ◽

Formica Fusca ◽

Before And After ◽

Key Factor ◽

Host Worker ◽

Cuticular Profiles

Temporary social parasite ant queens initiate new colonies by entering colonies of host species, where they begin laying eggs. As the resident queen can be killed during this process, host colonies may lose their entire future reproductive output. Selection thus favours the evolution of defence mechanisms, before and after parasite intrusion. Most studies on social parasites focus on host worker discrimination of parasite queens and their offspring. However, ant larvae can also influence brood composition by consuming eggs. This raises the question whether host larvae can aid in preventing colony takeover by consuming eggs laid by parasite queens. To test whether larvae could play a role in anti-parasite defence, we compared the rates at which larvae of a common host species, Formica fusca , consumed eggs laid by social parasite, non-parasite, nest-mate, or conspecific non-nest-mate queens. Larvae consumed social parasite eggs more than eggs laid by a heterospecific non-parasite queen, irrespective of the chemical distance between the egg cuticular profiles. Also, larvae consumed eggs laid by conspecific non-nest-mate queens more than those laid by nest-mate queens. Our study suggests that larvae may act as players in colony defence against social parasitism, and that social parasitism is a key factor shaping discrimination behaviour in ants.

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Relaxed selection underlies genome erosion in socially parasitic ant species

Nature Communications ◽

10.1038/s41467-021-23178-w ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Lukas Schrader ◽

Hailin Pan ◽

Martin Bollazzi ◽

Morten Schiøtt ◽

Fredrick J. Larabee ◽

...

Keyword(s):

Olfactory Receptors ◽

Social Parasite ◽

Effective Population ◽

Social Parasites ◽

Free Living ◽

Closely Related Species ◽

Genomic Changes ◽

The Social ◽

Population Sizes ◽

Leaf Cutting

AbstractInquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species. They have evolved many times convergently, are often evolutionarily young lineages, and are almost invariably rare. Focusing on the leaf-cutting ant genus Acromyrmex, we compared genomes of three inquiline social parasites with their free-living, closely-related hosts. The social parasite genomes show distinct signatures of erosion compared to the host lineages, as a consequence of relaxed selective constraints on traits associated with cooperative ant colony life and of inquilines having very small effective population sizes. We find parallel gene losses, particularly in olfactory receptors, consistent with inquiline species having highly reduced social behavioral repertoires. Many of the genomic changes that we uncover resemble those observed in the genomes of obligate non-social parasites and intracellular endosymbionts that branched off into highly specialized, host-dependent niches.

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Evolution and host specificity: a study of the invasion success of a specialized bumblebee social parasite

Canadian Journal of Zoology ◽

10.1139/z84-238 ◽

1984 ◽

Vol 62 (8) ◽

pp. 1641-1644 ◽

Cited By ~ 16

Author(s):

Richard M. Fisher

Keyword(s):

Host Specificity ◽

Invasion Success ◽

Host Specialization ◽

Social Parasite ◽

Host Defenses ◽

Social Parasites ◽

Laboratory Colonies ◽

Nest Usurpation ◽

Bombus Affinis ◽

Host Parasite

Species of Psithyrus (Hymenoptera: Apidae) are obligate social parasites of bumblebees. They range from monospecificity to species which have many Bombus hosts. Much of the reported variation in host–parasite behaviour which occurs during attempted nest usurpations may be explained in the context of host specificity. Psithyrus ashtoni is a relatively specialized bumblebee social parasite. The ability of P. ashtoni females to successfully enter laboratory colonies of Bombus affinis and Bombus terricola was tested. Female Psithyrus were introduced into more than 100 host colonies containing 0–58 workers. Parasites and host queens never fought, but in both hosts, invasion success decreased with increasing worker numbers. The passive nest usurpation behaviour of P. ashtoni differs from that of other, nonspecialized species of Psithyrus, which may kill or displace the host queen, and from that of completely specialized parasites, which may cohabit with both host queens and host workers. Host specialization may allow Psithyrus females to evolve behavioural and physiological features which minimize host defenses. Thus, while the number of available host species is limited, there is an increased probability of successful usurpation in nests of the appropriate host.

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Olfactory cues in host nest detection by the social parasite Polistes sulcifer (Hymenoptera, Vespidae)

Behavioural Processes ◽

10.1016/0376-6357(95)00030-5 ◽

1996 ◽

Vol 36 (3) ◽

pp. 213-218 ◽

Cited By ~ 7

Author(s):

R. Cervo ◽

F. Bertocci ◽

S. Turillazzi

Keyword(s):

Olfactory Cues ◽

Social Parasite ◽

Host Nest ◽

The Social

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Why are larvae of the social parasite wasp Polistes sulcifer not removed from the host nest?

Behavioral Ecology and Sociobiology ◽

10.1007/s00265-008-0560-1 ◽

2008 ◽

Vol 62 (8) ◽

pp. 1319-1331 ◽

Cited By ~ 16

Author(s):

R. Cervo ◽

F. R. Dani ◽

C. Cotoneschi ◽

C. Scala ◽

I. Lotti ◽

...

Keyword(s):

Social Parasite ◽

Host Nest ◽

The Social

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Discrimination of the Social ParasiteEctatomma parasiticumby Its Host Sibling Species (E. tuberculatum)

Psyche A Journal of Entomology ◽

10.1155/2013/573541 ◽

2013 ◽

Vol 2013 ◽

pp. 1-11 ◽

Cited By ~ 3

Author(s):

Renée Fénéron ◽

Chantal Poteaux ◽

Marie Boilève ◽

Jorge Valenzuela ◽

Fabrice Savarit

Keyword(s):

Sibling Species ◽

Evolutionary History ◽

Sympatric Speciation ◽

Social Parasite ◽

Local Distribution ◽

Chemical Profile ◽

Social Parasites ◽

New Findings ◽

The Social ◽

Survival And Reproduction

Among social parasites, workerless inquilines entirely depend on their host for survival and reproduction. They are usually close phylogenetic relatives of their host, which raises important questions about their evolutionary history and mechanisms of speciation at play. Here we present new findings onEctatomma parasiticum, the only inquiline ant described in the Ectatomminae subfamily. Field data confirmed its rarity and local distribution in a facultative polygynous population ofE. tuberculatumin Mexico. Genetic analyses demonstrated that the parasite is a sibling species of its host, from which it may have diverged recently. Polygyny is suggested to have favored the evolution of social parasite by sympatric speciation. Nevertheless, host workers from this population were able to discriminate parasites from their conspecifics. They treated the parasitic queens either as individuals of interest or as intruders, depending on their colonial origin, probably because of the peculiar chemical profile of the parasites and/or their reproductive status. We suggest thatE. parasiticumcould have conserved from its host sibling species the queen-specific substances that produce attracting and settling effect on workers, which, in return, would increase the probability to be detected. This hypothesis could explain the imperfect social integration of the parasite into host colonies.

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Behavioural and neurogenomic responses of host workers to social parasite invasion in a social insect

Insectes Sociaux ◽

10.1007/s00040-020-00765-6 ◽

2020 ◽

Vol 67 (2) ◽

pp. 295-308

Author(s):

A. Cini ◽

R. Branconi ◽

S. Patalano ◽

R. Cervo ◽

S. Sumner

Keyword(s):

Social Insect ◽

Interaction Network ◽

Egg Laying ◽

Centrality Measures ◽

Social Parasite ◽

Social Parasites ◽

Brain Gene Expression ◽

The Social ◽

Behavioural Phenotypes ◽

Defence Strategies

Abstract The strong coevolutionary arms race between social parasites and their hosts has dramatically shaped the life-history traits of both parties. One of the main strategies exhibited by hosts in response to parasitism is reproduction by host workers. We lack a mechanistic understanding of how these defence strategies unfold and, specifically, whether hosts exhibit more subtle strategies to reduce the costs of parasitism from the outset. Here we test the hypothesis that there are both behavioural and neurogenomic signatures of worker responses to parasitism, prior to overt expression in the form of egg-laying; we test this using the social parasite—social host system of the paper wasps Polistes sulcifer-Polistes dominula. We characterized individual workers’ position within the social interaction network of queenright and host colonies immediately after parasite usurpation, weeks before the workers’ reproductive rebellion is evident. Parasitism influenced network centrality measures, with workers in parasitized colonies showing increased connectedness and centrality compared to those in unparasitized ones. Next, we quantified brain gene expression levels for five genes related to physiological and behavioural phenotypes in Polistes wasps. The gene Imaginal disc growth factor (Idgf4), thought to be responsive to changes in the social environment, was significantly down-regulated in workers from parasitized colonies; this may be an indication that parasitized workers are anticipating a shift toward a less worker-like phenotype in preparation for their reproductive rebellion. Our results provide the first evidence of early behavioural and neurogenomic responses of host workers toward the presence of an inquiline social parasite in a social insect.

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