scholarly journals Insect societies fight back: the evolution of defensive traits against social parasites

2018 ◽  
Vol 373 (1751) ◽  
pp. 20170200 ◽  
Author(s):  
Christoph Grüter ◽  
Evelien Jongepier ◽  
Susanne Foitzik

Insect societies face many social parasites that exploit their altruistic behaviours or their resources. Due to the fitness costs these social parasites incur, hosts have evolved various behavioural, chemical, architectural and morphological defence traits. Similar to bacteria infecting multicellular hosts, social parasites have to successfully go through several steps to exploit their hosts. Here, we review how social insects try to interrupt this sequence of events. They can avoid parasite contact by choosing to nest in parasite-free locales or evade attacks by adapting their colony structure. Once social parasites attack, hosts attempt to detect them, which can be facilitated by adjustments in colony odour. If social parasites enter the nest, hosts can either aggressively defend their colony or take their young and flee. Nest structures are often shaped to prevent social parasite invasion or to safeguard host resources. Finally, if social parasites successfully establish themselves in host nests, hosts can rebel by killing the parasite brood or by reproducing in the parasites' presence. Hosts of social parasites can therefore develop multiple traits, leading to the evolution of complex defence portfolios of co-dependent traits. Social parasites can respond to these multi-level defences with counter-adaptations, potentially leading to geographical mosaics of coevolution. This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours’.

2019 ◽  
Vol 374 (1769) ◽  
pp. 20180193 ◽  
Author(s):  
Alessandro Cini ◽  
Seirian Sumner ◽  
Rita Cervo

Insect societies play a crucial role in the functioning of most ecosystems and have fascinated both scientists and the lay public for centuries. Despite the long history of study, we are still far from understanding how insect societies have evolved and how social cohesion in their colonies is maintained. Here we suggest inquiline social parasites of insect societies as an under-exploited experimental tool for understanding sociality. We draw on examples from obligate inquiline (permanent) social parasites in wasps, ants and bees to illustrate how these parasites may allow us to better understand societies and learn more about the evolution and functioning of insect societies. We highlight three main features of these social parasite–host systems—namely, close phylogenetic relationships, strong selective pressures arising from coevolution and multiple independent origins—that make inquiline social parasites particularly suited for this aim; we propose a conceptual comparative framework that considers trait losses, gains and modifications in social parasite–host systems. We give examples of how this framework can reveal the more elusive secrets of sociality by focusing on two cornerstones of sociality: communication and reproductive division of labour. Together with social parasites in other taxonomic groups, such as cuckoos in birds, social parasitism has a great potential to reveal the mechanisms and evolution of complex social groups. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


PLoS ONE ◽  
2017 ◽  
Vol 12 (12) ◽  
pp. e0190018 ◽  
Author(s):  
Marta Elia ◽  
Giuliano Blancato ◽  
Laura Picchi ◽  
Christophe Lucas ◽  
Anne-Geneviève Bagnères ◽  
...  

2020 ◽  
Author(s):  
Marek L Borowiec ◽  
Stefan P Cover ◽  
Christian Rabeling

Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 178 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life-history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed the first global phylogeny of Formica ants and representative formicine outgroups. The genus Formica originated in the Old World during the Oligocene (~30 Ma ago) and dispersed multiple times to the New World. Within Formica, the capacity for dependent colony foundation and temporary social parasitism arose once from a facultatively polygynous, independently colony founding ancestor. Within this parasitic clade, dulotic social parasitism evolved once from a facultatively temporary parasitic ancestor that likely practiced colony budding frequently. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from different facultative parasitic backgrounds in socially polymorphic organisms. In contrast to inquiline ant species in other genera, the high social parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.


2019 ◽  
Vol 374 (1769) ◽  
pp. 20180203 ◽  
Author(s):  
Jukka Suhonen ◽  
Jaakko J. Ilvonen ◽  
Tommi Nyman ◽  
Jouni Sorvari

Interspecific brood parasitism is common in many animal systems. Brood parasites enter the nests of other species and divert host resources for producing their own offspring, which can lead to strong antagonistic parasite–host coevolution. Here, we look at commonalities among social insect species that are victims of brood parasites, and use phylogenetic data and information on geographical range size to predict which species are most probably to fall victims to brood parasites in the future. In our analyses, we focus on three eusocial hymenopteran groups and their brood parasites: (i) bumblebees, (ii) Myrmica ants, and (iii) vespine and polistine wasps. In these groups, some, but not all, species are parasitized by obligate workerless inquilines that only produce reproductive-caste descendants. We find phylogenetic signals for geographical range size and the presence of parasites in bumblebees, but not in ants and wasps. Phylogenetic logistic regressions indicate that the probability of being attacked by one or more brood parasite species increases with the size of the geographical range in bumblebees, but the effect is statistically only marginally significant in ants. However, non-phylogenetic logistic regressions suggest that bumblebee species with the largest geographical range sizes may have a lower likelihood of harbouring social parasites than do hosts with medium-sized ranges. Our results provide new insights into the ecology and evolution of host–social parasite systems, and indicate that host phylogeny and geographical range size can be used to predict threats posed by social parasites, as well to design efficient conservation measures for both hosts and their parasites. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.


2004 ◽  
Vol 82 (12) ◽  
pp. 1843-1853 ◽  
Author(s):  
Anna L Birmingham ◽  
Shelley E Hoover ◽  
Mark L Winston ◽  
Ron C Ydenberg

Commercial greenhouses require high densities of managed bumble bee (Bombus occidentalis Greene, 1858 and Bombus impatiens Cresson, 1863) colonies to pollinate crops such as tomatoes (Lycopersicon esculentum Miller). We examined drifting, a behavioural consequence of introducing closely aggregated colonies into greenhouse habitats, to determine possible explanations for observed drifting frequencies. Bee drift is normally associated with increased individual mortality and disease transfer between colonies. In this study, individual bees frequently drifted into and remained within foreign colonies. More drifting bees were found in colonies with higher worker and brood populations and greater pollen stores. Increased intracolony aggressive interactions were not associated with a higher number of drifting bees. Drifting bees had a significantly greater number of mature eggs in their ovaries than did resident worker bees residing in colonies hosting drifters, suggesting that drifting could potentially increase the fitness of individual worker bees and may not be solely a function of disorientation and (or) nectar robbing. Taken together, our results suggest that drifting of workers into foreign colonies within greenhouses may demonstrate a predisposition to social parasitism. This selfish worker reproduction challenges our previous understanding of social insect societies as being cooperative societies.


2008 ◽  
Vol 33 (3) ◽  
pp. 321-327 ◽  
Author(s):  
CLAIRE CARVELL ◽  
PETER ROTHERY ◽  
RICHARD F. PYWELL ◽  
MATTHEW S. HEARD

1992 ◽  
Vol 124 (1) ◽  
pp. 69-77 ◽  
Author(s):  
Richard M. Fisher ◽  
Blair J. Sampson

AbstractPsithyrus spp. (Hymenoptera: Apidae) are obligate social parasites of bumble bees (Bombus spp.). Morphological and physiological features of P. ashtoni (Cresson) females, which may facilitate the successful usurpation of host nests, were examined. Parasite females were no larger than B. terricola Kirby queens, although they possessed a number of protective modifications to the exoskeleton, as well as increased offensive armament, including larger mandibles and a longer venom gland. Females of P. ashtoni and P. insularis (Smith) possessed a greater number of ovarioles than host queens, and produced smaller eggs. The Dufour’s glands of the two Psithyrus species were significantly larger than those of B. terricola. There appears to have been considerable convergence in the evolution of socially parasitic lifestyles in bumble bees and wasps (Vespula spp.), presumably as a consequence of similar selective pressures operating on parasites belonging to these distantly related but socially similar taxa.


2019 ◽  
Vol 286 (1898) ◽  
pp. 20182867 ◽  
Author(s):  
Unni Pulliainen ◽  
Heikki Helanterä ◽  
Liselotte Sundström ◽  
Eva Schultner

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.


ZooKeys ◽  
2020 ◽  
Vol 921 ◽  
pp. 23-48
Author(s):  
Steven J. Messer ◽  
Stefan P. Cover ◽  
Christian Rabeling

In ants, social parasitism is an umbrella term describing a variety of life-history strategies, where a parasitic species depends entirely on a free-living species, for part of or its entire life-cycle, for either colony founding, survival, and/or reproduction. The highly specialized inquiline social parasites are fully dependent on their hosts for their entire lifecycles. Most inquiline species are tolerant of the host queen in the parasitized colony, forgo producing a worker caste, and invest solely in the production of sexual offspring. In general, inquilines are rare, and their geographic distribution is limited, making it difficult to study them. Inquiline populations appear to be small, cryptic, and they are perhaps ephemeral. Thus, information about their natural history is often fragmentary or non-existent but is necessary for understanding the socially parasitic life history syndrome in more detail. Here, we describe two new species of inquiline social parasites, Nylanderia deyrupisp. nov. and Nylanderia parasiticasp. nov., from the southeastern United States, parasitizing Nylanderia wojciki and Nylanderia faisonensis, respectively. The formicine genus Nylanderia is large and globally distributed, but until the recent description of Nylanderia deceptrix, social parasites were unknown from this genus. In addition to describing the new social parasite species, we summarize the fragmentary information known about their biology, present a key to both the queens and the males of the Nylanderia social parasites, and discuss the morphology of the social parasites in the context of the inquiline syndrome.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Lukas Schrader ◽  
Hailin Pan ◽  
Martin Bollazzi ◽  
Morten Schiøtt ◽  
Fredrick J. Larabee ◽  
...  

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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