Evolutionary history of inquiline social parasitism in Plagiolepis ants

Degueldre, Félicien; Mardulyn, Patrick; Kuhn, Aléxandre; Pinel, Amélie; Karaman, Celal; Lebas, Claude; Schifani, Enrico; Bračko, Gregor; Wagner, Herbert C.; Kıran, Kadri; Borowiec, Lech; Passera, Luc; Abril, Sílvia; Espadaler, Xavier; Aron, Serge

doi:10.1016/j.ympev.2020.107016

Cited by 15 publications

(9 citation statements)

References 36 publications

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“…Strictly interpreted, Emery’s rule postulates a sister group relationship between host and parasite, whereas a less restrictive or “loose” interpretation signifies for example a congeneric, but not necessarily a sister taxon relationship ( 13 , 31 – 33 ). Consequently, two competing hypotheses were developed for explaining the speciation mechanisms of social parasites: 1) The interspecific hypothesis proposes that host and social parasite evolved reproductive isolation in allopatry, whereas 2) the intraspecific hypothesis postulates that the social parasite evolved directly from its host in sympatry ( 3 , 13 , 18 , 20 , 21 , 31 – 37 ). Empirical studies of temporary, dulotic, and host queen-intolerant workerless ant social parasites generally provide support for the interspecific hypothesis ( 14 , 38 – 48 ), whereas recent phylogenetic studies lend support to the intraspecific hypothesis for queen-tolerant inquilines ( 33 , 36 , 49 – 51 ).…”

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confidence: 99%

The evolution of social parasitism inFormicaants revealed by a global phylogeny

Borowiec

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2021

Proc. Natl. Acad. Sci. U.S.A.

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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 172 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 a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica, obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.

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confidence: 99%

The evolution of social parasitism inFormicaants revealed by a global phylogeny

Borowiec

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Rabeling

2021

Proc. Natl. Acad. Sci. U.S.A.

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“…Most of them are inquilines, which evolved multiple times, independently in the genus (Radchenko & Elmes, 2003;Jansen et al, 2010;Seifert, 2018). Unlike in other ant genera (e.g., Plagiolepis, see Degueldre et al, 2021), most parasite Myrmica spp. do not follow the strict version of Emery's rule (Emery, 1909), as their host species are not always their closest evolutionary relatives (Jansen et al, 2010).…”

Section: Short Notementioning

confidence: 83%

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Social parasitism has evolved several times and in different forms among ants, showing amazing morphofunctional, chemical and behavioral adaptations to this peculiar habit (Visicchio et al, 2001;Buschinger, 2009). Inquilinism is considered the most extreme of such forms: inquiline social parasites produce few to no workers while they concentrate their efforts on the production of reproducers which their hosts raise (Hölldobler & Wilson, 1990;Buschinger, 2009;Degueldre et al, 2021). As a result, inquiline ant species are rarely detected during field surveys.

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confidence: 99%

Social Parasite Ants in the Alps: a New Site of the Vulnerable Myrmica myrmicoxena and New Uppermost Altitudinal Limit for M. microrubra

et al. 2021

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We conducted a survey on the Alpine fauna of one of the largest Natural Park of the Italian Alps (Stelvio National Park) in the framework of a broad ecological monitoring of Alpine biodiversity. A two-years standardized sampling employing pitfall traps along a 1200 m altitudinal gradient led to the discovery of two interesting inquiline social parasite ants of the genus Myrmica: M. myrmicoxena Forel, 1895 and M. microrubra Seifert, 1993. Myrmica myrmicoxena, which is classified as Vulnerable according to the IUCN Red List, was so far known from only three sites across a narrow geographic range between Italy and Switzerland. Our data support the previous hypothesis over its ecology and host association. Myrmica microrubra is considered an incipient species of high evolutionary interest, sometimes regarded as an intraspecific form of M. rubra. While having a wide distribution in Europe, its presence in Italy was hitherto known only from a single site, and our record extends its altitudinal distribution limit in Europe upwards by about 600 m.

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“…Therefore, phylogenetic relatedness with the host was suggested to play a major role in facilitating social inquilinism, since the inquiline would share some common genetic factors promoting camouflage, known as Emery's rule (Cini et al 2019). Although recent phylogenetic studies have revised and sometimes rejected Emery's rule at the specific level (Huang and Dornhaus 2008;Lopez-Osorio et al 2015;Romiguier et al 2018; but see Savolainen and Vepsäläinen 2003;Degueldre et al 2021), most cases of social inquilines remain related to the same genus (Jansen et al 2010;Cardinal et al 2010), tribe (Schrader et al 2021), family (Ronquist 1994;Cardinal et al 2010), or even order (Gilbert et al 2012). The genetic basis underlying inquilines belonging to distinct orders or across wide phylogenetic distances is still less understood.…”

Section: Introductionmentioning

confidence: 99%

“…2015; Romiguier et al . 2018; but see Savolainen and Vepsäläinen 2003; Degueldre et al . 2021), most cases of social inquilines remain related to the same genus (Jansen et al .…”

Section: Introductionmentioning

confidence: 99%

The genome of the blind bee louse fly reveals deep convergences with its social host and illuminates Drosophila origins

Legout

Ogereau

Filée

et al. 2022

Preprint

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The nests of social insects often harbor a rich fauna of intruders, known as inquilines. Close relatedness between the host and the inquiline prevails due to potential genetic predispositions but how phylogenetically distant inquilines adapt to their hosts remains unclear. Here, we analyzed the genome of the wingless and blind bee louse fly Braula coeca, an inquiline of the Western honey bee Apis mellifera. We found that unlike many parasites, such as the human louse, the bee louse genome did not show significant erosion or strict reliance on an endosymbiont, likely due to a relatively recent age of inquilinism. However, a strikingly parallel evolution in a set of gene families was observed between the honey bee and the bee louse. Convergences included genes potentially involved in metabolism and immunity, and the loss of nearly all bitter-tasting gustatory receptors in agreement with life in a protective hive and a major diet of honey, pollens, and beeswax. Vision-related and odorant receptor genes also exhibited rapid losses. Only genes whose orthologs in the closely related Drosophila melanogaster respond to components of the honey bee alarm pheromones or floral aroma were retained, whereas the losses included orthologous receptors responsive to the anti-ovarian honey bee queen pheromone. These results establish a new model for the study of major morphological and neuroethological transitions and indicate that deep genetic convergences between phylogenetically distant organisms can underlie the evolution of social inquilinism.

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Evolutionary history of inquiline social parasitism in Plagiolepis ants

Cited by 15 publications

References 36 publications

The evolution of social parasitism inFormicaants revealed by a global phylogeny

The evolution of social parasitism inFormicaants revealed by a global phylogeny

Social Parasite Ants in the Alps: a New Site of the Vulnerable Myrmica myrmicoxena and New Uppermost Altitudinal Limit for M. microrubra

The genome of the blind bee louse fly reveals deep convergences with its social host and illuminates Drosophila origins

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