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Do the Parasitic Psithyrus Resemble Their Host Bumblebees in Colour Pattern? Paul H

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Do the Parasitic Psithyrus Resemble Their Host Bumblebees in Colour Pattern? Paul H Do the parasitic Psithyrus resemble their host bumblebees in colour pattern? Paul H. Williams To cite this version: Paul H. Williams. Do the parasitic Psithyrus resemble their host bumblebees in colour pattern?. Apidologie, Springer Verlag, 2008, 39 (6), pp.637-649. hal-00891964 HAL Id: hal-00891964 https://hal.archives-ouvertes.fr/hal-00891964 Submitted on 1 Jan 2008 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 39 (2008) 637–649 Available online at: c INRA/DIB-AGIB/ EDP Sciences, 2008 www.apidologie.org DOI: 10.1051/apido:2008048 Original article Do the parasitic Psithyrus resemble their host bumblebees in colour pattern?* Paul H. Williams Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK Received 17 January 2008 – Revised 28 July 2008 – Accepted 9 August 2008 Abstract – It has been claimed for the parasitic Psithyrus bumblebees that each parasite species resembles closely its particular narrow range of bumblebee host species in colour pattern. The generality of colour- pattern resemblance is assessed by applying quantitative tests at three levels of resolution in the detail of the colour patterns. The results show that at all three levels the parasites and hosts are significantly more likely to share similar colour patterns than would be expected by chance in Europe, but not in North America. Parasites do not appear to be significantly more specialised in host choice in Europe than in North America, although there is more evidence of parasite-host co-speciation in Europe than in North America. Parasite- host resemblance appears most likely to be explained by Müllerian mimicry. For the host-specific Psithyrus, the host species might serve as the most influential model because necessarily the host species must co-occur with the parasite and must be common. bumblebee / Bombus / cuckoo bee / colour pattern / mimicry 1. INTRODUCTION species for which hosts are reliably recorded (Tab. I: 16/30 world species) often parasitize / The subgenus Psithyrus includes approxi- just one host species (for 8 16 studied species), mately 30 species of bumblebees that are all or at most, relatively few (2–5) host species. obligate social parasites (inquiline or ‘cuckoo’ The central issue for this paper is that Reinig bumblebees) in colonies of the social bumble- (1935) concluded that each parasitic Psithyrus bees, which constitute almost all of the rest species shows a ‘similar’ or ‘very marked’ of the genus Bombus (another 220 species: resemblance in colour pattern to its particu- Williams, 1998). Obligate parasitism is evi- lar host species within each geographical re- dent for Psithyrus because females of all of gion. And yet so far, the generality of parasite- the species lack a worker caste and lack the host colour-pattern resemblance has not been structures on the hind legs that are necessary demonstrated quantitatively. A re-assessment to enable foragers to collect pollen, so that is necessary because, despite his broad review, Psithyrus are completely dependent on divert- much of Reinig’s work on parasite-host colour ing their hosts’ resources for the nutrition of patterns (Reinig, 1930, 1935) focussed primar- their larvae and hence for their reproduction ily on one species, B. (Ps.) rupestris (Fabri- (for descriptions of Psithyrus behaviour see cius), which varies strongly in colour pattern e.g. Hoffer, 1889; Sladen, 1912; Plath, 1934; across Europe and Asia, showing especially Alford, 1975;Fisher,1987). Those Psithyrus close resemblance in geographical variation to its principal hosts, B. lapidarius (Linnaeus) Corresponding author: P.H. Williams, and B. sichelii Radoszkowski. Consequently, [email protected] it is possible that the close parasite-host re- * Manuscript editor: Jean-Noël Tasei semblance in this particular case is atypi- Online material is available at: cal and has biased people’s perceptions of http\protect://www.apidologie.org the other species. Taking the opposing view, Article published by EDP Sciences 638 P.H. Williams Table I. Records of parasitic species of the subgenus Psithyrus (left column) breeding in colonies of host (other Bombus) species (right column) with colour patterns coded as described in Table II. )p (g ) p Psithyrus Host species species Location Source + colour + colour group* group* EUROPE barbutellus hortorum Løken Europe 333D 333D 1984 barbutellus hypnorum Løken Europe 333D 324D 1984 bohemicus lucorum Løken Europe 332 333D 1984 campestris humilis Løken Europe 333D 324P 1984 campestris pascuorum Løken Europe 333D 124D 1984 campestris pomorum Løken Europe 333D 100 1984 campestris pratorum Løken Europe 333D 132 1984 flavidus jonellus Løken Europe 333D 333D 1984 maxillosus argillaceus Popov S Europe 332 333D 1931 Rasmont maxillosus ruderatus & (corsicola) Corsica 300 300 Adamski 1996 norvegicus hypnorum Løken Europe 332 324D 1984 Psithyrus-host colour resemblance 639 perezi terrestris Friese (xanthopus) Corsica 100 100 1923 quadricolor soroeensis Løken Europe 332 333D 1984 quadricolor soroeensis Løken (globosus) Europe 132 333D 1984 quadricolor soroeensis Løken (meridionalis) (proteus) Europe 100 100 1984 rupestris lapidarius Løken Europe 100 100 1984 rupestris lapidarius Løken Europe 132 100 1984 rupestris lapidarius Løken (decipiens) Europe 133 133 1984 rupestris pascuorum Løken Europe 100 124D 1984 rupestris sichelii Løken Europe 133 133 1984 rupestris sylvarum Løken Europe 100 133 1984 sylvestris jonellus Løken Europe 332 333D 1984 sylvestris pratorum Løken Europe 332 132 1984 vestalis terrestris Løken Europe 332 333D 1984 640 P.H. Williams NORTH AMERICA ashtoni affinis Plath Boston 332 033 1934 ashtoni terricola Plath Boston 332 033 1934 citrinus impatiens Plath (laboriosus) Boston 034 034 1934 citrinus vagans Plath Boston 334D 033 1934 insularis appositus Hobbs Alberta 333D 343P 1966 insularis fervidus Hobbs (californicus) Alberta 333D 332 1966 insularis flavifrons British Sladen 333D 113 Columbia 1915 insularis nevadensis Hobbs Alberta 333D 033 1965 insularis ternarius Craig Saskatchewan 333D 233 1953 suckleyi terricola Hobbs (occidentalis) Alberta 333D 332 1968 variabilis pensylvanicus Frison Illinois 033 033 1916 * Colour-pattern groups as defined by Williams (2007). Psithyrus-host colour resemblance 641 Richards (1927, p. 262) challenged the gener- lutionary conservatism within each mono- ality of bumblebee parasite-host resemblance phyletic host-parasite lineage (Plath, 1922). in colour pattern: ‘The resemblance between However, Psithyrus in its entirety has come Psithyrus species and their hosts is scarcely to be accepted as a monophyletic group greater than might be expected on the laws of (e.g. Pérez, 1884; Gaschott, 1922; Popov, chance in such polymorphic genera’. Despite 1931; Plowright and Stephen, 1973; Obrecht this, the assertion of close parasite-host colour- and Scholl, 1981;Ito,1985; Williams, 1985; pattern resemblance, whatever the cause, has Pamilo et al., 1987; Williams, 1991, 1995; often been repeated in subsequent texts on Kawakita et al., 2004; Cameron et al., 2007; bumblebees (e.g. Plath, 1934; Free and Butler, Michener, 2007). Consequently, evolution- 1959;Alford,1975; Plowright and Owen, ary conservatism within monophyletic lin- 1980; Prys-Jones and Corbet, 1987; Goulson, eages containing both hosts and parasites can- 2003; Benton, 2006) and deserves a quantita- not explain the colour-pattern resemblance. tive assessment. Nonetheless, there is likely to be some phy- Three possible causes of any resemblance logenetic component to colour-pattern resem- between Psithyrus and their hosts have been blances among the different parasite species, considered. First, some authors (Vogt, 1909; resulting from some degree of evolutionary Plowright and Owen, 1980) have suggested conservatism within co-speciating lineages of that Psithyrus species could have been selected hosts and parasites. For example, red tails (ru- to converge upon the colour patterns of their pestris-group) or black tails (citrinus-group) particular host species to facilitate parasitism, are characteristic of different species groups as a form of aggressive mimicry, implicitly within the subgenus Psithyrus,andthese to deceive the host. However, the idea that might specialize on different species groups of colour-pattern mimicry of hosts by parasites hosts. might aid parasite entry into host nests was re- Third, a more general explanation for re- jected by Vogt parasites: Command not found. semblance among Psithyrus and their hosts is (1909, p. 56), Plowright and Owen (1980), Müllerian mimicry (Müller, 1879), in which and by recent reviews (Free and Butler, 1959; species share a warning colour pattern to ad- Alford, 1975; Goulson, 2003; Benton, 2006). vertise the painful sting to common preda- Accounts of Psithyrus entering nests write tors (e.g. Sladen, 1912; Free and Butler, 1959; of aggressive interactions with host queens Plowright and Owen, 1980; Prys-Jones and or workers inside the nest, where it is usu- Corbet, 1987; Goulson, 2003; Benton, 2006). ally dark, rather than in
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