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Beyond the Paradigms of Cospeciation and Hostswitch: Is Sympatric Speciation an Important Mode of Speciation for Parasites? S

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Beyond the Paradigms of Cospeciation and Hostswitch: Is Sympatric Speciation an Important Mode of Speciation for Parasites? S BEYOND THE PARADIGMS OF COSPECIATION AND HOSTSWITCH: IS SYMPATRIC SPECIATION AN IMPORTANT MODE OF SPECIATION FOR PARASITES? S. Morand, A. Šimková, S. Gourbière To cite this version: S. Morand, A. Šimková, S. Gourbière. BEYOND THE PARADIGMS OF COSPECIATION AND HOSTSWITCH: IS SYMPATRIC SPECIATION AN IMPORTANT MODE OF SPECIATION FOR PARASITES?. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 2008, pp.125-132. hal-03246070 HAL Id: hal-03246070 https://hal.sorbonne-universite.fr/hal-03246070 Submitted on 2 Jun 2021 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. VIE ET MILIEU - LIFE AND ENVIRONMENT, 2008, 58 (2): 125-132 BEYOND THE PARADIGMS OF COSPECIATION AND HOST- SWITCH: IS SYMPATRIC SPECIATION AN IMPORTANT MODE OF SPECIATION FOR PARASITES? S. MORAND 1*, A. ŠIMKOVÁ 2, S. GOURBIÈRE 3 1 Université Montpellier 2-CNRS, Institut des Sciences de l’Evolution, CC065, 34095 Montpellier cedex 05, France. 2 Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic 3 Laboratoire de Mathématique Physique et Systèmes (EA 4217), Université de Perpignan, Via Domitia, 52 avenue Paul Alduy, 66860 Perpignan cedex, France * Corresponding author: [email protected] SYMPATRIC SPECIATION ABSTRACT. – The great majority of studies on host-parasite associations, either theoretical or INTRA-HOST SPECIATION COSPECIATION empirical, have focused on cospeciation and host-switch minimizing the importance of sympat- SPECIES FLOCKS ric speciation, a mode of speciation that can be also defined as intra-host speciation. Sympatric CONGENERIC SPECIES speciation is considered when a single host species is infested by a monophyletic parasite line- age. The parasite speciates without a corresponding host cospeciation event and this leads to two or more lineages of parasites on single host species. A recent study illustrates how the diversification of Dactylogyrus spp. parasitizing cyprinid fish meets the four conditions required to recognize a case of sympatric speciation, according to Coyne (2007). However, inferring mode of speciation does not help to depict the mechanism of sympatric/intra-host speciation and theoretical model of speciation can be useful to investigate the conditions of sympatric specia- tion in parasites, as it has been already done for free-living organisms. Finally we aim at high- lighting that diversification of parasites through intra-host speciation is maybe a prevalent mode of speciation in parasites, as the numerous number of parasite species flocks suggest, and that parasites are also good models for investigating the mechanisms of sympatric speciation. INTRODUCTION The great majority of studies on host-parasite associa- tions, either theoretical or empirical, have then focused on Coyne (2007) has recently reviewed the reasons why cospeciation and host-switch minimizing the importance sympatric speciation is so controversial and why this of sympatric speciation, a mode of speciation that can be mode of speciation is so contested in evolutionary biolo- also defined as intra-host speciation or parasite duplica- gy. Sympatric speciation involves the splitting of an tion (Page 2003). However, the relative importance in ancestral species into two or more reproductively isolated number of congeneric parasite species or parasite flocks groups, the incipient species, without the need of geo- has been described earlier in the parasitological literature graphical isolation as involved in allopatric speciation. (Schad 1963, Gusev 1995, Beveridge et al. 2003, Boua- Importantly, the speciation should occur when these mer & Morand 2003, Matthee et al. 2004). incipient species are still in contact and are able to exchange genes. Interestingly, in his review, Coyne (2007) cited three studies on host parasite systems (Berlo- MODES OF SPECIATION IN PARASITES cher & Feder 2002, Sorenson et al. 2003, Simková et al. 2004) among five examples of sympatric speciation Earlier, it has been proposed that parasite phylogeny (Schliewen et al. 1994, Savolainen et al. 2006), suggest- mirrors host phylogeny, i.e. Farenholz’ rule, as summa- ing by this that host-parasite systems offer convincing rized by Klassen (1992) in a review on the history of host- models of sympatric speciation (McCoy 2003, Le Gac & parasite coevolution studies. Indeed, speciation of para- Giraud 2004, Giraud 2006). sites is often viewed to occur via co-speciation (Page However, for a long time it has been thought that the 2003, Clayton et al. 2004). Using a phylogenetic frame- evolution of parasite species should be closely linked to work, cospeciation in host-parasite systems was first the evolution of their host species. Hence, the emphasis demonstrated for pocket gophers and their chewing lice was put on co-phylogenetic events with two major para- (Hafner & Nadler 1988, Hafner et al. 1994, Reed & Haf- digms to explain the patterns of host-parasite associa- ner 1997) followed by several studies on various host- tions: switching events or inheritance from ancestors. parasite associations, such as primates and their pinworms These two paradigms have been summarized as ‘associa- (Hugot 1999). tion by colonization and association by descent (Brooks Several methodological development and improve- & McLennan 1991). ment of statistical tests of cospeciation have been pro- 126 S. MORAND, A. ŠIMKOVÁ, S. GOURBIÈRE posed: Brooks Parsimony Analysis (Brooks & McLennan bour more congeneric parasites than terrestrial birds, the 1991), tree reconciliation (Charleston 1998, Page & Char- main result was found in mammals. Poulin (1999) found leston 1998, Page 2003, Ronquist 1995), global fit meth- that large-bodied mammal species, or those living at low ods (Johnson et al. 2003; Legendre et al. 2002) (see Pater- latitudes, harbour more congeneric parasites than small- son & Bank 2001, Desdevises 2007, de Vienne et al. bodied mammals, or than those from higher latitudes. 2007). Allopatric parasite speciation was suggested to fol- This finding suggests that the size of the host, i.e. the host low the geographical isolation of their hosts as a plausible gut in this study, is a good predictor for the diversification mechanism of cospeciation (Weckstein 2004). However, of congeneric species. Large-bodied hosts seem to offer the mechanisms of parasite adaptation following the more opportunities for intra-host speciation than small- cospeciation events were rarely investigated. Cospecia- bodied hosts. Using congeneric parasites of fish, Šimková tion events were described in several host-parasite sys- et al. (2001) also showed that large-bodied fish harbour tems: chewing lice and pocket gophers (Hafner et al. more congeneric monogenean species than small-bodied 1994), pinworms and primates (Hugot 1999), Pneumo- fish. These observations confirm that the size of the “host cystis spp. and primates (Hugot et al. 2003), whereas as an island” is an important feature allowing the coexist- other studies failed to find extensive cospeciation, such as ence of several parasite species. A possible explanation is between chewing lice and penguins (Banks et al. 2006). that larger-bodied hosts have larger organs (guts in mam- In several host-parasite systems, there were no indices of mals, gills in fish) that offer more space but also more widespread cospeciation. This leads to a key question for micro-environments that allow parasites to exploit specif- evolutionary biologists: why and when do parasites fail to ically. speciate in response to host speciation (Johnson et al. Nevertheless, as emphasized by Poulin (1999) these 2003). communities of congeneric species may represent real Host-switch events have been exemplified in several species flocks, being the product of the radiation of an host-parasite systems (Desdevises et al. 2002), although ancestral taxon. Strict habitat selection is supposed to lead host shifts can produce congruent host and parasite phyl- to a higher frequency of sympatric speciation in parasite ogenies (Percy et al. 2004, Huyse & Volckaert 2005, de species than in free-living animals according to de Meeüs Vienne et al. 2007). Speciation following host switch is et al. (1995). Multiple congeners can also be the result of also widely observed in fish monogeneans (Desdevises et several independent host-switch events by congeneric al. 2002, Zietara & Lumme 2002, Huyse &Volckaert parasites that have evolved in other hosts (Paterson & 2005). Gray 1997). Vickery & Poulin (1998) as well suggested Finally, “missing the boat” or “extinction” was pro- that intra-host speciation could explain the occurrence of posed to explain the lack of incipient parasite species in congeneric parasite species in the same host species. Phy- incipient host species. This explanation refers to the logenetic information is then needed to discriminate hypothesis that the ancestral parasite species has missed among these hypotheses. one incipient host species during the host speciation proc- ess (Paterson & Gray 1997, Page 2003). WHAT IS SO DIFFICULT
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