sign in sign up
<<
Home , Cospeciation, Secondary contact, Sexual selection

BEYOND THE PARADIGMS OF AND HOSTSWITCH: IS SYMPATRIC 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 AN IMPORTANT MODE OF SPECIATION FOR PARASITES?. Vie et Milieu / & 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’, 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- 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 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 . (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 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 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 , the 1991), tree reconciliation (Charleston 1998, Page & Char- main result was found in . Poulin (1999) found leston 1998, Page 2003, Ronquist 1995), global fit meth- that large-bodied 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 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 . 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 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 “” 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 IN SYMPATRIC SPECIATION? AND HOW TO TEST ITS CONGENERIC SPECIES IN PARASITES EXISTENCE?

Multiple parasite congeners have been earlier exempli- Coyne (2007) emphasized that sympatric speciation is fied as evidence for radiation of species-flocks (Schad “hard to achieve because of the 1963, Petter 1966, Inglis 1971, Matthee et al. 2005). that occurs when incipient species interbreed. This recom- Kennedy & Bush (1992) and Poulin (1999) have surveyed bination breaks up the correlation between co-adapted published studies and found that congeneric helminths groups of genes that is necessary for species to form”. were quite common in parasite communities. For exam- There is a cost of hybridization due to the production of ple, several congeneric species are well-known: oxyurid with intermediate phenotype of intermediate fit- of tortoises (Schad 1963, Bouamer & Morand ness (Kondrashov & Shpak 1998, Kondrashov & Kon- 2003), strongyloid nematodes of horses and elephants drashov 1999). We should also take into consideration (Bucknell et al. 1996), cloacinids of kangaroos (Bev- that most theoretical models seem to show that sympatric eridge & Spratt 1996) and monogeneans of fish (Pariselle speciation occur under very restrictive conditions in real et al. 2003, Šimková et al. 2006). biological situations (Coyne & Price 2000, Gourbière Poulin (1999) tested the influences of ecological deter- 2004, Jiggins 2006). minants, such as body size, host density or latitude, as Establishing sympatric speciation requires four condi- explanatory factors of species richness in congeneric par- tions according to Coyne (2007): asite flocks parasitizing birds and mammals. Although - (i) the species must be sympatric; the incipient spe- Poulin (1999) found that aquatic species tend to har- cies could have speciated sympatrically and subsequently

Vie Milieu, 2008, 58 (2) SYMPATRIC SPECIATION IS IMPORTANT IN PARASITES 127 have become allopatric; , preferably based on genetic differ- - (ii) the sympatric species must show substantial ences;

Fig. 1. - Tanglegram of Dactylogyrus and cyprinid species (from Šimková et al. 2004). Intrahost duplications are depicted on the trees. Dactylogyrus speciation by intrahost duplication supported by bootstrap percentage greater than 50 are given in bold. Potential coevo- lution events are indicated by a, b, and c.

Vie Milieu, 2008, 58 (2) 128 S. MORAND, A. ŠIMKOVÁ, S. GOURBIÈRE

- (iii) the sympatric taxa must be sister species; how- than their hosts. Allopatric speciation may imply changes ever, this criterion could be difficult to meet as any in host-specificity of monogeneans that should first hybridization between taxa will render them closely relat- increase their host range by infecting fish in ed; secondary contacts and second decrease their host range - (iv) the biogeographic and evolutionary history of the to reach the strict host-specificity currently observed. As groups must make the existence of an allopatric phase strict host-specificity has been shown to be ancestral in very unlikely; a hard task as it requires to demonstrate most Dactylogyrus lineages (Šimková et al. 2006), this that the incipient species were never geographically iso- renders the latter scenario unlikely. lated. As mentioned above, monogeneans are not randomly Coyne (2007) suggested that cases of sympatric specia- distributed on fish gills. They show preferred positions on tion can be found on islands, such as oceanic islands or gills, which were investigated by Šimková et al. (2000, lakes, by searching for closely related species. Endemic 2006). For each parasite individual, position on gill arch, sister species of mobile organisms contained in these gill segment and gill area was recorded. The preferred islands are likely to have evolved without physical isola- position, or niche, corresponds to the sector where the tion (i.e. fish of African lakes). He suggested that maximum number of parasite individuals was found. The other cases can be found in a single host species that har- preferred niche (gill arch, segment and area) was mapped bours sister species of host-specific parasites. This corre- onto the using MacClade with Farris sponds to sympatric speciation within a host, with the host optimization (Maddison & Maddison 1992) (Fig. 2). Dac- considered as an island for its parasites (Kuris et al. 1980). tylogyrus species from one lineage, parasitizing the same host, then recognized as a case of intra-host speciation, were separated by their position (arch, segment or area) AN EXAMPLE OF SYMPATRIC (INTRA-HOST) on fish gills. If we consider changes, we note that no sis- SPECIATION: DACTYLOGYRUS SPP. OF ter species have identical niches for all three gill dimen- CYPRINID FISH sions. At least one of the niche parameters (arch, segment or area) has changed between these species. Finally, Dactylogyrus species are a group of monogenean gill Šimková et al. (2004, 2006) hypothesized that this mode parasites that are highly specific to freshwater fish of the of sympatric speciation should be closely related to mor- family Cyprinidae. Šimková et al. (2004) sampled Dacty- phological evolution of attachment organs. logyrus species from cyprinids in Europe, and using molecular data proposed a phylogeny of most Dactylogy- rus species from Central Europe. They used TreeMap 1.0 COMPETITIVE SPECIATION AS THE (Page 1994) to depict the host-parasite associations using MECHANISM OF INTRA-HOST SPECIATION? a Dactylogyrus phylogenetic tree inferred from the analy- sis of molecular data and a cyprinid tree (Fig. 1). The Competitive speciation is based on theoretical models comparison of host and parasite phylogenetic relation- in which a quantitative ecological trait is under disruptive ships indicated that a high number of intra-host speciation selection generated by frequency and density dependent occurred in Dactylogyrus lineages. Then, parasite diversi- intra-specific competition (Dieckmann et al. 2004, Coyne fication can be mainly explained by these speciation & Orr 2004). This ecological trait can pleiotropically events that are correlated to strict host specificity. affect in some models (e.g. Gourbière 2004), The four conditions of Coyne (2007) seem to be met: while other models describe the evolution of pref- - (i) the parasite species are sympatric, they live on the erences according to the ecological trait under natural gills of the same host species, although they are not dis- selection (Bürger et al. 2006). All these theoretical mod- tributed randomly on the gills (see below); els refer to the ecological notion of character displace- - (ii) reproductive isolation is associated with genetic ment (Taper & Case 1985). Gourbière et al. (unpublished) isolation; using Dactylogyrus species have investigated the condi- - (iii) the congeneric parasites are sister species as tions for within-host competitive speciation of parasites revealed by the tanglegram (Fig.1); and shown that they are exactly the same as the condi- - (iv) the biogeographic and evolutionary history of the tions for competitive diversification of non-parasitic spe- cyprinid hosts make the existence of an allopatric phase cies (Dieckmann & Doebeli 1999, Doebeli & Dieckmann for these congeneric parasite species very unlikely and 2000). These conditions are surprisingly robust whatever limited to three co-speciation events depicted by TreeM- the life-histories of the considered organisms, parasites or ap. However, it remains possible that some Dactylogyrus free-living, and moreover are quite easy to get. species have speciated allopatrically in geographically How and when competitive speciation can play a role isolated fish populations, and then re-infected fish hosts in parasite diversification may depend on the host, and after between host populations. This more precisely on the potential niches that the host can scenario implies that monogeneans evolve more rapidly offer for parasites to live on. Competitive speciation may

Vie Milieu, 2008, 58 (2) SYMPATRIC SPECIATION IS IMPORTANT IN PARASITES 129

Fig. 2. - Mapping of preferred position of Dactylogyrus on fish gills (upper drawing) onto the Dactylogyrus phylogeny (from Šimková et al. 2004), lower drawings from left to right: arc, segment, area of fish gill.

Vie Milieu, 2008, 58 (2) 130 S. MORAND, A. ŠIMKOVÁ, S. GOURBIÈRE also depend on the parasite itself, and on the quantitative may be more common in other parasitic systems as new traits that are susceptible to be affected. studies are conducted (Giraud 2006, Lopez-Villavicencio One additional difficulty with intra-host speciation is et al. 2007, Pérez-Tris et al. 2007). that the opportunity to observe it on the tanglegram Future studies should investigate the mechanisms that depends on additional host features. For instance, the promote sympatric speciation. For this we need theoreti- of the hosts, such as diet preferences or spatial cal models, biological investigations and comparative distribution, can change the actual number of host-switch tests. Competitive speciation models offer the way to the- events, which will change the possibility to detect intra- oretically study intra-host speciation. Species diversifica- host speciation. This is simply because a high rate of host- tion is mechanically associated with post-zygotic isola- switches would tend to shorten the time period where the tion, as hybrids with intermediate phenotype should expe- monophyletic signal can be detected after within-host rience strong competition from individuals of both incipi- (see also the link between host ecology ent species (i.e. the cost of hybridization). This, in turns and parasite specificity, Šimková et al. 2006). This may generates the conditions for the evolution of pre-zygotic explain why intra-host speciation should be more easily isolation. The conditions for the evolution of pre-zygotic observed in freshwater fish, where fish species are more isolation may be more restrictive than the conditions for isolated “as islands” from each others due to the river sys- evolutionary diversification. This has actually been loose- tems or ecological specialisation. This isolation may pre- ly reported in previous studies investigating reinforce- vent host-switching events. ment by evolution of with respect to Parasites should show ecological traits linked to poten- either the ecological trait under disruptive selection or a tial competition and to reproductive isolation. Coexisting neutral marker trait (Gourbière & Mallet 2005). We need monogenean species have more similar morphology in to adapt these theoretical models to the parasitic mode of attachment organs when they live in close contact on gills, life. Second, we need to find the traits that promote the but are more dissimilar in the size of their copulatory coexistence of congeneric species on the same hosts. Can- organs (Rohde & Hobbs 1986, Rohde 1989, Šimková et didate traits are haptor morphology for gill monogeneans al. 2002). Morphological evolution of the attachment (Šimková et al. 2001). However, we should be aware that can be viewed as the result of adaptive processes we are far from knowing the traits promoting the coexist- for selection of the position on gill of a given host fish, ence of other parasites such as gut nematodes. Next, we whereas morphological evolution of the reproductive should show whether these traits are only related to coex- apparatus can be viewed as the result of the evolution of istence or to host micro-environment exploitation. Are pre-zygotic barriers among incipient species (Morand et these traits involved in the speciation process? The traits al. 2002, Jarkovský et al. 2004). Competition process associated with pre-zygotic isolation and assortative mat- may have lead to switch in the “niche position space” on ing seem to be good candidates for investigating the the gills, whereas pre-zygotic barriers have helped to mechanism of intra-host speciation processes. Last, we maintain the incipient species integrity. need to perform comparative analyses using a good phyl- ogenetic framework (Morand & Poulin 2003), which may allow us to test the relevant hypotheses. CONCLUSION AND SUGGESTIONS FOR Finally, paraphrasing Jiggins (2006) and knowing the FURTHER RESEARCH difficulty of investigating the case of speciation, we should abandon the assumption that allopatric speciation The two paradigms of parasite speciation, cospeciation is the “null hypothesis” as we always refer to the hypoth- and host-switch, have focused the attention of evolution- esis of speciation with . Future research should ary biologists on specific cases of host-parasite models, concentrate on the more proximal causes of speciation where the number of congeneric species living on one and on the potential traits causing divergence. host species are often low. Investigating the process of intra-host speciation in parasites implies to focus on the Acknowledgements - Dactylogyrus research was partially study of parasite flocks that are far from being rare funded by the Ichthyoparasitology, Centre of Excellence, Proj- ect No. LC 522, by Ministry of Education, Youth and Sports of (Kennedy & Bush 1992, Poulin 1999). the Czech Republic. A.Š. was supported by a Research Project Here we suggest that sympatric speciation, or intra- from Masaryk University, Brno, Project No. MSM 0021622416. host speciation, represents a considerable process of spe- We thank an anonymous referee for helpful comments. ciation in gill monogeneans. This mode of speciation is potentially more frequent as it is obscured by host-switch favoured in rich-host communities, i.e. marine environ- REFERENCES ment for example (Desdevises et al. 2002, Plaisance et al. 2005), or where no ecological barriers may limit host- Banks JC, Palma RL, Paterson AM 2006. Cophylogenetic rela- switch events such as hydrological basins in freshwater tionships between penguins and their chewing lice. J Evol environment (Pariselle et al. 2003). Intra-host speciation Biol 19: 156-166.

Vie Milieu, 2008, 58 (2) SYMPATRIC SPECIATION IS IMPORTANT IN PARASITES 131

Bentz S, Leroy S, du Preez, L, Mariaux J, Vaucher C, Verneau O Gourbière S, Mallet J 2005. Has adaptive dynamics contributed 2001. Origin and evolution of African Polystoma (Monoge- to the understanding of adaptive and sympatric speciation? J nea: Polystomatidae) assessed by molecular methods. Int J Evol Biol 18:1201-1204. Parasitol 31: 697-705. Gusev AV 1995. Some pathways and factors of monogenean Berlocher SH, Feder JL 2002. Sympatric speciation in phy- . Can J Fish Aquatic Sci 52: 52-56 tophagous : moving beyond controversy? Ann Rev Hafner MS, Nadler SA 1988. Phylogenetic trees support the Entomol 47: 773-815. coevolution of parasites and their hosts. Nature 332: 258- Bucknell D, Hoste H, Gasser RB, Beveridge I 1996. The struc- 259. ture of the community of strongyloid nematodes of domestic Hafner MS, Sudman PD, Villablanca, FX, Spradling TA, equids. J Helminthol 70: 185-192. Demestes JW, Nadler SA 1994. Disparate rates of molecular Beveridge I, Chilton NB, Spratt DM 2002. The occurrence of evolution in cospeciating hosts and parasites. Science 265: species flocks in the genus Cloacina (Strongyloi- 1087-1090. dea : Cloacininae), parasitic in the stomachs of kangaroos Hugot JP 1999. Primates and their pinworm parasites: The Cam- and wallabies. Aust J Zool 50: 597–620. eron hypothesis revisited. Syst Biol 48: 523-546. Beveridge I, Spratt DM 1996. The helminth fauna of Australasi- Hugot JP, Demanche C, Barriel V, Dei-Cas E, Guillot J 2003. an marsupials: Origins and evolutionary . Adv Para- Phylogenetic and evolution of -derived sitol 37: 135-254. Pneumocystis based on mitochondrial or nuclear DNA Bouamer S, Morand S 2003. Phylogeny of Palaearctic Pharyn- sequences comparison. Syst Biol 52: 735-744 godonidae parasite species of Testudinidae: a morphological Huyse T, Volckaert FA 2005. Comparing host and parasite phyl- approach. Can J Zool 81: 1885-1893. ogenies: Gyrodactylus flatworms jumping from goby to Brooks DR, McLennan DA 1991. Phylogeny, ecology, and goby. Syst Biol 54: 710-8. behavior. A research program in comparative biology. The Inglis WG 1971. Speciation in parasitic nematodes. Adv Parasi- University of Chicago Press, London. tol 9: 201-223. Bürger R, Schneider KA, Willensdorfer M 2006. The conditions Jarkovský J, Morand S, Šimková A, Gelnar M 2004. Reproduc- for speciation through intraspecific competition. Evolution tive barriers of congeneric monogenean species (Dactylogy- 60: 2185-2206. rus: Monogenea): attachment apparatus morphology or cop- Charleston MA 1998. Jungles: a new solution to the host/para- ulatory incompatibility? Parasitol Res 92: 95-105. site phylogeny reconciliation problem. Math Biosci 149: Jiggins CD 2006. Sympatric Speciation: Why the Controversy? 191-223. Current Biology 16: R333-R334 Clayton DH, Bush SE, Johnson KP 2004. Ecology of congru- Johnson KP, Adams RJ, Page RDM, Clayton DH 2003. When ence: past meets present. Syst Biol 53: 165-173. do parasites fail to speciate in response to host speciation? Syst Biol 52: 37-47. Coyne JA 2007. Sympatric speciation. Current Biol 17: 787- 788. Kennedy CR, Bush AO 1992. Species richness in helminth com- munities: The importance of multiple congeners. Parasitolo- Coyne JA, Orr HA 2004. Speciation. Sinauer Associates, Sun- gy 104: 189-197. derland, MA. Klassen GJ 1992. Coevolution: A history of the - Coyne JA, Price TD 2000. Little evidence for sympatric specia- ary approach to studying host parasite associations. J Parasi- tion in island birds. Evolution 54: 2166-2171. tol 78: 573-587 Desdevises Y 2007. Cophylogeny: insights from fish-parasite Kondrashov AS, Kondrashov FA 1999. Interactions among systems. Parasitologia 49(3): 125-128. quantitative traits in the course of sympatric speciation. Desdevises Y, Morand S, Jousson O, Legendre P 2002. Coevo- Nature 400: 351-354. lution between Lamellodiscus (Monogenea: Diplectanidae) Kondrashov AS, Shpak M 1998. by and Sparidae (Teleostei): The study of a complex host-para- means of assortative mating. P Roy Soc B-Biol Sci 265: 2273- site system. Evolution 56: 2459-2471. 2278. de Meeüs T, Hochberg ME, Renaud F 1995. Maintenance of two Kuris AM, Blaustein AR, Alió JJ 1980. Hosts as islands. Am Nat genetic entities by habitat selection. Evol Ecol 9: 131-138. 116: 570-586. de Vienne DM, Giraud T, Shykoff JA 2007. When can host shifts Le Gac M, Giraud T 2004. What is sympatric speciation in para- produce congruent host and parasite phylogenies? A simula- sites? Trends Parasitol 20: 207-208. tion approach. J Evol Biol 20(4): 1428-1438. Legendre P, Desdevises Y, Bazin E 2002. A statistical test for Dieckmann U, Doebeli M 1999. On the origin of species by host-parasite coevolution. Syst Biol 51: 217-234. sympatric speciation. Nature 400: 354-357. Lopez-Villavicencio M, Jonot O, Coantic A, Hood ME, Enjal- Dieckmann U, Doebeli M, Metz JAJ, Tautz D 2004. Adaptive bert J, Giraud T 2007. Multiple Infections by the anther smut Speciation. Cambridge Studies in Adaptive Dynamics, Cam- pathogen are frequent and involve related strains. PLoS bridge University Press. Pathogens 3: e176. Doebeli M, Dieckmann U 2000. Evolutionary branching and Maddison WP, Maddison DR 1992. MacClade: analysis of phy- sympatric speciation caused by different types of ecological logeny and character evolution. Sinauer Associates, Sunder- interactions. Am Nat 156: S77-S101. land, MA. Giraud T 2006. Speciation in parasites: host switching does not Matthee S, Krecek RC, McGeoch MA 2004. A comparison of automatically lead to allopatry. Trends Parasitol. 22: 151- the intestinal helminth communities of Equidae in Southern 152 Africa. J Parasitol 90: 1263-1273. Gourbière S 2004. How do natural and contrib- McCoy KD 2003. Sympatric speciation in parasites – what is ute to sympatric speciation? J Evol Biol 17: 1297-1309. sympatry? Trends Parasitol 19: 400-404.

Vie Milieu, 2008, 58 (2) 132 S. MORAND, A. ŠIMKOVÁ, S. GOURBIÈRE

Morand S, Šimková A, Matejusovà I, Plaisance L, Verneau O, Ronquist F 1995. Reconstructing the history of host-parasite Desdevises Y 2002. Investigating patterns may reveal proc- associations using generalised parsimony. 11: esses: evolutionary ecology of ectoparasitic monogenean. Int 73-89. J Parasitol 32: 111-119. Schliewen UK, Tautz D, Pääbo S 1994. Sympatric speciation Morand S, Poulin R 2003. Phylogenies, the comparative method suggested by monophyly of crater lake . Nature 368: and parasite evolutionary ecology. Adv Parasitol 54: 281- 629-632. 302. Savolainen V, Anstett MC, Lexer C, Hutton I, Clarkson JJ, Page RDM 2003. Tangled Trees: Phylogeny, cospeciation, and Norup MV, Powell MP, Springate D, Salamin N, Baker WJ coevolution. The University of Chicago Press. 2006. Sympatric speciation in palms on an oceanic island. Page RDM, Charleston MA 1998. Trees within trees - phylog- Nature 441: 210-213. eny and historical associations. Trends Ecol Evol 13: 356- Schad GA 1963. Niche diversification in a parasite species 359. flock. Nature 198: 404-406. Pariselle A, Morand S, Deveney M, Pouyaud L 2003. Parasite Šimková A, Desdevises Y, Gelnar M, Morand S 2000. Co-exist- species richness of closely related hosts: historical scenario ence of nine gill ectoparasites (Dactylogyrus: Monogenea) and “genetic” hypothesis. In Combes C, Jourdane J eds, parasitising the roach (Rutilus rutilus L.): history and present Hommage à Louis Euzet: Taxonomy, ecology and evolution ecology. Int J Parasitol 30: 1077-1088. of metazoan parasites. PUP, Perpignan: 147-16. Šimková A, Desdevises Y, Gelnar M, Morand S 2001. Morpho- Paterson AM, Banks JB 2001. Analytical approaches to measur- metric correlates of host specificity in Dactylogyrus species ing cospeciation of host and parasites: through a glass, dark- (Monogenea) parasites of European Cyprinid fish. Parasitol- ly. Int J Parasitol 31: 1012-1022. ogy 123: 169-177. Paterson AM, Gray RD 1997. Host-parasite cospeciation, host Šimková A, Ondrackova M, Gelnar M, Morand S 2002. Mor- switching, and missing the boat. In Clayton DH Moore J eds, phology and coexistence of congeneric ectoparasite species: Host-Parasite Evolution: General Principles and Avian Mod- reinforcement of reproductive isolation? Biol J Linn Soc 76: els, Oxford University Press, Oxford: 236-250. 125-135. Percy DM, Page RDM, Cronk QCB 2004. Plant- interac- Šimková A, Morand S, Jobet E, Gelnar M, Verneau O 2004. tions: double-dating associated insect and plant lineages Molecular phylogeny of congeneric monogenean parasites reveals asynchronous radiations. Syst Biol 53: 120-127. (Dactylogyrus): a case of intrahost speciation. Evolution 58: Pérez-Tris J, Hellgren O, Krizanauskiene A, Jonas Waldenström 1001-1018. J, Secondi J, Bonneaud C, Jon Fjeldsa J, Hasselquist D, Šimková A, Verneau O, Gelnar M, Morand S 2006. Specificity Bensc S 2007. Within-Host Speciation of Malaria Parasites. and specialization of congeneric monogeneans parasitizing PLoS ONE: e235. Cyprinid fish. Evolution 60: 1023-1037. Petter AJ 1966. Équilibre des espèces dans les populations de Sorenson MD, Sefc KM, Payne RB 2003. Speciation by host Nématodes parasites du côlon des tortues terrestres. Mem switch in brood parasitic indigobirds. Nature 424: 928-931. Mus Natl Hist Nat Ser A Zool 39: 1-252. Taper ML, Case TJ 1985. Quantitative genetic models for the Plaisance L, Littlewood DTJ, Olson PD, Morand S 2005. coevolution of . Ecology 66:355-371. Molecular phylogeny of gill monogeneans (Platyhelminthes, Vickery WL, Poulin R 1998. Parasite extinction and colonisa- Monogenea, Dactylogyridae) and colonisation of Indo-West tion and the evolution of parasite communities: a simulation Pacific butterflyfish hosts (Perciformes, Chaetodontidae). study. Int J Parasitol 28: 727-737. Zool Scripta 34: 425-436. Weckstein JD 2004. explains cophylogenetic pat- Poulin R 1999. Speciation and diversification of parasite lineag- terns in toucan chewing lice. Syst Biol 53: 154-164. es: an analysis of congeneric parasite species in . Evol Ecol 13: 455-467. Zietara MS, Lumme J 2002. Speciation by host switch and adap- tive radiation in a fish parasite genus Gyrodactylus (Mono- Reed DL, Hafner MS 1997. Host specificity of chewing lice on genea, Gyrodactylidae). Evolution 56: 2445-2458. pocket gophers: A potential mechanism for cospeciation. J Mam 78: 655-660. Rohde K 1989. Simple ecological systems, simple solutions to complex problems? Evol Theory 8: 305-350. Rohde K, Hobbs R 1986. Species segregation: Competition of reinforcement of reproductive barriers? In Cremin M et al. eds. Parasite . Papers on parasites, their hosts and their Received November 8, 2007 associations to honour JFA Sprent, University of Queensland Accepted May 14, 2008 Press, St. Lucia: 189-199. Associate Editor : Y Desdevises

Vie Milieu, 2008, 58 (2)