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The Evolution of Monogenean Diversity

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The Evolution of Monogenean Diversity International Journal for Parasitology 32 (2002) 245–254 www.parasitology-online.com Invited review The evolution of monogenean diversity Robert Poulin* Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand Received 10 April 2001; received in revised form 10 September 2001; accepted 28 September 2001 Abstract The Monogenea are an ideal group for investigations of the processes behind their past diversification and their present diversity for at least three reasons: they are diverse both in terms of morphology and numbers, they are generally host specific, and their phylogeny is well resolved, at least to the family level. The present investigation takes a broad look at monogenean diversity in order to try to determine whether the diversification of monogeneans is driven by some ecological features of the parasites themselves, or by extrinsic factors associated with their hosts. First, our current knowledge of monogenean diversity appears good enough to warrant investigation into its evolution. The body size of new species correlates negatively with their year of description both generally and within given families, i.e. it decreases over time in a way that suggests that only some of the smallest species are left to be discovered. Second, the occurrence of congeneric monogenean species on the same host species is not associated with host body size, once phylogenetic influences are controlled. This analysis suggests that host size is not one of the factors promoting local diversification of monogenean taxa. Third, the species richness of the different monogenean families does not correlate with the average body size of their members. Thus, this basic parasite life-history trait is not a determinant of diversification rates. Combined, the results of these separate analyses provide preliminary answers to some of the big questions concerning the diversification of monogeneans, but leave many other questions unanswered. The phylogenetic analytical frame- work adopted here should allow these questions to be tackled once the necessary data become available. q 2002 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved. Keywords: Body size; Congeneric species; Phylogenetic effects; Speciation; Sympatry 1. Introduction respect to their morphology and ecology: from an ancestor parasitic on the skin of early vertebrates, monogeneans have Estimating the present diversity of organisms and how it expanded to colonize internal as well as external organs of a is maintained, and understanding how they diversified in the range of living aquatic vertebrates, and now display a vari- past, are the new cornerstones of conservation biology, ecol- ety of designs (Kearn, 1994; Whittington et al., 2000). ogy and evolutionary biology. Given that parasites account Second, the phylogeny of monogenean families is well for a considerable proportion of existing biodiversity, these resolved (Boeger and Kritsky, 1993, 1997; Mollaret et al., questions are increasingly being asked in relation to para- 2000), and the elucidation of within-family relationships is sitic organisms (Brooks and Hoberg, 2000; Poulin and well under way (e.g. Sinnappah et al., 2001). A good knowl- Morand, 2000). The study of past parasite diversification edge of the relationships among members of a clade, espe- and present parasite biodiversity is still in its infancy, cially among higher taxa such as families, is essential for the however. study of diversity using modern comparative methods The Monogenea are an ideal parasite taxon for investiga- (Poulin, 1995; Sasal and Morand, 1998). Third, monoge- tions of past diversification and present diversity for at least neans tend to be host specific, i.e. each monogenean species three reasons. First, monogeneans are a diverse group, with infects only one or very few host species (Poulin, 1992; several thousand species currently described. Brooks and Sasal et al., 1999). This is not necessarily the outcome of McLennan (1993a) suggested that the Monogenea are the strict cospeciation between the parasites and their hosts, only clade among the parasitic flatworms to have undergone although this has been documented in monogeneans (Desde- an adaptive radiation (but see Rohde, 1996). Monogeneans vises et al., 2000). There is also evidence of host switching are diverse not only in terms of numbers but also with during the coevolutionary history of monogeneans and their hosts, from studies both at the level of sister species (e.g. * Tel.: 164-3-479-7983; fax: 164-3-479-7584. Gue´gan and Agne`se, 1991) and among more basal branches E-mail address: [email protected] (R. Poulin). in the monogenean phylogeny (Boeger and Kritsky, 1997). 0020-7519/02/$20.00 q 2002 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved. PII: S0020-7519(01)00329-0 246 R. Poulin / International Journal for Parasitology 32 (2002) 245–254 The high host specificity shown by most monogeneans, described. In many taxa, recently described species tend to however, makes it easier to search for a link between the be of smaller size than previously recognised species, ecological characteristics of the hosts and the diversity of simply because the probability of detection increases with their monogenean parasites, and to control for the phyloge- body size (Gaston, 1991; Gaston and Blackburn, 1994). In netic history of their associations. the early years of scientific investigation, both small and In this paper, I will take a broad look at monogenean large species are found and described formally; as time diversity in order to try to determine whether the diversifi- goes by, all the large species are known and the only ones cation of monogeneans is driven by some ecological left to be documented are the small ones. The efficiency of features of the parasites themselves, or by extrinsic factors the numerous methods used to collect ectoparasites on fish associated with their hosts or their external environment. I varies greatly (see Grutter, 1995), and it is likely that earlier will use various databases and apply modern comparative surveys based on visual inspection of the host missed many methods as much as possible (Sasal and Morand, 1998). of the smaller parasites. Using this approach with parasitic Any such attempt at general answers is bound to be met copepods, Poulin (1996a) found a negative correlation with criticism: exceptions can always be found to the between parasite body size and year of description among general trends that emerge from comparative analyses. In copepod species parasitic on fish hosts, but there was no a sense, the analyses presented here can be viewed as preli- relationship between these variables among copepod minary. My aim, though, is to provide tentative answers to species parasitic on invertebrate hosts. These results mean some big general questions, and not to find definitive that we have achieved a good inventory of copepods para- answers to specific questions. The broad patterns, if any, sitic on fish, since only the small species are left undiscov- that emerge from the comparative analyses can be used to ered, whereas our knowledge of copepods parasitic on generate hypotheses about the evolutionary processes that invertebrates is much more patchy and many large-bodied promote monogenean diversification, hypotheses that can species are yet to be recorded even today. then be tested in specific systems. Here, I will proceed with a similar analysis on monoge- Three separate investigations are combined here to tackle nean species. If no relationship is observed between the the issue of monogenean diversity. First, it is important to body size of monogenean species and their year of descrip- assess how good our estimates of monogenean diversity tion, it will mean that we are a long way from a complete really are, and I will try to evaluate how far we are from a inventory, even of the relatively large-bodied species. If, on complete inventory of living monogenean species. Any the other hand, a negative correlation is observed between attempt to understand the diversification of a group must body size and year of description, it will indicate that we be based on reasonably comprehensive estimates of the have reached a point where only some very small species group’s diversity, and I will thus, as a first step, make sure are left undiscovered. Any conclusion will only be based on we know enough about monogenean diversity to study its existing data, of course, but I assume that its implications determinants. Second, I will focus on congeneric monoge- would extend to the yet-to-be-discovered monogenean nean species that exploit the same host species, and attempt fauna. to determine whether one external factor, namely the size of the host, can promote the coexistence of closely related 2.1. Methods species. The assumption here is that congeneric species on the same host are sister species, and that their occurrence is Data on body sizes of monogenean species described the result of an intrahost speciation event. Third, I will before 1963 were obtained from Yamaguti (1963), and verify whether the species richness of the different mono- those from monogenean species described since then were genean families correlates with the average body size of obtained from original species descriptions published in their members, to see whether this basic parasite life-history four selected journals: Journal of Parasitology, Journal of trait is a determinant of diversification rates. Helminthology, Proceedings of the Helminthological Society of Washington, and Folia Parasitologica. Yamaguti (1963) did not present body size data for all the species he 2. How well do we know monogenean diversity? compiled, and the four above journals do not account for all species described since the 1960s, but together these sources We do not have a complete inventory of existing mono- provide a representative sample. Monogenean body size genean species, and we will not have one for many years, if was taken as total body length; when a range was provided ever.
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