Polyploid Hosts: Strange Attractors for Parasites?

Abstract

While a major force in higher plant evolution (Stebbins 1971, 1977), polyploidy is largely restricted among animals to lower vertebrates such as fish, amphibians and reptiles (Ohno 1970, Bogart 1980, Schultz 1980). Interestingly, many polyploid fish species occur in the African cyprinid family (Oellerman and Skelton 1990, Golubtsov and Krysanov 1993, Doadrio 1994, Guegan et al. 1995). Although cases of host-parasite associations in polyploid host species are absent in the literature, they are of interest because they permit comparative study of host-parasite adaptation. We aim to show here that polyploid host species may harbour higher parasite species richness than their diploid relatives, and in this context, studies of polyploids and their associated parasites may considerably help evolutionary ecologists and parasitologists to better understand hostparasite interactions. We have studied monogenean ectoparasites of North and West African freshwater fishes. The occurrence of monogenean host specificity is attributed to independent specialization which has evolved for reasons other than interspecific competition that can include host-parasite coevolution (Klassen and Beverley-Burton 1989, Guegan and Agnese 1991, Van Every and Kritsky 1992), enhancement of mating by congeners (Rohde 1989), or avoidance of hybridization (Euzet and Combes 1980). Patterns in monogenean community richness and organisation among host species have been explained by host body size and age (Guegan et al. 1992), host geographical range and latitudinal gradients (Rohde 1989), host diversity (Rohde 1989, Guegan and Kennedy 1993), or host phylogeny (Guegan and Kennedy 1993). We used the infracommunity species richness observed on the richest host individual (richness values are ranked from 0 to 13 across host species), for 29 African cyprinid fish species and a total of 618 collected specimens, and this data were regressed against the 6 independent variables: host species body size, geographical range, host diversity defined as the number of species per fish genus, host species phylogeny, latitudinal gradients (West and North Africa), and host species ploidy level (threefold levels of ploidy were found: 2n = 50, 2n = 100, 2n = 150). To address the question of whether the parasite species richness is correlated with some traits of their hosts, we applied both simple and multiple regression procedures (Sokal and Rohlf 1981). Generally, closely related host species are more likely to exhibit similar development than distant species (Felsenstein 1985, Pagel and Harvey 1988), and they cannot be treated as statistically independent points. For instance, a relationship between parasites and host ploidy level across all fish species may be a result of phylogenetic history since fish species that share common descent are likely to be subject to similar evolutionary constraints and are likely to exhibit similar ploidy level. Comparative methods have recently been proposed to take this non-independence into account, considering phylogeny fixed and controlling for its effect on regressions (Harvey and Pagel 1991). Here, we used the independent comparisons method (Pagel 1992, Purvis and Rambault 1994, 1995) to identify a set of independently evolved comparisons within fish taxa. The host phylogeny was obtained from morphological data together with molecular data. We made a second control for sampling effort (defined as the number of collected specimens per fish species), as uneven sampling bias affects richness estimates (Gregory 1990, Walther et al. 1995). For all regressions, host body size, host geographical range and host diversity logarithmic values were used (Harvey 1982). Parasite species richness values were log (x + 1) transformed. Across species of cyprinid fishes, the number of parasite species observed correlates positively, in decreasing order of significance, with host body size (r = 0.53, p = 0.001), host diversity (r = 0.45, p = 0.001), host phylogeny (r = 0.35, p = 0.001) and host ploidy level (r = 0.21, p = 0.005). The number of parasite species a fish species harbours does not correlate significantly with neither host latitude (r = 0.06, p = 0.186)