Correlation of parasite speciation and specificity with host evolutionary relationships

Abstract

Protopolystoma (Monogenea, Polystomatidae) is strictly specific to the anuran amphibian genus Xenopus. The host group is characterised by a polyploid series in which chromosome numbers reflect diploid, tetraploid, octoploid and dodecaploid constitutions; the series is considered to have evolved through interspecies hybridisation and genome duplication. This study correlates information on host evolutionary relationships with patterns of parasite speciation and host specificity. Protopolystoma is restricted to one subgenus (Xenopus) with multiples of 36 chromosomes, and is absent from the subgenus Silurana (with multiples of 20 chromosomes). Molecular, biochemical and karyotype evidence distinguishes three subgroups within Xenopus. Representative species from each subgroup, Xenopus muelleri, Xenopus fraseri and Xenopus laevis, have been examined for polystomatid infection. Two species of Protopolystoma occur in each of these host species. In X. muelleri, the two Protopolystoma species reflect parasite co-speciation corresponding with the divergence of two sibling host species. Xenopus fraseri and X. laevis (both with 2n = 36 chromosomes) are implicated in the hybrid origin of two octoploid species, Xenopus wittei and Xenopus vestitus (both 2n = 72). The relationships of the Protopolystoma species in these Xenopus taxa reflect this presumed ancestry. Xenopus wittei carries two species of Protopolystoma, one shared with X. fraseri and the other shared with X. laevis. Xenopus vestitus carries a single species of Protopolystoma which is shared with X. laevis but there is no "heirloom" which reflects its hybrid origin involving X. fraseri. In addition to these shared parasite species which may reflect shared host genes, X. fraseri and X. laevis each carry separate species-specific Protopolystoma which do not occur in other Xenopus species even where there is evidence of common genetic information (as in the allopolyploid wittei and vestitus). This case study may be interpreted as indicating a powerful influence of host genetic factors on susceptibility to infection, host-specificity, and parasite speciation.