Abstract
BackgroundHow various host–parasite combinations have been established is an important question in evolutionary biology. We have previously described two nematode species, Rhigonema naylae and Travassosinema claudiae, which are parasites of the xystodesmid millipede Parafontaria laminata in Aichi Prefecture, Japan. Rhigonema naylae belongs to the superfamily Rhigonematoidea, which exclusively consists of parasites of millipedes. T. claudiae belongs to the superfamily Thelastomatoidea, which includes a wide variety of species that parasitize many invertebrates. These nematodes were isolated together with a high prevalence; however, the phylogenetic, evolutionary, and ecological relationships between these two parasitic nematodes and between hosts and parasites are not well known.ResultsWe collected nine species (11 isolates) of xystodesmid millipedes from seven locations in Japan, and found that all species were co-infected with the parasitic nematodes Rhigonematoidea spp. and Thelastomatoidea spp. We found that the infection prevalence and population densities of Rhigonematoidea spp. were higher than those of Thelastomatoidea spp. However, the population densities of Rhigonematoidea spp. were not negatively affected by co-infection with Thelastomatoidea spp., suggesting that these parasites are not competitive. We also found a positive correlation between the prevalence of parasitic nematodes and host body size. In Rhigonematoidea spp., combinations of parasitic nematode groups and host genera seem to be fixed, suggesting the evolution of a more specialized interaction between Rhigonematoidea spp. and their host. On the other hand, host preference of Thelastomatoidea spp. was not specific to any millipede species, indicating a non-intimate interaction between these parasites and their hosts.ConclusionsThe two nematode superfamilies, Rhigonematoidea and Thelastomatoidea, have phylogenetically distinct origins, and might have acquired xystodesmid millipede parasitism independently. Currently, the two nematodes co-parasitize millipedes without any clear negative impact on each other or the host millipedes. Our study provides an example of balanced complex symbioses among parasitic nematodes and between parasitic nematodes and host millipedes, which have been established over a long evolutionary history.
Highlights
How various host–parasite combinations have been established is an important question in evolutionary biology
Two parasitic nematodes R. naylae and T. claudiae isolated from the two millipedes Parafontaria laminata Chubu University as a collection site (CU) and Parafontaria tonominea species complex CU We isolated two parasitic nematodes, R. naylae and T. claudiae, from the xystodesmid millipede, P. laminata, in the Chubu University campus in Aichi Prefecture, Japan (Table 1, Fig. 1)
A total of 113 P. laminata CU millipedes were captured from April 2018 to July 2019, and parasitic nematode infections were examined
Summary
How various host–parasite combinations have been established is an important question in evolutionary biology. T. claudiae belongs to the superfamily Thelastomatoidea, which includes a wide variety of species that parasitize many invertebrates These nematodes were isolated together with a high prevalence; the phylogenetic, evolutionary, and ecological relationships between these two parasitic nematodes and between hosts and parasites are not well known. Some parasitic nematodes live together with hosts as commensals [12, 24, 25, 54] or mutualistic partners [39], but others are harmful to the hosts [4, 7, 17, 56] These four interactions—phoresis, commensalism, parasitism, and mutualism—are all recognized as subcategories of symbiosis [15], and are commonly observed in the phylum Nematoda. Examples include pine wilt disease in Eastern Asia and Europe caused by the invasive pine-wood nematode Bursaphelenchus xylophilus [22], and crop diseases caused by a variety of plant parasitic/pathogenic nematodes in agricultural fields globally [61]
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