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Patterns of host specificity and transmission among parasites of wild ...

Patterns of host specificity and transmission among parasites of wild ...

652A.B. Pedersen et al.

652A.B. Pedersen et al. / International Journal for Parasitology 35 (2005) 647–657Fig. 3. The relationship between transmission strategy and host specificity within the three best-represented groups: (a) viruses (nZ80), (b) protozoa (nZ79),and (c) helminths (nZ153). The number of parasites transmitted by each strategy is represented by the height of each bar, and the specificity scores assigned toindividual parasite species are represented by colors within each bar, with darker colors indicating a greater level of host specificity.A higher proportion of helminths transmitted by intermediatehosts or non-close contact alone could infect hosts frommultiple families or orders (Fig. 3(c) and Table 1(c)).3.4. Comparison with parasites from humans anddomesticated animalsThe taxonomic distribution of parasites of wild primates(i.e. non-human primates) differed from parasites reportedfrom humans and domesticated species (Fig. 4(a)–(d); notethat arthropods were omitted for this comparison). The mostsignificant differences in the taxonomic representation ofparasites occurred between humans vs. wild primates(Fig. 4(a) and (b)), and this difference was highly significant(c 2 Z318.03, d.f.Z4, P!0.0001). In particular, 87% ofparasites from wild primates were helminths, viruses andprotozoa, whereas bacteria and fungi comprised themajority (60%) of human pathogens.Despite these differences, there was a high degree ofoverlap among parasites from humans and wild primates,with 114 (27.5%) shared between wild primates and humans(Table 2). Approximately half of all bacteria and fungireported from wild primates were also reported as humanpathogens. Even though the greatest total number ofparasites shared between the two databases involvedhelminths, only 20% of all wild primate helminths werereported to infect humans. As predicted, the vast majority(90%) of non-human primate parasites also reported from

Table 1Associations between parasite transmission strategy and host specificity based on chi-square analysis of major transmission routes (presence/absence) inrelation to host specificity scores(a) VirusesTransmission strategyAll data (nZ80) aDir c 2 d.f. P bClose contact C 33.24 4 0.000CloseCnon-close NS 4.77 4 0.372Vector borne K 31.60 4 0.000(b) ProtozoansTransmission strategy All data (nZ79) Excl. low confidence (nZ50)Dir c 2 d.f. P Dir c 2 d.f. P cClose contact K 18.44 4 0.001 K 14.05 4 0.007Non-close contact C 13.12 4 0.011 C 12.17 4 0.016CloseCnon-close K 16.97 4 0.002 K 14.10 4 0.007Vector borne C 16.37 4 0.003 C 14.31 4 0.006(c) HelminthsTransmission strategy All data (nZ163) Excl. low confidence (nZ80)Dir c 2 d.f. P Dir c 2 d.f. P dCloseCnon-close C 23.04 4 0.000 C 23.20 4 0.000Non-close contact K 15.10 4 0.005 K 12.10 4 0.016Vector borne C 10.91 4 0.028 NS 2.56 4 0.633Intermediate host K 31.72 4 0.000 K 9.95 4 0.014Each analysis was repeated using all available data and those for which high or moderate confidence was assigned to specificity scores. Symbols (C/K)indicate the directionality of the association (i.e. whether parasites with that transmission strategy were more or less specific than parasites transmitted by otherroutes). c 2 , Chi-square scores. d.f., Degrees of freedom, P, P value corrected by the Bonferroni method (aZ0.05/n, where n is the number of tests and a, b, cand d refer to the Bonferroni corrected P values.a No low confidence scores.b aZ0.017.c aZ0.0125.d aZ0.0125.A.B. Pedersen et al. / International Journal for Parasitology 35 (2005) 647–657 653humans were recorded as multihost parasites, capable ofinfecting hosts from multiple families and orders.Viruses reported from both humans and wild primateswere primarily RNA viruses (85% of shared viruses), andover half were transmitted by arthropod vectors (Fig. 5).Protozoa reported to infect both wild primates and humansspanned multiple phyla and were transmitted either by acombination of close and non-close contact (70%) orarthropod vectors (29%; Fig. 5). Approximately half(45%) of the helminths that overlapped with wild primateand human hosts had complex life cycles and transmissionby intermediate hosts, and the remainder were nematodestransmitted by non-close contact or arthropod vectors(Fig. 5). Only 10% of the shared parasites were recordedas being transmitted by close contact only, and all of thesewere viruses.Finally, 44.7% (51 of 114) of non-human primateparasites reported to infect humans were classified asemerging based on a recent analysis of risk factorsassociated with human diseases (Taylor et al., 2001). Overhalf of these ‘emerging parasites’ were viruses; in fact, 28%of all viruses reported from wild primates were classifiedas emerging in humans (Table 2). Moreover, there wasa significant association between emerging diseasesand transmission strategy (c 2 Z15.37; d.f.Z4; PZ0.008).Given that a shared parasite was transmitted by closecontact, it was highly likely to be recorded as emerging inhumans (Table 2(b)), and the same was true for parasitestransmitted by arthropod vectors. Shared parasites transmittedby intermediate hosts were least likely to be classifiedas emerging in humans (Table 2(b)).4. DiscussionWe found that a remarkable number of primatepathogens (68%) were reported to infect multiple hostspecies. Since most of these affected hosts were from morethan one family or order, our data suggest that speciesspecificparasites are an exception to the rule (Fig. 1). Thisobservation is consistent with patterns from studies ofpathogens in humans and domesticated animals (Cleavelandet al., 2001; Taylor et al., 2001; Woolhouse et al., 2001).However, it runs counter to the hypothesis that hostspecificity (and, more generally, niche specialisation) offersgreater opportunity for diversification and coexistenceamong parasitic organisms and their hosts (Berenbaum,1996; McPeek, 1996; Poulin, 1998). A number of factors

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