Trends in Parasitology
ReviewUngulate Helminth Transmission and Two Evolutionary Puzzles
Section snippets
Two Evolutionary Puzzles
The evolution of complex life cycles in helminths has attracted much recent and ongoing interest [1, 2, 3]. This study originated with two puzzling observations on helminth life cycles in ungulates. First, ungulates (see Glossary), as primary consumers in conventional food webs, should be directly infected by free-living helminth propagules (eggs or larvae), which are voided with ungulate faeces, typically landing on herbage. Second, as large mammals with high survival/reproduction prospects
Helminths in Ungulates
Ungulates are commonly infected by helminths, which continue to be an economic problem [9].
We provide an overview of the diversity of ungulate helminth life cycles to explore transmission barriers and the function of ungulates as hosts. We surveyed the literature for ungulate helminths, mostly consulting original sources (see Box S1 in the supplemental information online). For each helminth family, we recorded the ungulate host status (intermediate, paratenic, or definitive), the number of
Nontrophic Transmission Strategies
Although trophic transmission modes are overwhelmingly the commonest forms of transmission to ungulates (Figure 1), nontrophic modes occur, most notably among nematodes. Here arthropod vector transmission to ungulates has arisen thrice (Figure 1), occurring in five nematode families (Table 1). Since these arthropods are closely associated with ungulates, no obvious transmission barrier exists. Some vectors deposit infective larvae close to the site of infection on the ungulate; these then
Trophic Transmission Strategies
Figure 2 outlines the principal modes of trophic transmission to ungulates, and it shows where a trophic vacuum may limit transmission. In basic food webs, plants are primary producers (trophic level 1), and herbivores are primary consumers (trophic level 2). Ungulates, with their main diet of herbage, should therefore acquire most of their trophically transmitted helminths from larval stages associated with or on vegetation. This is in fact so. Some 64% of trematode and 35% of nematode
Why Should Ungulates Ever Be Intermediate Hosts?
The large size of ungulates, with abundant niche space and potential resources, together with low ungulate mortality rates, provides optimum habitat for adult helminths. The vast majority of ungulate helminths use the ungulate as their definitive host (Table 1). Of 239 genera infecting ungulates (see Tables S1–S5 in the supplemental information online), 233 (97.5%) treat the ungulates as definitive hosts, but only four (1.7%) treat them as intermediate hosts, and two (0.8%) treat them as
Concluding Remarks
Our survey of ungulate transmission, together with phylogenetic mapping, indicated that ungulate helminth parasitism has independently evolved some 25 times via six distinct transmission routes. In many cases, these transmission strategies probably predate the evolution of ungulates 65 to 60 million years ago, such that helminth colonisation of ungulates occurred by host switching. Host switching is well illustrated by the polystomatid monogenean Oculotrema hippopotami on hippopotamus, the only
Acknowledgments
D.B. was supported by the Deutsche Forschungsgemeinschaft (grant DFG 5336/3-1). We thank the editor and the three reviewers for their insights, which have greatly improved the review.
Glossary
- Bauplan (German: blueprint)
- used in biology to refer to the shared characteristics of members of a systematic group (taxon). The concept is frequently used in systematics and evolution.
- Definitive host
- a host in a life cycle in which the parasite attains sexual maturity and produces propagules.
- Intermediate host
- a host occurring between the propagule stage in a life cycle and the definitive host, in which growth and development of the larva takes place.
- Paratenic host
- a host occurring between the
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2023, Ecological ModellingCitation Excerpt :Nematodes have been shown to continue to persist near waterholes, relative to nearby grazing zones, even despite unfavorable environmental conditions (Ng'ang'a et al., 2004). Nematodes transmitted via ingestion from the environment have a latency between hatching and infectivity, posited as an evolved counterstrategy to ungulate fecal avoidance behavior (Chubb et al., 2020) – as such, the presence of dung is partially decoupled temporally from infective parasite peaks. Numerous ungulate species, including bovines, have a strong aversion to fecal depositions (Dohi et al., 1991; Fankhauser et al., 2008; Hutchings et al., 1998; Schütz et al., 2021; Smith et al., 2009; Verwer et al., 2016; Ezenwa 2004).
Pancreatic eurytrematosis in small ruminants: A forgotten disease or an untold history?
2022, Veterinary ParasitologyCitation Excerpt :Herein, we review the historical and technical information on PE in goats and sheep gathered from scattered and often unnoticed knowledge worldwide. Trematodes have developed and adapted successfully to environmental adversities over time as major parasites and have become a risk to the health of humans and animals as agents of foodborne and neglected tropical diseases (Fürst et al., 2012; Chubb et al., 2020). The Eurytrema genus comprises Digenean trematodes that have affected domestic and wild ruminants, but they have often remained unnoticed for their relevance and impact on livestock production (Tang and Tang, 1977; Little, 1979; Ilha et al., 2005; Patra et al., 2022).
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2022, Current Research in Parasitology and Vector-Borne DiseasesCitation Excerpt :Parasites with longer CLCs have smaller first hosts (Fig. 3); the first hosts in three- and four-host life-cycles are > 100,000 times smaller than the first (and only) host in one-host cycles, and they are probably > 100,000 times as abundant (Hatton et al., 2019). Propagules are normal-sized food for the small first hosts in longer CLCs, whereas the large first hosts in one-host cycles probably consume propagules accidentally (Fig. 3), especially if they avoid foraging near egg-laden faeces (Chubb et al., 2020). By first infecting smaller, more abundant hosts, longer CLCs become bridges to hard-to-reach hosts.
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