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. 2022 May;31(9):2730-2751.
doi: 10.1111/mec.16421. Epub 2022 Apr 2.

Assessing rates of parasite coinfection and spatiotemporal strain variation via metabarcoding: Insights for the conservation of European turtle doves Streptopelia turtur

Rebecca C Thomas  1   2 , Jenny C Dunn  3   4 , Deborah A Dawson  2 , Helen Hipperson  2 , Gavin J Horsburgh  2 , Antony J Morris  3 , Chris Orsman  3 , John Mallord  3 , Philip V Grice  5 , Keith C Hamer  1 , Cyril Eraud  6 , Lormée Hervé  6 , Simon J Goodman  1
Affiliations

Assessing rates of parasite coinfection and spatiotemporal strain variation via metabarcoding: Insights for the conservation of European turtle doves Streptopelia turtur

Rebecca C Thomas et al. Mol Ecol. 2022 May.

Abstract

Understanding the frequency, spatiotemporal dynamics and impacts of parasite coinfections is fundamental to developing control measures and predicting disease impacts. The European turtle dove (Streptopelia turtur) is one of Europe's most threatened bird species. High prevalence of infection by the protozoan parasite Trichomonas gallinae has previously been identified, but the role of this and other coinfecting parasites in turtle dove declines remains unclear. Using a high-throughput sequencing approach, we identified seven strains of T. gallinae, including two novel strains, from ITS1/5.8S/ITS2 ribosomal sequences in turtle doves on breeding and wintering grounds, with further intrastrain variation and four novel subtypes revealed by the iron-hydrogenase gene. High spatiotemporal turnover was observed in T. gallinae strain composition, and infection was prevalent in all populations (89%-100%). Coinfection by multiple Trichomonas strains was rarer than expected (1% observed compared to 38.6% expected), suggesting either within-host competition, or high mortality of coinfected individuals. In contrast, coinfection by multiple haemosporidians was common (43%), as was coinfection by haemosporidians and T. gallinae (90%), with positive associations between strains of T. gallinae and Leucocytozoon suggesting a mechanism such as parasite-induced immune modulation. We found no evidence for negative associations between coinfections and host body condition. We suggest that longitudinal studies involving the recapture and investigation of infection status of individuals over their lifespan are crucial to understand the epidemiology of coinfections in natural populations.

Keywords: Trichomonas gallinae; NGS; coinfection; haemosporidians; high-throughput sequencing; next-generation sequencing.

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Conflict of interest statement

The authors have no conflict of interest.

Figures

FIGURE 1
FIGURE 1
Maximum clade credibility tree of the ITS ribosomal region of all unique Trichomonas gallinae sequences from GenBank, using Bayesian inferenced in BEAST. Sequences isolated from turtle doves in our study are marked with a *; all other sequences are labelled with an example GenBank accession number and the full list of sequences analysed is provided in Appendix S2; sequences isolated from turtle doves in our and other studies are emboldened. Also labelled are the hosts and location from which each sequence has been isolated. If a sequence was isolated from more than one species within a family, or more than one country within a continent, the sequence is labelled with that family or continent; if a sequence was isolated from only one species within a family, or only one country within a continent, the sequence is labelled with the species and or country. Branch reliability is provided as a proportion of 1000 bootstrap replicates
FIGURE 2
FIGURE 2
Maximum clade credibility tree of the Fe‐hyd ribosomal region of all unique Trichomonas gallinae sequences from GenBank, using Bayesian inference in BEAST. Sequences isolated from turtle doves in our study are marked with a *; all other sequences are labelled with an example GenBank accession number and the full list of sequences analysed is provided in Appendix S3; sequences isolated from turtle doves in our and other studies are emboldened. Also labelled are the hosts and location from which each sequence has been isolated. If a sequence was isolated from more than one species within a family, or more than one country within a continent, the sequence is labelled with that family or continent; if a sequence was isolated from only one species within a family, or only one country within a continent, the sequence is labelled with the species and or country. Branch reliability is provided as a proportion of 1000 bootstrap replicates
FIGURE 3
FIGURE 3
Pie charts reflecting the strain frequency composition of Trichomonas gallinae (based on the ITS type) in the sampled populations of turtle doves
FIGURE 4
FIGURE 4
Between year differences in prevalence of Trichomonas gallinae strains (a) type A, (b) GEO, and (c) Tcl‐1. Dots show mean values ± SE. Between country differences in prevalence of T. gallinae strains (d) type A, (e) type C, and (f) GEO. Bars show mean values ± SE. Results from statistical analyses are given in Table 5; letters above bars indicate significant differences at p < .05; letters in brackets indicate marginally significant differences at .05 < p < .1
FIGURE 5
FIGURE 5
Cooccurrence matrix for parasite strains showing nonrandom associations between Trichomonas gallinae (GEO, type A and type C), Haemoproteus (HD‐TD) and Leucocytozoon (LA‐TD, LB‐TD, LD‐TD and LE‐TD) strains in UK breeding turtle doves
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