Genetic diversity and population genetics of large lungworms (Dictyocaulus, Nematoda) in wild deer in Hungary

Abstract

Dictyocaulus nematode worms live as parasites in the lower airways of ungulates and can cause significant disease in both wild and farmed hosts. This study represents the first population genetic analysis of large lungworms in wildlife. Specifically, we quantify genetic variation in Dictyocaulus lungworms from wild deer (red deer, fallow deer and roe deer) in Hungary, based on mitochondrial cytochrome c oxidase subunit 1 (cox1) sequence data, using population genetic and phylogenetic analyses. The studied Dictyocaulus taxa display considerable genetic diversity. At least one cryptic species and a new parasite–host relationship are revealed by our molecular study. Population genetic analyses for Dictyocaulus eckerti revealed high gene flow amongst weakly structured spatial populations that utilise the three host deer species considered here. Our results suggest that D. eckerti is a widespread generalist parasite in ungulates, with a diverse genetic backround and high evolutionary potential. In contrast, evidence of cryptic genetic structure at regional geographic scales was observed for Dictyocaulus capreolus, which infects just one host species, suggesting it is a specialist within the studied area. D. capreolus displayed lower genetic diversity overall, with only moderate gene flow compared to the closely related D. eckerti. We suggest that the differing vagility and dispersal behaviour of hosts are important contributing factors to the population structure of lungworms, and possibly other nematode parasites with single-host life cycles. Our findings are of relevance for the management of lungworms in deer farms and wild deer populations.

Transmission of Helminths between Species of Ruminants in Austria Appears More Likely to Occur than Generally Assumed

“…T. axei seems to be a real generalist as has been shown by transmission experiments (see above), and this is corroborated by its genetic population structure with high diversity and high gene flow between sympatric hosts ( 49 ). In lungworms of the genus Dictyocaulus from wild ungulates from Hungary different gene flow rates suggested different host range capacities in the three species Dictyocaulus eckerti, Dictyocaulus capreolus , and Dictyocaulus viviparus with D. eckerti being the most generalist species, while D. capreolus seems to have a cryptic genetic structure ( 50 ). As red deer was shown to harbor lungworms, which were genetically distinct from the other Dictyocaulus species, a new name, Dictyocaulus cervi , was proposed recently ( 51 ).…”

The population genetics of parasitic nematodes of wild animals

“…and Dama spp.). Analysis of mitochondrial sequence data found weak genetic structuring in D. eckerti [ 86 ], while D. capreolus (specific to roe deer, Capreolus capreolus ), had comparatively lower genetic diversity and more strongly genetically structured populations when sampled sympatrically [ 86 ]. Dictyocaulus capreolus is susceptible to population bottlenecks if roe deer numbers fall, whereas D. eckerti can weather a crash in the population of any one host species by persisting in other host species, and thereby maintain a high census size (N, see Table 1 ).…”

“…Nematode species that use more than one host species often have less structured populations than the movement of any one host species would predict. This has been observed in Trichinella spp., which shows gene flow at the continental scale [ 38 ], in Dictyocaulus eckerti , a generalist parasite of deer [ 86 ], and in Neoheligmonella granjoni [ 72 , 73 ]. The use of multiple mobile host species allows nematodes to traverse or colonise a wider range of habitats than would be possible using only a single host, and this tends to promote parasite gene flow.…”

Sequence analyses of mitochondrial gene may support the existence of cryptic species withinAscaridia galli

“…Furthermore, mtDNA is a useful and reliable marker for the identification of cryptic nematode species (Blouin, 2002). A recent study showed that mt cox 1 sequences can provide a rich source of genetic markers to assess the genetic diversity and cryptic species of Dictyocaulus lungworms (Ács et al ., 2016). Trichuris infecting primates represents a complex of cryptic species, with some species being able to infect both humans and non-human primates based on mt genome datasets (Hawash et al ., 2015).…”