Genital Tract Screening Finds Widespread Infection With Mustelid Gammaherpesvirus 1 in the European Badger (Meles Meles)

Abstract

: Sexually transmitted diseases (STDs) can be important drivers of population dynamics because of their negative effects on reproduction. However, screening for STDs, especially in wildlife populations, is widely neglected. Using the promiscuous, polygynandrous European badger ( Meles meles) as a model, we investigated the presence and prevalence of herpesviruses (HVs) in a wild, high-density population and assessed potential differences in somatic fitness and female reproductive condition between infected and uninfected individuals. We collected n=98 genital swabs from 71 females (51 adults and 20 cubs) and 27 males (26 adults and 1 cub) during spring and summer 2015. Using a PCR specific for a mustelid α-HV, all genital-swab samples tested negative. In a panherpes PCR, a γ-HV was found in 55% (54/98; 39 adults and 15 cubs), identified as mustelid gammaherpesvirus 1 (MusGHV-1) using DNA sequencing. This contrasts with the results of a previous study, which reported MusGHV-1 in 98% (354/361) of blood samples taken from 218 badgers in the same population using PCR. The detection of MusHV-1 in the female reproductive tract strongly indicates the potential for a horizontal and, likely also a vertical, route of transmission. Our results suggest a potential linkage of genital HVs and impaired future reproductive success in females, but because reproductive failure can have many reasons in badgers, the causative link of this negative relationship remains to be investigated.

Effects of Mustelid gammaherpesvirus 1 (MusGHV-1) Reactivation in European Badger (Meles meles) Genital Tracts on Reproductive Fitness

“…Genital MusGHV-1 reactivation rates in our Irish dataset are comparable to those previously reported in an English badger population [47]. Nevertheless, the overall badger MusGHV-1 reactivation rates of 61.8% found in this study and of 50.6% (excluding cubs) in Kent et al [47] at a near 100% prevalence in blood [49] are higher than gammaherpesvirus reactivation rates reported in other species: human EBV (22-90% seropositive rate) has been reported with viral DNA isolation from 8-28% from cervical fluids and semen samples [54]; horse EHV-5 DNA has been found in 14.7% of uterine flushing samples and 2.6% of genital swabs; horse EHV-2 (79.7% seroprevalence [55]): 1.6% from uterine flushing; 2.3% from genital swabs [25,56]; reindeer CvHV-2 DNA has been found in 24% of vaginal swabs (unspecified seroprevalence) [20]; cattle BHV-4 (96.9% seroprevalence) DNA in 48.5% of uterine swabs and 51.5% of vaginal swabs [57]. The exceptionally high prevalence of MusGHV-1 DNA in badger genital tracts further strengthens that sexual transmission may be an important route in gammaherpesvirus transmission comparable to human KSHV [58] and murine MHV-4 [13].…”

“…Overall, we found no difference in the body weights of genital MusGHV-1 positive and negative individuals suggesting that MusGHV-1 reactivation does not affect-nor was triggered by-host body condition, mirroring results from in England [47]. We did, however, identify a nonsignificant trend in pregnant females, where genital MusGHV-1 positive individuals had lighter body weights than those that tested negative (Figure 1), indicating that during pregnancy, reactivation may lead to decreased body condition [61], or-conversely-that reduced body condition during pregnancy may promote MusGHV-1 reactivation [62].…”

“…This corroborates other studies on gammaherpesvirus transmission (e.g., MHV-4 transmission in mice [13]; EBV in humans [82]), but contradicts a study of BHV-4 transmission in cattle, where intrauterine infection was found in 4/7 stillbirth foetuses [76]. Nevertheless, primary infection in foetuses may likely happen during parturition, or through close postnatal contact with the mother, explaining results from a previous study that found 75% 3-month old prepubescent cubs presenting positive for genital MusGHV-1 [47].…”

“…Confirming sexual transmission in a free-ranging population without using manipulative experiments is extremely challenging, but indirect evidence permits inference of horizontal and/or vertical transmission, for example, by isolating the pathogen DNA using PCR from swabs of genital tracts, placenta tissues, or foetal tissues. A population-wide screening survey revealed a reactivation rate of 55% in genital tract mucosae of badgers in a high density population in the UK [47], indicating a high likelihood of sexual transmission. This same study also linked reactivation of genital MusGHV-1 to reduced future reproductive success in female badgers [47], but did not investigate the factors contributing to herpesvirus reactivation.…”

“…A population-wide screening survey revealed a reactivation rate of 55% in genital tract mucosae of badgers in a high density population in the UK [47], indicating a high likelihood of sexual transmission. This same study also linked reactivation of genital MusGHV-1 to reduced future reproductive success in female badgers [47], but did not investigate the factors contributing to herpesvirus reactivation. Here, we use badger samples collected post-mortem from across the Republic of Ireland under a national culling programme for the management of bovine tuberculosis to investigate:…”