Introduction
Pathogens, particularly those causing emerging diseases, can be a major
driver of mortality in wildlife (McCallum, 2008; Fereidouni et al.,
2019; Fisher and Garner, 2020), which can be aggravated by changing
environments and climate change (Dwyer et al., 2020; Paniw et al.,
2022). Cross-sectional studies are often employed to study patterns of
pathogen prevalence and transmission, yet their power to assess
long-term patterns of pathogen emergence, dynamics and overall pathogen
prevalence are limited (Reis et al., 2021). The advantage of
longitudinal surveillance studies rest in their ability to identify
factors underpinning pathogen transmission, assess the impact of
pathogens on individual hosts and populations, and track host-pathogen
dynamics (Ryser-Degiorgis, 2013; Walton et al., 2016; Watsa and Wildlife
Disease Surveillance Focus Group, 2020). Since long-term projects are
difficult to sustain and pathogen monitoring and detection can be
challenging (reviewed in Thomas et al., 2021), such long-term datasets
populations are still exceptional in natural (Patterson et al., 2017;
McDonald et al., 2018).
Pathogens of the Mycobacterium tuberculosis complex (MTC), the
causative agents of the disease tuberculosis (TB), are among the most
significant emerging pathogens globally (CSFPH, 2019). Generally,
Mycobacterium infections are chronic, progressive and characterized by
prolonged latent (i.e. non-infectious) or subclinical (i.e. without
clinical signs but potentially still infectious to others) periods
(Houben and Dodd, 2016; CSFPH, 2019; Dwyer et al., 2020; Jolma et al.,
2021). If the disease progresses to the development of overt clinical
signs, their onset is usually followed by health decline and death
(Alexander et al., 2010; Fairbanks et al., 2015). A wide variety of
mammals can be infected with MTC bacteria ( CSFPH, 2019; Reis et al.,
2021), which can easily be transmitted between multiple hosts species,
with implications for entire ecosystems (Michel et al., 2006; Hardstaff
et al., 2014). Thus, a well-founded understanding of transmission and
host-pathogen dynamics is imperative for the development of adequate TB
surveillance and management strategies (de Lisle et al., 2002). However,
despite intense research efforts in several TB host systems (reviewed in
Reis et al., 2021), quantitative data TB exposure, prevalence and
progression are still rare for many wildlife species affected by TB.
Meerkats (Suricata suricatta ) are highly social, cooperatively
breeding small carnivores (Clutton-Brock and Manser, 2016) native to
southern Africa, a hotspot region for TB in wildlife (Michel et al.,
2006; Tanner et al., 2015). Within the Kalahari Meerkat Project (KMP;
Clutton-Brock and Manser, 2016), a natural population has been routinely
monitored since 1993. First evidence of infections withMycobacterium suricattae , previously believed to be M.
bovis , were reported in the late 1990s (Drewe, Foote et al., 2009;
Parsons et al., 2013). Meerkats have a complex social system
characterized by small to medium sized social groups (two to fifty
individuals). Reproduction is largely monopolized by dominant breeding
pairs (Clutton-Brock and Manser, 2016), which differ from subordinates
in physiology (Young et al., 2006; Smyth et al., 2018), social network
position(Drewe, 2010), and mortality risk (Cram et al., 2018). Social
interactions within and between group are frequent (Clutton-Brock and
Manser, 2016), making meerkats an excellent model to investigate
pathogen transmission in a social context (Drewe, 2010).
Meerkats are a particularly good model system to investigate TB
epidemiology because transmission, progression, and pathology ofM. suricattae infection mirrors patterns found in other wildlife
hosts: Transmission occurs mostly via aerial routes or social
interactions (Gallagher and Clifton-Hadley, 2000; Drewe, 2010; Drewe et
al., 2011). Infection are initially characterized by long latent or
subclinical periods (Drewe et al., 2011; Tomlinson et al., 2013;
McDonald et al., 2018), followed by rapid progression to terminal stages
upon onset of clinical signs (Alexander et al., 2010; Fairbanks et al.,
2015). Typical signs of TB infections, including lymphadenopathy,
particularly of submandibular, inguinal and cervical lymph nodes, and
physical deterioration 1990s (Drewe, Foote et al., 2009; Parsons et al.,
2013)., typically develop ~12 months post infection
(Donadio et al., 2022). After progression to clinical TB, meerkats
usually become terminally ill with open lesions at affected lymph nodes
and die within several months, with no recovery once clinical stage was
reached (Patterson et al., 2021). Thus, TB was reported to impact life
history and survival, and can lead to group extinctions (Duncan et al.,
2021), a pattern aggravated by climate change (Paniw et al., 2022).
Despite some detailed knowledge
gained from previous cross-sectional studies regarding TB in meerkats
(summarized in Table 1), the dynamics around its spread across the
population, and how TB disease manifests over a meerkats’ lifetime,
remain obscure (see Supplementary Table 1). To fill these gaps, we
leverage an extensive long-term dataset with over 25 years of detailed
individual data (n= 3,420 individuals) to examine TB spread across the
population. Specifically, we quantify TB exposure, prevalence of
clinical TB, and mortality, provide timelines of typical disease
progression in individuals and groups and describe inter-individual and
temporal variation in TB progression. These findings provide crucial
context by which to understand TB epidemiology and ecology.