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.