Adverse ecological and social conditions during early life are known to influence development, with rippling effects that may explain variation in adult health and fitness. The adaptive function of such developmental plasticity, however, remains relatively untested in long‐lived animals, resulting in much debate over which evolutionary models are most applicable. Furthermore, despite the promise of clinical interventions that might alleviate the health consequences of early‐life adversity, research on the proximate mechanisms governing phenotypic responses to adversity have been largely limited to studies on glucocorticoids. Here, we synthesize the current state of research on developmental plasticity, discussing both ultimate and proximate mechanisms. First, we evaluate the utility of adaptive models proposed to explain developmental responses to early‐life adversity, particularly for long‐lived mammals such as humans. In doing so, we highlight how parent‐offspring conflict complicates our understanding of whether mothers or offspring benefit from these responses. Second, we discuss the role of glucocorticoids and a second physiological system—the gut microbiome—that has emerged as an additional, clinically relevant mechanism by which early‐life adversity can influence development. Finally, we suggest ways in which nonhuman primates can serve as models to study the effects of early‐life adversity, both from evolutionary and clinical perspectives.
Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations.
Despite increasing appreciation for parasitism as an important component of primate ecology and evolution, surprisingly few studies have demonstrated the costs of helminth parasitism in primates. Detecting parasite-related costs in primates is particularly difficult because it requires detailed, long-term data on individual host reproductive success, survival, and parasitism. The identification of the larval tapeworm Taenia serialis in geladas under intensive long-term study in the Ethiopian Highlands (Nguyen et al. [2015] American Journal of Primatology, 77:579-594; Schneider-Crease et al. [2013] Veterinary Parasitology 198:240-243) provides an opportunity to examine how an endemic parasite impacts host reproductive success and survival. We used survival analyses to assess the mortality risk associated with protuberant larval cysts characteristic of T. serialis using a decade of data from a gelada population in the Simien Mountains National Park (SMNP), Ethiopia. We demonstrated strikingly high mortality associated with T. serialis cysts in adult females, particularly for younger adults. The estimated effect of cysts on male mortality was similar, although the effect was not statistically significant, likely owing to the smaller sample size. Additionally, the offspring of mothers with cysts experienced increased mortality, which was driven almost entirely by maternal death. Mothers with cysts had such high mortality that they rarely completed an interbirth interval. Comparison with a study of this parasite in another gelada population on the Guassa Plateau (Nguyen et al. [2015] American Journal of Primatology, 77:579-594) revealed lower cyst prevalence in the SMNP and similar cyst-associated mortality. However, many more females with cysts completed interbirth intervals at Guassa than in the SMNP, suggesting that T. serialis cysts may kill hosts more rapidly in the SMNP. Our results point toward the underlying causes of individual and population-level heterogeneity in T. serialis-associated mortality as important areas for future research.
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