Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds

Abstract

Recovery from infection is not always complete, and mild chronic infection may persist. Although the direct costs of such infections are apparently small, the potential for any long-term effects on Darwinian fitness is poorly understood. In a wild population of great reed warblers, we found that low-level chronic malaria infection reduced life span as well as the lifetime number and quality of offspring. These delayed fitness effects of malaria appear to be mediated by telomere degradation, a result supported by controlled infection experiments on birds in captivity. The results of this study imply that chronic infection may be causing a series of small adverse effects that accumulate and eventually impair phenotypic quality and Darwinian fitness.

Cellular aging dynamics after acute malaria infection: A 12‐month longitudinal study

“…Although telomere shortening has been shown in acute infections in experimental animal models (Asghar, Hasselquist, et al., 2015; Asghar et al., 2016; Ilmonen et al., 2008), such effect has not been reported in humans. Previous studies have shown that chronic viral infections (i.e., HCV, CMV, and HIV) accelerate cellular aging in humans, as reflected by shorter telomere length and elevated CDKN2A expression (van de Berg et al., 2010; Gianesin et al., 2016; Leung et al., 2017; Pathai et al., 2013; Robinson et al., 2013; Zannetti et al., 2006).…”

“…After repeated infections, individuals gradually acquire immunity that protects against disease but are unable to clear asymptomatic low‐level parasitemia (Doolan, Dobano, & Baird, 2009). Whether repeated malaria episodes or chronic asymptomatic infections have an even more pronounced and long‐lasting effect on cellular aging (and lifespan) in humans, as shown in birds with asymptomatic chronic malaria infection (Asghar, Hasselquist, et al., 2015), needs to be investigated. Such findings would have major implications on the need to further speed up the global efforts to eliminate malaria.…”

“…Aging may be the cause of diseases, but infectious diseases can also act as exogenous drivers of aging and the underlying mechanisms may include enhanced inflammation, pathogen‐dependent tissue destruction, or accelerated cellular aging through increased cell turnover (Asghar, Hasselquist, et al., 2015; Asghar et al., 2016; Gavazzi & Krause, 2002). Recently, we have shown that chronic asymptomatic malaria infections resulted in reduced lifespan, mediated through faster telomere shortening in birds (Asghar, Hasselquist, et al., 2015; Asghar et al., 2016). …”

“…However, the risk of any long‐term adverse effect is poorly understood. Recent studies showed that malaria infection in birds results in accelerated telomere shortening in peripheral blood and other tissues (liver, lungs, kidney, heart, spleen, and brain), and persistent chronic asymptomatic malaria infections result in reduced lifespan, implying that a seemingly mild disease accelerates cellular aging (Asghar, Hasselquist, et al., 2015; Asghar et al., 2016; Karell, Bensch, Ahola, & Asghar, 2017). Furthermore, induced Salmonella infection in mice (Ilmonen, Kotrschal, & Penn, 2008) leads to accelerated telomere shortening in blood.…”

Avian malaria: a new lease of life for an old experimental model to study the evolutionary ecology ofPlasmodium

“…Long-term monitoring of a wild population of blue tits has revealed strong associations between malaria infection on bird survival and recapture rates [45]. More recently, malaria infection has been found to accelerate the senescence of great reed warblers through telomere degradation [46]. Experimental infections, on the other hand, have consistently shown anaemia to be one of the primary virulence determinants in avian malaria infections [23,36,42].…”