Detection, not mortality, constrains the evolution of virulence

Abstract

Why would a pathogen evolve to kill its hosts when killing a host ends a pathogen’s own opportunity for transmission? A vast body of scientific literature has attempted to answer this question using “trade-off theory,” which posits that host mortality persists due to its cost being balanced by benefits of other traits that correlate with host mortality. The most commonly invoked trade-off is the mortality-transmission trade-off, where increasingly harmful pathogens are assumed to transmit at higher rates from hosts while the hosts are alive, but the pathogens truncate their infectious period by killing their hosts. Here I show that costs of mortality are too small to plausibly constrain the evolution of disease severity except in systems where survival is rare. I alternatively propose that disease severity can be much more readily constrained by a cost of behavioral change due to the detection of infection, whereby increasingly harmful pathogens have increasing likelihood of detection and behavioral change following detection, thereby limiting opportunities for transmission. Using a mathematical model, I show the conditions under which detection can limit disease severity. Ultimately, this argument may explain why empirical support for trade-off theory has been limited and mixed.

High virulence is associated with pathogen spreadability in a songbird–bacterial system

“…Reduced feeding efficiency has also been documented in free-living house finches with conjunctivitis relative to clinically healthy birds [44], though here we only detected significantly lower peck rates at food for index birds infected with the high-virulence, but not low-virulence, strain relative to uninfected controls. While past work in this system has not directly examined whether strain virulence is associated with higher degrees of behavioural morbidity, our results and the few other systems where virulence and behavioural changes have been explicitly studied [10] are consistent with the possibility that high-virulence strains result in more extreme behavioural morbidity. If pecks at food are important opportunities for contact with feeder surfaces and resulting MG deposition, the lower food peck rates in the high-virulence treatment relative to controls should reduce rather than augment powder spread.…”

“…Whether the high estimated infectiousness of symptomatic humans in this study was a result of higher pathogen loads in symptomatic versus asymptomatic hosts, or aspects of spreadability such as coughing or sneezing that facilitated spread of a given amount of influenza from symptomatic hosts, was not determined. However, such studies suggest that even when aspects of virulence such as tissue inflammation and behavioural morbidity have some opposing effects on spreadability as appears the case in house finches, intermediate to high levels of virulence can still be favoured if the spreadability benefits of tissue inflammation to pathogens outweigh the transmission costs associated with behavioural morbidity [10].…”

“…Under this framework, higher virulence can be favoured whenever the benefits to pathogens from high within-host exploitation (for example, by augmenting the amount of within-host pathogen available to transmit) outweigh the associated fitness costs of virulence for pathogens (i.e. fewer opportunities for transmission due to morbidity [10] and mortality [11], or other trade-offs [12]). Thus, a common but not universal assumption of this framework is that transmission benefits to virulence for pathogens are largely load-dependent (e.g.…”

Which ‘imperfect vaccines’ encourage the evolution of higher virulence?

“…When the case mortality from the infection is very low, say 0.001—as is approximately true for countless human respiratory and gastro-intestinal infections [at least in well-nourished populations, [ 4 ]]—we can offer a plausibility argument that mortality is not limiting higher transmission [e.g. [ 32 ]]. With a case mortality rate of 0.001, even a 10-fold increase in death rate would not be enough to offset the most modest increases in transmission rate, in which case a higher transmission rate should evolve.…”