The role of the ratio of vector and host densities in the evolution of transmission modes in vector-borne diseases. The example of sylvatic Trypanosoma cruzi

Abstract

Pathogens may use different routes of transmission to maximize their spread among host populations. Theoretical and empirical work conducted on directly-transmitted diseases suggest that horizontal (i.e., through host contacts) and vertical (i.e., from mother to offspring) transmission modes trade off, on the ground that highly virulent pathogens, which produce larger parasite loads, are more efficiently transmitted horizontally, and that less virulent pathogens, which impair host fitness less significantly, are better transmitted vertically. Other factors than virulence such as host density could also select for different transmission modes, but they have barely been studied. In vector-borne diseases, pathogen transmission rate is strongly affected by host-vector relative densities and by processes of saturation in contacts between hosts and vectors. The parasite Trypanosoma cruzi which is transmitted by triatomine bugs to several vertebrate hosts is responsible for Chagas' disease in Latin America. It is also widespread in sylvatic cycles in the southeastern U.S. in which it typically induces no mortality costs to its customary hosts. Besides classical transmission via vector bites, alternative ways to generate infections in hosts such as vertical and oral transmission (via the consumption of vectors by hosts) have been reported in these cycles. The two major T. cruzi strains occurring in the U.S. seem to exhibit differential efficiencies at vertical and classical horizontal transmissions. We investigated whether the vector-host ratio affects the outcome of the competition between the two parasite strains using an epidemiological two-strain model considering all possible transmission routes for sylvatic T. cruzi. We were able to show that the vector-host ratio influences the evolution of transmission modes providing that oral transmission is included in the model as a possible transmission mode, that oral and classical transmissions saturate at different vector-host ratios and that the vector-host ratio is between the two saturation thresholds. Even if data on parasite strategies and demography of hosts and vectors in the field are crucially lacking to test to what extent the conditions needed for the vector-host ratio to influence evolution of transmission modes are plausible, our results open new perspectives for understanding the specialization of the two major T. cruzi strains occurring in the U.S. Our work also provides an original theoretical framework to investigate the evolution of alternative transmission modes in vector-borne diseases.

Graphical analysis of evolutionary trade-off in sylvatic Trypanosoma cruzi transmission modes

“…The importance of contact process saturation (also suggested by [10]) in this weighting was seen in [20], where the contact process (leading to either stercorarian or oral transmission) whose saturation threshold was closer to the actual vector-host ratio was advantaged. The results of the present study highlight the difference in nature of the trade-off between horizontal host-vector transmission modes and vertical transmission in hosts, which bypasses vectors altogether.…”

“…Sylvatic T. cruzi transmission of two strains within a single host-vector cycle can be modeled by a nonlinear dynamical system with differential equations tracking the numbers of hosts and vectors infected with each strain, as well as total population densities [15,20]. Since hosts' immune responses preclude coinfection, the model predicts competitive exclusion, with outcomes measured by reproductive numbers.…”

“…, and b = p max ≤ 1, leaving implicit for now the dependence upon Q, which was studied in [20]. Note that a compares the strengths of the two contact-based transmission routes, both functions of Q, while b measures the maximum "efficiency" of vertical transmission (under the implicit assumption that the descendants of a given subset of the host population comprise the same proportion of the population as their forebears).…”

“…Sylvatic transmission of T. cruzi has been modelled successfully using classical nonlinear dynamical systems [5,6,7,12,13,14,15,20] to study the roles played in infection dynamics by issues such as contact process saturation, the aforementioned multiple host infection routes, crossimmunity, vector dispersal and migration, and vector-host population dynamics. A deterministic model of interstrain competition predicts classical competitive exclusion based on the pathogen's reproductive numbers [15,20], from which a fitness measure can be derived, paralleling the notion of invasion fitness (e.g., [9]).…”

“…A deterministic model of interstrain competition predicts classical competitive exclusion based on the pathogen's reproductive numbers [15,20], from which a fitness measure can be derived, paralleling the notion of invasion fitness (e.g., [9]). One study identified conditions under which the vector-host density ratio can affect the outcome of the competition between two T. cruzi strains [20]; another used an adaptive trade-off framework to estimate trade-off strength and degrees of adaptation to stercorarian, vertical, and oral transmissibility in sylvatic cycles [15] for types I and IV. These estimates suggest that T. cruzi IV must be well adapted to both oral and vertical transmissibility, enough to dominate in raccoons even when the rates of both types of potential infection event are low, and in woodrats when these rates are higher (but still consistent with field and lab observations).…”