Competition, virulence, host body mass and the diversification of macro-parasites

Abstract

Adaptive speciation has been much debated in recent years, with a strong emphasis on how competition can lead to the diversification of ecological and sexual traits. Surprisingly, little attention has been paid to this evolutionary process to explain intrahost diversification of parasites. We expanded the theory of competitive speciation to look at the effect of key features of the parasite lifestyle, namely fragmentation, aggregation and virulence, on the conditions and rate of sympatric speciation under the standard 'pleiotropic scenario'. The conditions for competitive speciation were found similar to those for non-parasite species, but not the rate of diversification. Adaptive evolution proceeds faster in highly fragmented parasite populations and for weakly aggregated and virulent parasites. Combining these theoretical results with standard empirical allometric relationships, we showed that parasite diversification can be faster in host species of intermediate body mass. The increase in parasite load with body mass, indeed, fuels evolution by increasing mutants production, but because of the deleterious effect of virulence, it simultaneously weakens selection for resource specialization. Those two antagonistic effects lead to optimal parasite burden and host body mass for diversification. Data on the diversity of fishes' gills parasites were found consistent with the existence of such optimum.

Fundamental Factors Determining the Nature of Parasite Aggregation in Hosts

“…Aggregation of parasites amongst hosts is one of the rare phenomena in biology that has been described as a ‘law’ [ 1 , 5 ]. The negative binomial distribution has been of central importance to establish evidence for aggregation in data [ 5 , 42 ], as well as to provide theoretical predictions on ecological and evolutionary consequences of parasite distributions among hosts [ 6 , 9 , 43 ]. However, a good fit to a negative binomial distribution does not provide any information about the causes of aggregation since a number of different biological phenomena have been proposed to generate this flexible distribution [ 44 ], as well as different combinations of statistical laws [ 13 ].…”

“…Aggregation has been shown to affect parasite ecology by stabilizing host-parasite population dynamics [ 6 , 7 ] and facilitating interspecific co-infection as a result of increased host susceptibility [ 8 ]. Aggregation also influences parasite evolution by, e.g., increasing the level of intra-specific competitive interaction and the rate of within-host adaptive parasite diversification [ 9 ]. Accordingly, aggregation of parasites amongst hosts affects the transmission of infectious human diseases [ 10 ].…”

Aggregation of Infective Stages of Parasites as an Adaptation and Its Implications for the Study of Parasite-Host Interactions

“…The stability of parasite-host interactions is thought to be dependent on the degree of parasite aggregation (Anderson and May 1978;Anderson and Gordon 1982). Parasite aggregation among hosts can also either increase (Cornell et al 2003) or decrease (Rascalou and Gourbière 2014) the rate of parasite adaptive evolution. Taken collectively, aggregation of infective stages of parasites in the environment might have an obvious cause and an important consequence that helps explain other phenomenon well described in parasitehost study systems.…”

Modelling the Effects of Mass Drug Administration on the Molecular Epidemiology of Schistosomes

“…Models on plant parasites, for instance, have indicated that evolutionary divergence of parasite phenotypes can be driven by seasonal transmission and associated fitness trade-offs (Hamelin et al, 2011), such as may also occur with annual treatments and reduced density-dependent factors. One such recent model describes how competition explains intra-host diversification of parasites (Rascalou and Gourbiere, 2014). They show that parasite adaptive evolution is faster in highly fragments parasites populations and for weakly aggregated and virulent parasites, all factors which could be affected by drug selective pressures, hybridizations and associated trade-offs.…”