Evolution of complex life cycles in trophically transmitted helminths. I. Host incorporation and trophic ascent

Abstract

Links between parasites and food webs are evolutionarily ancient but dynamic: life history theory provides insights into helminth complex life cycle origins. Most adult helminths benefit by sexual reproduction in vertebrates, often high up food chains, but direct infection is commonly constrained by a trophic vacuum between free-living propagules and definitive hosts. Intermediate hosts fill this vacuum, facilitating transmission to definitive hosts. The central question concerns why sexual reproduction, and sometimes even larval growth, is suppressed in intermediate hosts, favouring growth arrest at larval maturity in intermediate hosts and reproductive suppression until transmission to definitive hosts? Increased longevity and higher growth in definitive hosts can generate selection for larger parasite body size and higher fecundity at sexual maturity. Life cycle length is increased by two evolutionary mechanisms, upward and downward incorporation, allowing simple (one-host) cycles to become complex (multihost). In downward incorporation, an intermediate host is added below the definitive host: models suggest that downward incorporation probably evolves only after ecological or evolutionary perturbations create a trophic vacuum. In upward incorporation, a new definitive host is added above the original definitive host, which subsequently becomes an intermediate host, again maintained by the trophic vacuum: theory suggests that this is plausible even under constant ecological/evolutionary conditions. The final cycle is similar irrespective of its origin (upward or downward). Insights about host incorporation are best gained by linking comparative phylogenetic analyses (describing evolutionary history) with evolutionary models (examining selective forces). Ascent of host trophic levels and evolution of optimal host taxa ranges are discussed.

Parasite life-cycle studies: a plea to resurrect an old parasitological tradition

“…Mathematical models have revealed that increases in life-cycle complexity that enhance the probability of transmission to the definitive host, opportunities for sexual outcrossing in that host, or lifetime fecundity should be under strong selection in many plausible situations (Brown et al, 2001;Choisy et al, 2003;Parker et al, 2003Parker et al, , 2015. Predictions from these models generally fit well with empirical observations.…”

The evolution of transmission mode

“…Prey of the original host may frequently have ingested parasite transmission stages because of their proximity to the original host and thereby may have become intermediate hosts. Being prey to the original host may enhance transmission back to that host [106]. Such downward incorporation has been associated with the occurrence of a ‘trophic vacuum’, i.e.…”

“…Platyhelminthes appear to present such an example of downward incorporation: the lineage ancestral to digeneans and cestodes has become parasitic in invertebrates [101]. Paratenic hosts may also be acquired by downward incorporation as a means of increasing transmission [106]. Intermediate hosts could also be added via ‘lateral incorporation’ if the parasite has multiple hosts involved; in a generalist pathogen each of two parasite stages come to specialize on one of the hosts [106].…”

“…Paratenic hosts may also be acquired by downward incorporation as a means of increasing transmission [106]. Intermediate hosts could also be added via ‘lateral incorporation’ if the parasite has multiple hosts involved; in a generalist pathogen each of two parasite stages come to specialize on one of the hosts [106]. …”

Patterns and processes influencing helminth parasites of Arctic coastal communities during climate change

“…In a way, the present-day conditions of parasites' transmission in the high Arctic are comparable with those in the glacial refugia. The instances of non-specific parasitism can be considered as a model demonstrating different stages of lateral incorporation (sensu Parker et al, 2015) of new hosts, which may result in speciation of helminths.…”