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Parasitism is an extremely common strategy in nature and has evolved separately at least fifty times (Poulin, 1998, Palm and Klimpel, 2007). Recent studies have shown that parasitic species make up a far greater proportion of life on Earth than had previously been presumed, some 40% of known species are parasitic at some stage in their lives and up to 75% of all food web interactions involve at least one species of parasite (Dobson et al., 2008), moreover parasites have been demonstrated to make up a larger biomass in studied ecosystems than the top predator species, having a biomass on par with that of birds or fish (Kuris et al., 2008). These studies have made it clear that parasites are of huge ecological importance and that serious consideration must be given to the role that parasitic species play in the abundance, fecundity and evolutionary development of their host species (Lafferty, 1999). These findings have also made it clear that parasitism is and long has been a highly effective survival strategy and have shown that it is relatively common for free living organisms to possess the morphological characters to permit a change to parasitism (Rothschild and Clay, 1952, Conway Morris, 1981).
A major boundary potentially parasitic organisms need to overcome is one of transmission (Smith-Trail, 1980). Being able to survive and thrive in another organism is all well and good, but without the means to reliably acquire new hosts, any advantage to being parasitic could rapidly be offset by limited transmission; for this reason many parasite species will infect a host only when one becomes available due to a stochastic event, and will complete their life cycle unimpeded by the lack of a host should one not be available. An obvious example of this would be many parasitic protist species, such as Acanthamoeba castellani (Stapleton et al., 2009).
Different parasite species employ vastly different tactics in order to acquire and infect new host organisms, one of the more common, and hence more successful, strategies is trophic transmission (Kuris et al., 2008), or transmission via ingestion by the host of a parasite propagule along with the hosts' normal diet. An example of this strategy is Teladorsagia circumcincta, a parasitic nematode which infects its host, the domestic sheep Ovis aries, by attaching itself to blades of grass and being ingested by the host as it grazes (O'Connor et al., 2006).
T. Circumcincta is an example of a parasite which employs direct transmission, reproducing in its host and passing eggs into the environment, to hatch into larvae and subsequently be ingested by a new host; this is considered a simple life cycle (SLC). However many species of parasites have evolved to exploit a series of different hosts in their life cycle, typically moving up a trophic level with each change of host, such parasites are considered to have complex life cycles, with each individual potentially infecting up to four hosts in its life (Matsuno and Ono, 1996, Parker et al., 2003a, Briand and Cohen, 1987).
In recent years there has been a rise in interest in the life cycles of parasite species, with much work focusing on the costs and benefits as well as life history optimisation of model parasite species; such studies have huge potential to benefit a number of industries and fields; medicine, agriculture and ecology to name just a few (Gandon, 2004), but in order to fully appreciate a parasites life cycle it is important to understand how and why it evolved, however the issue of how parasite life cycles evolved has received far less attention than it deserves (Choisy et al., 2003, Parker et al., 2003a, Hammerschmidt et al., 2009). The aim of this paper is to serve as a critical review of our current understanding of the evolution of complex parasite life cycles (CLC's), using tropically transmitted helminth parasites as an example of how and under which conditions such life cycles evolve. The majority of this paper will focus upon recently published work in the area of CLC evolution, to review the most current theories and the evidence supporting them. It is however important to keep in mind that parasitism is, as has been mentioned, very common in nature and as such parasitism as a life strategy has in all probability been arrived at through different means in different species, and so the theories presented here are not necessarily mutually exclusive.
1. Complex Life Cycles
Before going into too great an amount of detail regarding the theories of CLC evolution, it seems prudent to give some perspective by looking at a typical example of a helminth species CLC. You will see from figure 1 that development does not occur in the final, definitive host but only in the environment and earlier hosts. No development takes place in a paratenic host, but its inclusion in the life cycle can still be advantageous to the parasite, e.g. as a means of dispersal (Parker et al., 2009).
Figure 1. Diagram of a complex life cycle typical of helminth parasite species, in bold is the developmental stage of the parasite.
An example of a trophically transmitted helminth species in which the life cycle fits the above diagram is the cestode Schistocephalus solidus; in this species eggs hatch in the environment and the resulting larvae infect the first host, a copepod. The larvae develop here until the copepod is ingested by the next host, the three-spined stickleback where further development takes place until the stickleback is eaten by a piscivourous avian predator and the parasite can begin producing eggs, which pass out of the host in its faeces (Michaud et al., 2006, Hammerschmidt et al., 2009)
2. The Addition of Hosts
2i. Upward Incorporation
The classic theory of CLC evolution involves the upward incorporation of host species, which predate upon the earlier hosts of a parasite. In this example a pre existing SLC parasite evolves to survive the process of its host's ingestion by a predator by subsequently parasitizing that predator (Brown et al., 2001, Smith-Trail, 1980); in this example the higher trophic predator becomes the definitive host, and the former host becomes the intermediate. A diagrammatic representation of this is shown in Fig. 2; a third host would be added in the same manner.
Figure. 2. Proposed evolutionarily ancestral life cycles of a complex life cycle developed by upward incorporation of a host, a. shows the original single host life cycle, b. a theoretical cycle where the parasite can complete its life cycle in either its original host, or that hosts predator, and c. a typical life cycle seen in extant helminth parasites, where the parasite no longer reproduces in the first host. (adapted from Parker et al. 2003a).
There are varying theories as to why this may have occurred, the most popular of which is the idea that in situations where a host is predated frequently enough to apply sufficient selection pressure upon a parasite, a significant increase in fitness can be gained by surviving the process of the hosts demise, with the simplest escape route for the parasite, considering its adaptation or even dependence upon parasitism, being a movement into the predator rather than the environment (Smith-Trail, 1980, Poulin, 1998, Lafferty, 1999). This idea is further supported by Lafferty's (1999) observation that any organism achieving this would not only survive where it otherwise would not, but also “trade up” into a host which is both larger and longer lived, both characteristics which would increase the success of the parasite (Parker et al., 2003b).
However in 2001, Brown et al. proposed a compelling alternate hypothesis to explain the evolution of upward incorporation of host species; their theory is based upon the fact that higher trophic level predator species act as concentrators of those parasites which employ their prey as intermediate hosts, thus providing the parasites an inexpensive and naturally occurring means of increasing their own genetic variability. This theory is supported by the fact that it has been demonstrated that parasites will preferentially reproduce sexually rather than asexually where the option is available (Trouve et al., 1999).
Physical evidence supporting upward incorporation as a process has been provided by phylogenetic analyses which imply that the acanthocephalans first parasitized arthropod species, and later adopted vertebrate hosts when predation upon those arthropods became common enough for such adaptation to become advantageous (Herlyn et al., 2003). Choisy et al. (2003) and Parker et al. (2003a) have provided this theory further support by demonstrating that it is theoretically viable, through the use of computer modelling.
2ii. Downward Incorporation:
A proposed alternate method of host addition is downward incorporation. In downward incorporation the first host parasitized in the ancestral SLC remains the definitive host after the addition of subsequent hosts (Choisy et al., 2003), see Fig.3. It is theorised that the addition of a hosts prey as an intermediate or paratenic host can occur where that species regularly ingests the parasites eggs in the environment, and where the cost of adapting to that prey species' physiology is low (Poulin, 2007).
Figure. 3. Theorised evolutionary progression of life-cycles leading to the development of complex life-cycles by downward incorporation of host species, a. represents the original, single host cycle. b. a theorised intermediate stage between a. and c., an existing complex life cycle (adapted from Poulin, 2007)
There is a compelling body of phylogenetic evidence to support the idea of downward incorporation. CLC's appear to have evolved through this process several times within different groups of the Nematoda, which are believed to have first been parasites of vertebrates, and to have later added invertebrate intermediate hosts, possibly to enhance rates of transmission to their definitive hosts (Blaxter et al., 1998).
Parasitic Platyhelminthes are also believed to have acquired CLC's through downward incorporation (Littlewood et al., 1999, Gibson and Bray, 1994), with the Cestoda adding arthropod intermediate hosts (Olson et al., 2001), while the Digenea added mollusc intermediate hosts to their existing parasitic SLC's (Cribb et al., 2003, Rauch et al., 2005). As with upward incorporation, downward incorporation has been demonstrated to be viable through the use of computer modelling (Choisy et al., 2003, Parker et al., 2003a).
2iii. Lateral Incorporation:
A third and final means of incorporation of hosts by parasite species is lateral incorporation, or the incorporation of hosts of the same trophic level as an existing host (Parker et al., 2003a). This is believed to occur in instances where the fitness gained by a mutant invading a new host can more than offset the costs of becoming more generalist; this would probably occur in instances where the new host is physiologically very similar to the established one, and a fitness advantage can be had by, for example, a lower rate of competition with conspecifics (Palm and Klimpel, 2007).
3. Why Add Hosts?
While the previous section explains the mechanisms by which CLC's may evolve, it is important to look at the specific advantages gained through host addition; for however viable it may be to exist with a sequence of host species some significant fitness advantage must be gained by any mutant venturing into a new host in order for it to become the norm for that parasite, after all, a huge number of parasites thrive despite employing SLC's. This section explores the current theories relating to the benefits gained from specific host types, with the aim of gaining an appreciation for their benefit to a parasite species.
3i. Intermediate Hosts:
The major theory relating to what a parasite gains from the an intermediate host is that the host serves as an efficient means of inoculating the definitive host and gaining the associated fitness advantages (see section 2i), this alone however does not explain the cessation of reproduction in an intermediate host. We know from figures 1 and 2 that it is likely that at some point during the evolution of CLC's that reproduction will have taken place in both the definitive host and the species which would later become the intermediate host, meaning that the absence of reproduction is an acquired trait and so must benefit the parasite.
Unlike parasitoids, which are distinct from parasites in that they aim to completely consume the host, leading to its demise (Godfray, 1994), parasites require that their host remain functional in order to complete their life cycle; this is especially true of intermediate hosts as the host must remain active in order to encounter its predators, the parasites definitive host. This means that it is unlikely that intermediate hosts would benefit the parasite by serving as a food source, as this would enfeeble the host, with an end result more akin to parasitoid infections (Parker et al., 2003a).
Parker et al. (2003b) suggest that growth to maturity and subsequent reproduction while in an intermediate host would result in increased parasite mortality, due to a greater immune response being evoked. This would imply that it would be to the parasites advantage to limit its growth when occupying an intermediate host, and this is in fact well known to be the case, and is seen in the form of growth arrest of a parasite as a result of its reaching a certain size, or as a result of environmental cues (Viney, 2002, Parker et al., 2009, Ball et al., 2008). Growth arrest simply halts the development of the parasite at a particular size, and allows the parasite to remain in the host while also applying very little stress until such a time as the parasite can move to its definitive host and become sexually mature (Parker et al., 2009, Iwasa and Wada, 2006).
3ii. Paratenic Hosts:
While little or no feeding takes place in an intermediate host, it is generally agreed that parasite development does take place. Whereas a paratenic host is defined by the lack of parasite development while in the host (Poulin, 2007, Bush et al., 2001).
Paratenic hosts have long been believed to serve solely as transmission vectors between other host species separated by a gap in trophic level, sometimes being described as ‘ecological bridges' (Marcogliese, 2001); however intermediate hosts provide this same benefit and so this alone does not explain the necessity for paratenic hosts (Parker et al., 2009). The lack of development in paratenic hosts is most likely due to the specific situations in which such hosts are used, the specific details of which are beyond the scope of this review, but have been explained in detail by Ball et al. (2008).
Another theorised benefit of paratenic hosts is their role in allowing parasites to disperse within and between environments, known as phoresy (Morand et al., 1995). However while this may be the case in some situations, it is unlikely to be the sole purpose of paratenic hosts, as many are used in aquatic systems where transportation is more easily facilitated by water currents (Herlyn et al., 2003).
3iii. Bothriocephalus; an example
An example of benefits gained with addition of a paratenic host include if there is space!
4. The Challenges Parasites Overcome
This section will look at the specific challenges parasites must overcome when switching hosts, it is important to appreciate this as it explains what costs are met by a parasite when changing host, which similarly indicates the importance of making that change; for example the significant cost of moving between taxa (and the environment), or of being a generalist. Logic dictates that any gains from parasitism must outweigh these costs. We will consider varying host immunity and environmental conditions, as well as the necessity for careful timing of host change.
4i. Host Physiology:
A key factor in the addition of hosts is, of course, the cost of adapting to that hosts physiology. This is likely to vary depending how different the physiologies (particularly the immunologies) of the two hosts are; therefore it can be assumed that the cost of switching hosts increases in correlation with the degree in which the hosts differ physiologically. If we again consider the cestode S. Solidus (mentioned in section 1), the costs it incurs for switching from the environment, into an arthropod then a fish and finally a bird must be substantial. The most profound example of this is parasite adaptation to deal with host immune systems.
4ii. Host Immune Response:
Perhaps the biggest hurdle for a parasite to overcome is the host species immune response to their presence, the importance of host immunity to a parasite being comparable to the pressures which predators impose upon wild populations (Bize et al., 2008).
Surviving in spite of host immunity is challenge enough, but a parasite which utilises multiple host species must survive in the presence of quite different immune systems, and needs to optimise its response to whichever host it finds itself in. For example switching from an arthropod host to a vertebrate would involve considerable physiological adaptation, as vertebrates possess active immunity whereas arthropods do not. Similarly the cost of surviving in a vertebrate host is therefore likely to be considerable and so the benefits must too be considerable (Poulin, 2007, Thomas et al., 2009).
4iii. Timing of Host Change:
The seasonal timing of host change is often optimised to enhance the likelihood of transmission, with parasites striving to have their infective stages available to potential hosts at times when those hosts are most susceptible to infection (Tinsley, 1999). For parasite species where the timing of their movement into a new host is crucial to their success, there is an inherent risk of failure, with potentially fatal results should they not time the move precisely (Hammerschmidt et al., 2009). Some species overcome this problem by removing the need for precise timing, for example many species of nematode produce extremely durable eggs, able to survive desiccation and extremes of temperature and so be present in their hosts environment for a greater amount of time (Perry, 1999).
Given the wealth of evidence to support the ideas of host addition by both upward and downward incorporation, and the lack of opposing theories, it is fair to conclude that both are likely to have played a major role in CLC evolution in helminth parasites. Which of the two processes are used by a parasite appears to be an issue of the specifics of the SLC used by that parasite species' ancestors. In situations where an SLC parasite utilises a definitive host which is a top predator in its food web the opportunity exists to improve fitness through downward incorporation, whereas a host species which occupies a lower trophic level does not present its parasites the same opportunity.
A more debatable issue is the reason why a parasite benefits from adding additional hosts to its life cycle. Smith-trail's (1980) original theory that additional hosts are added simply to prevent a parasites' demise as a result of predation on its host is a compelling one, and is given much strength by the input of those parasitologists who have followed him, such as Lafferty (1999) who points out a range of very plausible benefits which improve the long-term fitness of those mutants able to achieve it, such as a larger and longer lived host. However these theories are largely theoretical and lack any compelling and specific evidence.
The alternative hypothesis proposed by Brown et al. (2001) that host addition benefits parasites by bringing conspecifics together in a single host, and thus facilitating sexual reproduction is well supported by established fact as well as their own optimality models, however this theory does have limitations and can only be applied to some species as not all reproduce sexually.
In both of these theories there are very clear benefits to be gained by a parasite adding hosts, and in either case these benefits may be enough to facilitate host addition. There is however no clear reason why these theories should be mutually exclusive, and in reality where ever it is possible parasites are undoubtedly enjoying all of the benefits theorised above, which makes singling out any one benefit as the driving factor behind host addition impossible without living examples which exclude the others, and no such examples have yet been presented.
Where parasite species using downward incorporation are concerned, the ancestral SLC would already involve a definitive host which confers the advantages that have just been mentioned, and so in this case some other benefit must be gained by host addition. The benefits of intermediate and paratenic hosts (discussed in sections 3i and 3ii respectively) suggest that parasites use these hosts either as a means of transportation or as a method of improving the chances of inoculating a definitive host. While phoresy may be important in some species, in many it is completely unnecessary; this leaves the idea of improved transmission as both the most logical and best supported by the literature. Therefore it is probable that the major benefit gained from downward incorporation is a greater success rate in reaching a definitive host; however it is worth noting that any species adding hosts through upward incorporation would also gain these benefits.
Lateral incorporation has less obvious immediate benefits; however it is important to remember that food-webs can be very complex, and that the simplified life cycle diagrams we often see do not demonstrate the range of interactions which occur between species in nature (McFarland et al., 2003), it is therefore very possible that examples of lateral incorporation could simply be parasites taking ‘detours' enroute to their definitive host (Latham et al., 2003).
The key to the understanding of multi-host parasite lifecycles is the differing physiologies of the hosts involved; only when this is considered do the costs and benefits of host addition begin to make sense. Similarly host physiology could help to explain some of the less obvious questions in this topic, for example why a parasite may in some situations have a paratenic host rather than an intermediate one, the answer to which may lie in the degree to which all of the parasites hosts differ; a move into a very different host may require significant change in the parasites own physiology in order to cope with the new hosts immune system for example, and this change in the parasite may well manifest as a change in its developmental stage, making that new host an intermediate one. Whereas movement into a new, but physiologically similar host may not require such adaptation and so no development may occur, making that new host paratenic. This if true would be an example of parasites utilising existing characteristics to facilitate their lives as parasites.
A recurring problem in the study of CLC evolution is the lack of real life examples to demonstrate theories, with the majority of recent study being based upon computer models, for example the work of Parker et al. (2003a) and Choisey et al. (2003). While computer modelling can be a very powerful tool, the results of simulations are far more compelling when they can be related directly to what is seen in nature. This would be the most profitable area for continued research to focus upon, with the vast diversity of parasite fauna in the world some excellent examples of different CLC strategies are doubtless just waiting to be discovered and reported.