Introduction

One of the major differences between a parasitic and a free-living lifestyle is the requirement that a parasite must periodically pass from host to host. This transmission phase of its life cycle may involve active host-seeking stages or passive transfer via ingestion of the current host by the next one. However, many parasites dwelling in the circulatory system or superficially, in the skin, utilize a third mode of transfer, that of vector transmission. In this case a haematophagous, or blood-sucking, arthropod transports the parasite to another host. Many micro- and macroparasites of medical or veterinary importance, such as arboviruses, bacteria, rickettsia, protozoa and nematodes, are carried between hosts in this way (Lehane, 1991).

The parasite may have very transient contact with its transport vehicle, by passing from one host to the next on contaminated vector mouth-parts or by being ingested but passing through the gut unchanged and exiting in contaminated faeces. This type of transmission is known as 'mechanical'. Alternatively, 'biological' transmission occurs when the parasite undergoes a distinct life-cycle phase within the vector and engages in a parasitic association with it. This can just involve a phase of parasite growth and differentiation, as seen in filarial worms, such as Wuchereria bancrofti, where exsheathed microfilariae penetrate the midgut and undergo two moults within the thoracic flight muscles (Kettle, 1990). Alternatively, pathogens such as the plague bacillus, Yersinia pestis, and many of the arboviruses multiply in the vector but do not change in form. Finally, the malaria parasites and many of the trypanosomes and leishmanias both multiply and change to new forms within the vector.

┬ęCAB International 2002. The Behavioural Ecology of Parasites (eds E.E. Lewis, J.F. Campbell and M.V.K. Sukhdeo)

Mechanical transmission is, in effect, passive and no opportunity is created for the parasite or pathogen to interact with the vector. For mechanical passage via contaminated mouth-parts to be successful, rapid biting of successive new hosts must occur, because vector-transmitted parasites are short-lived in the environment. This mode of transmission is probably quite rare. Examples include parasites transmitted by fleas, such as the myxoma virus, which, in Britain, is carried from rabbit to rabbit by the flea Spilopsyllus cuniculi. In addition, parasite density in the host's blood meal must be great for the tiny volumes of blood that remain on most mouth-parts to contain sufficient parasites to infect a new host. In this respect, tabanid flies, with their spongy mouth-parts, which soak up blood, could be expected to be capable of mechanical transmission. Tabanus fuscicostatus transmits Trypanosoma evansi, the causative agent of surra in horses and camels, in this manner.

In contrast, if the vector also acts as a 'host' to parasite life stages, complex interactions between arthropod and parasite are likely to evolve. Evolutionary pressure will drive parasites to enhance their transmission success. In the case of vector transmission, it is reasonable to assume that the basic case reproduction number, R0 (the number of new infections that arise from a single current infection), in a defined population of susceptibles (Macdonald, 1957) will be increased if more vector-host contact occurs and if transfer between vector and host becomes more efficient. This is particularly so as transmission dynamics of vector-borne diseases are very different from those of directly transmitted diseases, because R0 can be an order of magnitude greater. The basic equations used to model R0 for vector-transmitted diseases incorporate the vectorial capacity (Q of the bloodsucking insect population. Vectorial capacity is the daily rate at which future inoculations arise from a current infective case (Garrett-Jones, 1964). Thus, in these cases, R0 = C/r (where r is the rate of recovery from infectiousness) (Garrett-Jones and Shidrawi, 1969). An estimate of C is derived from eight components (Dye, 1990); however, for each of these components assumptions are made that do not always hold (Dye, 1990; Rogers and Packer, 1993). For example, host selection by vectors is not always random and may be influenced by the disease status of the host (Day and Edman, 1983) and mosquito biting behaviour changes when infected with malaria (Anderson et al., 1999). It is almost inevitable that adaptive changes that enhance parasite transmission will cause changes to vector life-history traits, because the interests of the parasite are intricately linked with that of the vector via blood feeding (Hurd et al., 1995; Klowden, 1995); thus Cwill be underestimated.

Blood feeding is essential to the fitness of the vector, as it provides the female with a proteinaceous meal for egg production, and it is essential to the parasite, as host contact provides an opportunity for transmission. But blood feeding can be risky, due to host defensive behaviour (Day and Edman, 1984a; Randolph et al., 1992). Increased host contact increases the chances of vector mortality. Thus many vectors face trade-offs in terms of feeding strategies between carbohydrate (nectar) meals, which allow maintenance metabolism, and blood meals, which will increase reproductive output but may shorten lifespan (Koella, 1999). This is exemplified by mosquitoes, where feeding drive will be matched to the minimum meal size required to mature a batch of eggs (Clements, 1992) and trade-off decisions will be made with regard to egg-batch size/mortality risk (Anderson and Roitberg, 1999). For the parasite too, a conflict exists between maximizing host contact by increased vector biting and minimizing vector mortality by decreased biting. The parasite's success is thus constrained by a conflict between increasing transmission by increasing biting and decreasing mortality by decreasing biting. However, the optimum balance between host contact (biting) and mortality risk may not be the same for vector and parasite. This concept has been explored in a model of the transmission success of malaria sporozoites as a function of mosquito biting rate (Koella, 1999; Schwartz and Koella, 2001). Koella's model predicts that selection pressure will increase parasite transmission by changing the compromise between vector biting rate and vector reproductive output such that parasite success is maximized. If the trade-off positions postulated in this model also pertain to other haematophagous insects, we should expect many vector-transmitted parasites to evolve to a situation where they alter some aspect of biting behaviour. Evidence will be presented below to demonstrate that there are indeed many examples of parasites that do change both the host-seeking and the biting behaviour aspects of the blood-feeding behaviour of their vectors in ways that intuitively suggest that transmission to the vertebrate host will be enhanced.

Despite the obvious importance of vector blood-feeding behaviour to parasite-transmission dynamics, there is a major lack of quantitative data on the consequence of parasitic-induced alteration of this life-history trait. In particular, few studies have demonstrated that changes in vector feeding actually do increase parasite transmission. Yet verification of increased parasite success is fundamental to our understanding of the evolutionary significance of parasite-induced alteration of vector blood feeding.

If and when changes in behaviour are observed, are these non-adaptive pathological consequences of infection or has the parasite directly manipulated the host? Many authors have argued the importance of distinguishing between these options if we are to understand the evolutionary significance of host behavioural changes (Minchella, 1985; Moore and Gotelli, 1990; Horton and Moore, 1993; Hurd, 1998). Poulin (1995) identified key indicators of adaptive manipulation. Paramount among these was the need to demonstrate fitness benefits for the parasite. Natural selection will clearly favour a parasite that is able to alter the behaviour of its vector such that its transmission success is enhanced compared with that of its conspecifics. In addition, Poulin (1995) suggested that parasite-induced changes in host behaviour that are adaptive are likely to be complex, to function precisely to enhance transmission, to have arisen by chance and to have evolved several times in different taxa (see also Moore and Gotelli, 1990; Poulin, 1998).

True vector manipulation will occur via an extension of the pheno-type of the parasite (Dawkins, 1982, 1990) such that manipulator molecules are produced that directly affect vector behaviour patterns (Hurd, 1998). Manipulative effort is costly for the parasite; thus the degree of manipulation is likely to be constrained and manipulation will be optimized, not maximized (Poulin, 1994). A survey of the current literature on vector-parasite interactions suggests that we appear to be a very long way from identifying manipulator molecules in any vector-transmitted parasite. Thus, at the present time, the issue of pathology versus adaptive manipulation is difficult to assess and will remain so until substantive studies of several associations provide evidence with which to weigh the alternative hypotheses.

Blood feeding provides the point of contact between the vector and the next host, but this is not the only factor that is a candidate for adaptive manipulation. The activity and longevity of the vector will also affect chances of parasite success. Vectors with reduced lifespan may have fewer encounters with their hosts and thus fewer chances for transmission. This is particularly so if the parasite has a long developmental or extrinsic latent period in the host prior to becoming a patent infection, as do malaria parasites and filarial worms. If vector lifespan is compromised by infection during this developmental phase, there will be no transmission. It is difficult to generalize concerning the effect of parasites on vector lifespan, because conclusions resulting from survivorship studies are contradictory, even when the same parasite-vector association is being assessed (Lines et al., 1991; Lyimo and Koella, 1992). In addition, studies need to be conducted in the field, where stressors in addition to infection operate and parasites are associated with their natural vectors. One of the major problems that we face here is the difficulty in determining the age of insect vectors. Methods for assessing age or, more importantly, parous status (number of blood meals taken) that are simpler, quicker and more reliable than the present age-grading techniques (Detinova, 1962; Sokolova, 1994) need to be devised.

Parasites that develop and reproduce within the vector inevitably utilize host resources. If the vector does not replenish these resources more often than an uninfected organism, activity and/or longevity are likely to be compromised. In addition, many parasites evoke a defence response in their vector that, even if it does not eliminate the parasite, will be costly to the vector in metabolic terms (Ferdig et al., 1993; Richman et al., 1997; Luckhart et al., 1998). There is growing evidence to support the view that vector resource allocation may be altered by infection such that the balance between reproduction and growth and maintenance is changed, due to a curtailment of reproductive effort (Hurd, 2001). Evolutionary theory suggests that delayed or depressed reproduction will result in increased lifespan (Price, 1980); thus, if fecundity is reduced, activity levels and longevity may remain unchanged by the demands imposed by the infection, and fecundity reduction may be a strategy that minimizes the effects of infection (Hurd, 2001). Although parasites from many taxa are known to adversely affect the egg production of their vectors (Hurd, 1990), studies that provide data with which to assess the evolutionary history of this manipulation are rare.

Changes in vector behaviour must have a physiological, biochemical and molecular basis; thus it is as important to consider these aspects of manipulation as to try to determine whether behavioural changes actually enhance parasite success. A few studies are beginning to unravel the mechanisms underlying the curtailment of vector reproductive success. However, our understanding of the biochemical and molecular bases of the various aspects of haematophagous behaviour is negligible (apart from the endocrine control of the responsiveness of Aedes aegypti lactic acid receptors (Davis, 1984; Klowden et al., 1987)).

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