The principles of disease dynamics can be considered in abstract terms, divorced from any particular instantiation. Three major aspects distinguish animal STDs from their non-sexually transmitted counterparts (Lockhart et al., 1996), namely the nature of the transmission dynamics, their age-specificity, and the fitness consequences of the disease on the host. In STDs transmission depends on frequency rather than density of infectives; STDs are transmitted and expressed in the adult rather than juvenile stage; and STDs generally result in sterility rather than in high mortality. These ideas will be developed in the following sections.
In applied plant pathology, where the major concern has been with the spatial spread in crops planted at relatively uniform spacing, the predominant axiomatic approach has been to consider dispersal from a point source. This contrasts with studies of disease in natural systems where the interest has been on understanding population regulation. Here, the main approach has been to consider how individual behavior influences contacts, and how these contacts vary with density. I will take this perspective here.
To gain a better axiomatic perspective on venereal diseases, I will focus on the relationship between contacts and density. The intuitive and natural assumption is that the number of contacts will increase with increasing density, and this is the classical mass-action assumption that has been made in most epidemiological models. However, because there has been some semantic confusion about the term ‘mass-action’ as applied to epidemiological models (De Jong et al., 1995), I simply call this ‘density-dependent transmission’. Density-dependent transmission also follows from passive dispersal of propagules: the closer individuals are, the more likely they are to become diseased.
However, in sexually transmitted diseases in humans and many animals, the number of sexual contacts per individual in a given interval may be relatively insensitive to density. People generally do not acquire more partners at more crowded parties and animals are limited in their mating opportunities by many factors unrelated to population density (e.g. territoriality, social structure, mate guarding, sperm plugs, etc.). It follows that if contact number is independent of density, then transmission depends only on the fraction of individuals that have the disease: this is ‘frequency-dependent transmission’ (Getz & Pickering, 1983; Antonovics et al., 1995; Lloyd-Smith et al., 2004). This type of transmission is expected for human venereal diseases; it was used in the first models of gonorrhea (Hethcote & Yorke, 1984) and is now used in general models of acquired immune-deficiency syndrome (AIDS) (Anderson & May, 1991). Therefore, when a disease biologist speaks of sexual transmission in animals, the transmission dynamics is now canonically assumed to be frequency dependent.
We can now ask if this kind of frequency-dependent transmission also occurs in plants: Do plants have ‘axiomatic STDs’?. The answer is that they do, at least approximately so, but for a very different reason than in animals. Plants do not limit their number of partners and do not have territories, but pollinators are able to adjust their flight distances to compensate for changes in plant density (Levin & Kerster, 1969; Handel, 1983; Schmitt, 1983). Indeed, much of the stimulus for the early work on pollinator flight distances was to show that genetic neighborhoods in plants might be relatively independent of plant density. Indeed, it was this expectation that led us to make a direct conceptual, rather than definitional, connection between pollinator transmission in plants and sexual transmission in animals (Antonovics & Alexander, 1993; Thrall et al., 1993b).
Another similarity between vector and sexual transmission arises if we assume that a vector such as a mosquito or tick takes a limited number of blood meals over its lifetime, or in some period of time. Transmission depends on the probability that the vector bites an infected host (i.e. on disease frequency within the host population), and measures of ‘vectorial capacity’ or the effectiveness of vectors at transmitting a disease include frequency-dependent terms (Anderson, 1981). There is also an increasing interest in applying frequency-dependent transmission to explain the prevalence of pathogens in vectors in natural communities that act as reservoirs for human diseases (Schmidt & Ostfeld, 2001; LoGiudice et al., 2003). Frequency-dependent transmission is therefore often posited as an approximation for both sexually transmitted and vector-transmitted diseases.
If we use this axiomatic approach and identify human venereal diseases as being canonically characterized by frequency-dependent transmission, it becomes clear that many plant diseases that I included in the previous sections as being venereally transmitted on ‘definitional’ grounds do not have frequency-dependent transmission. For example, most grass smuts that infect inflorescences are dispersed by wind and would be expected to show density-dependent transmission.
These distinctions are very important because whether a disease is transmitted in a frequency-dependent or density-dependent manner has large consequences for host–pathogen dynamics (Getz & Pickering, 1983; Antonovics, 1994). Single-species thresholds (Thrall et al., 1993b; Lockhart et al., 1996) and two-species thresholds are quite different, and in studies of disease prevalence in natural populations the expected positive relationship between density and disease prevalence may be reversed (Antonovics et al., 1997). Moreover, while density-dependent transmission readily promotes population regulation, it is initially hard to see how frequency-dependent transmission would do so given that pathogen spread does not increase as host density increases. However, diseases with frequency-dependent transmission can regulate populations if there is also disease-independent regulation that only acts on the healthy class (Thrall et al., 1993b, 1995). It is interesting that these conditions happen to be easiest to meet if the disease is also sterilizing and resource limitation acts on juveniles that, in the absence of vertical transmission, are not expected to acquire STDs. These features are typically found in many STDs, including the pollinator-transmitted anther smuts (Lockhart et al., 1996).
The mechanisms of vector transmission are very rich biologically, and the simple scenario of pollinators flying further when host individuals are spaced further apart is a rather blatant oversimplification. Indeed, studies showing that seed set may be reduced at low densities suggests that such ‘compensatory behavior’ by pollinators may be restricted to a limited range of densities (Kunin, 1993, 1997; Wilcock & Neiland, 2002). Vectors may respond to host density because of ‘functional’ responses that result from changes in vector behavior, or ‘numerical’ responses that result from changes in the size of the vector population. Pathogens may also have life-history stages within the vector (e.g. many aphid and leaf-hopper transmitted plant viruses). Where the vector uses the host as a resource, it is likely that vector dynamics is coupled at some level with host dynamics; this is often assumed in many malaria models (Bailey, 1982). However, if the number of vectors is limited by factors other than host abundance, and if they cannot rapidly increase their visitation rate as host density increases, then the number of vector contacts per host individual is expected to decline as the density of hosts increases. Indeed, at very high densities, one expects disease transmission by vectors to decline.
There have been essentially no experimental studies determining how disease transmission varies with density and frequency, either in plants or animals. The exceptions are studies of anther-smut transmission over a range of host and pathogen densities. Antonovics & Alexander (1993) showed that spore deposition, a surrogate measure of pollinator visitation, increased with an increasing frequency of diseased individuals, but declined somewhat with increasing density of diseased individuals. Antonovics et al. (1995), in a reanalysis of this data, also showed that spore deposition declined with an increase in total population density, indicating pollinator limitation. Bucheli & Shykoff (1999) also examined spore deposition over a range of disease densities and frequencies, as well as overall plant spacings. Their results showed a more complicated pattern, with treatment effects being significant only at the first sampling date. At the first sampling, spore deposition increased with diseased plant frequency, and was uninfluenced by plant spacings of 0.5 m and 1.5 m, but then declined at very large plant spacings (3.0 m). Biere & Honders (1998), studying anther-smut transmission in a natural population of mapped individuals of Silene alba and Silene dioica showed that disease spread was best explained by frequency-dependent transmission in patches where plants were closely spaced, but by density-dependent transmission in patches where plants were further apart. Because of their convenience and immobility, plants provide much better opportunities than animals to investigate the dynamics of the transmission process both experimentally and observationally. Extending such experiments to other disease systems is important for establishing empirical generalizations about the transmission process.
In humans, where experiments are impossible but individuals are more easily identified, individual behaviors and mating structures are used to infer rates of STD spread (Anderson et al., 1989). There is therefore a rather large and somewhat overwhelming body of theory on effects of number of partners, copulations per partner and concurrence of multiple partnerships and sexual activity classes on STD spread in humans (Castillo-Chavez et al., 2002). However, it is difficult to see how such a theory could be easily applied to natural populations of plants or animals. Even in mammals, where there is extensive data on mating systems, it is often unclear how to translate this data into measures of potential disease transmission (Thrall et al., 2000; Altizer et al., 2003).
Another axiomatic property of STDs in animals is that they are transmitted at the adult stage only during the mating or flowering season. Several expected features of STDs follow from this.
First, in the absence of alternative transmission modes or alternate hosts, the persistence of such diseases is dependent on overlapping generations. If reproduction is continuous, as in humans, these conditions are easy to meet, but in seasonally reproducing organisms it requires that the hosts be perennial. We showed (Thrall et al., 1993a) that records of anther-smut disease were much more frequent in perennial than in annual members of the Caryophyllaceae. Viruses that are transmitted to another adult plant via the pollen also appear to be frequent in small fruits and orchard crops that are perennial (Mandahar, 1981; Mink, 1993). Conversely, we can predict that if a disease is transmitted only in the adult phase, then there should be alternative adult transmission modes or methods whereby the disease can persist over winter; this appears to often be the case in many of the inflorescence smuts in the Ustilaginales that infect annual grasses (Fischer & Holton, 1957). It would be interesting to review the life-histories of adult-transmitted diseases in annual and perennial hosts.
Second, because of this requirement for host persistence, we would also predict that diseases transmitted in the adult phase would have a much smaller effect on host mortality than diseases which are transmitted in the juvenile stages. I discuss this further in the following section.
Third, if the disease is transmitted only to adults, as in the case of frequency-dependent sexual transmission, then the diseased class will include no juveniles (e.g. no seedlings or prereproductives), whereas the healthy class will include both juveniles and adults. It is well known that resource limitation on growth and survival in perennial plants are much more likely to act at the seeding stage than at the adult stage (Shaw & Antonovics, 1985). Therefore, resource factors limiting population size are more likely to act on the healthy class that includes juveniles than on the diseased class that includes only adults. This inequality of resource limitation on the diseased and healthy classes facilitates the coexistence of hosts and their pathogens when there is frequency-dependent transmission. The reason is that while the healthy class may increase at a greater rate than the diseased class when the population is small, and may therefore wash out the disease, this is reversed when the population is large. Therefore, the disease has an advantage in large populations not because it is transmitted more, but because diseased individuals are less affected by resource limitation (Thrall et al., 1993b).
The negative effect of a pathogen on the fitness of the host can be expressed either as increased mortality or as decreased fecundity. Much of the focus in classical disease biology has been on the mortality component of virulence, but there are a number of reasons to expect STDs to primarily affect fertility. Diseases that affect fertility are likely to have a more severe effect on population size than diseases that affect mortality because increased mortality also reduces the duration of the infection. Consequently, the forces that affect the evolution of virulence are different depending on whether the pathogen increases mortality or decreases fecundity (O’Keefe & Antonovics, 2002).
First, as mentioned above, the persistence of many STDs without alternative transmission modes is dependent on perenniality; increasing host mortality would greatly decrease disease persistence. However, simple adaptive reasoning would suggest that all pathogens should evolve in the direction of increasing sterility rather than decreasing mortality, as sterility components of virulence do not affect the duration of the infectious period. Indeed, in many examples of ‘parasitic castration’ the growth rate and longevity of the host are increased (Clay, 1991). Second, because transmission is during the reproductive process, lesions that are associated with disease transmission will be likely to negatively influence reproductive success. Third, theoretical studies on conditions for coexistence of frequency-dependent pathogens with their hosts show that such coexistence is more likely when the disease causes sterility rather than mortality (Thrall et al., 1993b). In an analysis of causal relationships between sterility and transmission mode, we failed to distinguish whether sexual transmission led to the evolution of sterility, or whether sterility favored the establishment of STDs (Lockhart et al., 1996). However, this study was broadly comparative and there is a need for more rigorous phylogenetic studies of virulence evolution, and this may be especially productive in plants given the diversity of transmission modes that are associated with reproduction.
Evolution of sexual transmission
Another axiomatic aspect of sexual transmission in animals is that we would expect this transmission mode to be favored at low population densities, when sexual contacts might more common than nonsexual contacts (Smith & Dobson, 1992). We used generalized contact functions to investigate the evolution of transmission mode (Thrall et al., 1998) by considering the relative success of pathogen strains that allocated differently to sexual and non-sexual transmission. We showed that the relative success of pathogens with different degrees of the two types of transmission was indeed related to the equilibrium population sizes of the diseased populations, but that these sizes were not just determined by transmission mode but by the sterility and mortality effects of the disease. Another particularly interesting result was that even if two strains excluded each other from an individual host, they could still coexist if they had different transmission modes (Thrall & Antonovics 1997). It is interesting that several human sexually transmitted diseases have a nonsexually transmitted counterpart (e.g. herpes 1 and herpes 2, pubic lice and head lice, genital and ocular chlamydia, syphilis and yaws). There is little information in plant pathogens on factors that might determine the evolution of different transmission modes, or the pathways of such evolution as determined by phylogenetic relationships. A system that shows promise for untangling the evolution of transmission modes is the Epichloë system, which has both vertical and horizontal transmission (Meijer & Leuchtmann, 2000, 2001).