Introductions
The search for universal patterns of biodiversity requires a broad understanding of all species
interactions, including symbiotic associations. Symbiotic relationships are critical drivers of
community structure and coevolutionary processes (Vogelsang et al. 2006, Moran 2007, Noda et
al. 2007, Schmitt et al. 2007). Symbiosis as defined here in the current proposal follows the
definition of and includes parasitism, mutualism, and commensalism (Boucher 1985, Sapp
1994). Typically when there is a large size difference between members of symbiotic
interactions, the larger member is referred to as the host and the smaller member, leaving
external on, or internal inside the host, the symbiote. Often, ecologists have dismissed
commensalistic interactions, the 0, +ve end the symbiotic spectrum, as having little importance
in community dynamics. This is wrong on two fronts. First, species rarely interaction in simple
pair-wise interactions by rather species interactions as webs of involvement (REF). Hence,
although the host of a commensalistic interaction may not be impacted by the symbiote (the 0
affect of the interaction), the benefits that the symbiote derives from the host (the +ve effects of
the interaction) may have significant effects on how the symbiote interacts with other species.
Secondly, both theory and empirical evidence suggest that microbial symbiotic associations are
dynamic with commensalisms and parasitism opposite extremes of a continuum of effects
(Hochberg and van Baalen 2000, Thompson & Cunningham 2002, Neuhauser & Fargione 2004,
Sapp 2004, McCreadie et al.2005).
Of particular interest is what promotes the various states of symbiosis. For example, the
evolution of mutualism has raised several puzzling questions that often have been addressed by
invoking the ‘prisoner’s dilemma’ couched in game theory (De Mazancourt 2005). Using a
fungal symbiote (trichomycetes) and an insect host (larval black fly) as our model system, we
are exploring nature of microbial symbiotic associations in running-water habitats. Using this
model system and making a few simple assumptions, we propose a simple dynamic model which
can account for all states of the symbiosis based solely on the environmental conditions in which
the host is found and the population size of the symbiote.
Trichomycete - black fly model system
The Harpellales (Zygomycota), known commonly as ‘trichomycetes’, are a cosmopolitan class
of filamentous fungi in the guts of various arthropods, particularly the larvae of aquatic several
orders of aquatic insects(Lichtwardt 1986, 1996). Host larvae are colonized upon ingestion of
asexual trichospores (Lichtwardt 1996). Following sporangiospore extrusion, young thalli attach
to either the midgut or hindgut lining and produce new trichospores within 24 h (Vojvodic &
McCreadie 2007). These trichospores are shed into the gut lumen and exit the host via the anus.
Sexual reproduction, via zygospores, is known in some species (Lichtwardt 1996). At least some
species of trichomycetes are able to invade the larval germ tissue, eventually replacing the adult
female black fly eggs with ovarian fungal cysts. These cysts are then deposited by females
during oviposition (Moss & Descals 1986, Labeyrie et al. 1996). It is though this process is a
dispersal mechanism for trichomycetes (Lichwardt 1986).
Larval black flies are found in habitats ranging from temporary trickles to large rivers, and are
often a dominant part of the stream macroinvertebrate community (Adler & McCreadie 1997).
Larvae adhere to solid substrates in the stream and obtain food as filter feeders, scrapers, and
collector-gatherers (Currie & Craig 1988). The adults are terrestrial and the female typically
requires a blood-meal to develop a clutch of eggs. Black flies are an ideal choice of hosts for our
model study because 1) larvae play a critical role in resource turnover (Cummins 1988) and
therefore are an important subcomponent of the lotic community, 2) colonized hosts can be
identified to species easily and colonization of hosts by trichomycetes and 3) is not influenced by
the presence of non-trichomycete symbiotes (Kim & Adler 2005).
Paragraph about commensalism/parasitism continuum.
Fitness is a measure of the reproductive success of an individual allele, organism or species,
depending upon the context. Fitness depends upon the relative rate of survival to a specific age
and the expected number of offspring at the age and may be measured as a growth rate r (also
known as the invasion rate, the intrinsic rate of increase or the Malthusian parameter) or as a
reproductive number (the per generation ratio of multiplication) (Brommer 2000, Roff 2008).The
growth rate is the parameter r satisfying the Euler-Lotka equation  e  rx l x mx  1 while the
reproduction number R0 is defined as  l x mx . In each case, the sum is taken over each age x, lx is
the survival rate to age x and mx is the fecundity at age x. Estimating fitness would require agespecific estimates of survival rates and fecundity (stored in a so-called Leslie matrix (McGraw
and Caswell, 1996) but alternatively phenotypic attributes known to correlate with fitness can be
used as a measure for fitness. For example, experimental measures of fitness for trichomycetes
are head size and number of offspring (ref).
In a first model for the relationship between fitness and parasitism, we model the fitness of an
individual trichomycetes as a parameter that depends directly upon environmental factors,
including available resources and parasitism. In a later model, we will define fitness in a more
conventional way as measured from a population-based SIR model and show that our
conclusions are similar.
The Model
First we make the simple assumption that it is the net difference between costs and benefits
exchanged by participants in a symbiotic association determines where on the commensalism B
parasitism continuum the association lies. Because costs and benefits should vary over spatial
and temporal axes, we also suggest that shifts along this continuum should be common. The
second assumption that the symbiote imposes a cost on the host and that it can augment the host
procurement of a needed resource. Hence mutualism then becomes a point on a continuum of
effects as the benefit:cost ratio to the host changes over gradients of host resource and symbiote
density. In our model system trichomycetes require the host for reproduction, hence the
relationship with the host remains positive. We are now in a position to explore, mathematically,
the implications and predictions of these simple assumptions.
Assumptions of model
I) Fitness, F, depends on a number of resources, R1, R2 ... including RE, the availability of
resource E
F  F R1 , R2 ,..., RE 
 k1 R1  k 2 R2    k E RE
For simplicity, fitness effects are considered to be additive and linear; changing this assumption
does not change model predictions. (need to check and verify)
ii) Contribution of resource availability to fitness does not increase without bound. There is a
maximum value, R
_ I ,that the ith resource can contribute to fitness.
F = k1 R
_ 1(1e a 1R1) + k2 R
_ 2 (1e a 2R2) ... + kE R
_ E (1e a E RE), where ki and ai are
constants and R̂i is the maximum value the ith resource can contribute to fitness.
iii) Symbiotes benefit host fitness by increasing the availability of resource E and exerting a
cost, C, on fitness on a per capita basis. Resource availability depends linearly on the size of
the symbiote population:
RE  RE 0  BE  N where RE 0 is the availability of resource E in the absence of the
symbiote, N is the population size of the symbiote per host, and BE is the net per capita benefit
of the symbiote. Fitness cost of the symbiotes is thus
F  F R1 , R2 ,..., RE   CF N
Model Predictions
The net effect of a symbiote population of size N on host fitness, F, is thus
F  F ( N )  F (0)  F R1 , R2 ,..., RE 0  BE N   CF N  F R1 , R2 ,..., RE 0 

 k E Rˆ E (1  e  sE  RE 0  BE N  )  C F N  k E Rˆ E (1  e  sE R0 E )
 k Rˆ (e sE R0 E  e  sE  RE 0  BE N  )  C N
E
E



F
 k E Rˆ E e  sE R0 E 1  e  sE BE N  C F N
The effect is positive ( F  0 ), if:


k E Rˆ E e  sE R0 E 1  e  sE BE N  C F N
The phase diagram (Fig. 1) shows expectations over gradients of food availability and symbiote
density. The line separating the parasitic and mutualistic regions shows the size of the symbiote
population under a commensalistic association for a given resource availability. In practice,
commensalism would be a band because some minimal difference is needed before beneficial
or parasitic effects would be detectable.
Our model predicts that the nature of the symbiosis would vary with host gains and losses
associated with changes over gradients of food and symbiote density. Because both
trichomycete density and host-food resources vary over spatial and temporal axes, our model
also implies that the nature of the association should show both temporal variation and
geographic structure. If costs and benefits are species specific to each symbiote then symbiote
diversity and species composition would be predict to also effect host fitness.
Laboratory experiments to date provide support for many aspects of this model. Under
conditions of high larval food supply the trichomycete Smittium culsetae appears to be a
commensal as host survival did not vary between colonized and uncolonized larvae. However,
under conditions of starvation, hosts with S. culsetae had a significantly higher survival rate
than host without this fungus. Under these conditions, S. culsetae shifts to a mutualist.
Laboratory experiments that member of the genus Smittum can also be parasitic. Smittium
(probably culisetae), was shown to induce mortality rates exceeding 80% in Anopheles
gambiae (Coluzzi 1966). Similar mortality rates were found for various species of mosquitoes
infected with Smittium morbosum Sweeny (e.g., Dubitskii 1978, Sweeney 1981, Shimada et al.
1995).
Summary
How and why symbiosis arises among often phylogenetically very different participants has
been of interest to both ecologists and evolutionary biologists for decades. We suggest a simple
solution to the varying states of the symbiotic interactions under the conditions of an obligate
endosymbiote (requires the host) interacting with a facultative host (does not require the
symbiote). Given the simple assumptions that the symbiote imposes a cost on the host and that
it can augment the host procurement of a needed resource, then commensalism, mutualism and
parasitism mutualism become points along a continuum of effects as the benefit /cost ratio to
the host changes over gradients of host resource and symbiote density.