Life history strategies and host-parasite coevolution

Learning objectives

Appreciate the multiple forms parasites can take
Be able to define general parasite terms (e.g., obligate, facultative, etc.)
Understand parasite life history tradeoffs
Be able to quantify parasite specialism

Parasite diversity

_{Byers et al. 2019 PRSB}

Parasite diversity

_{Dallas et al. 2018 GEB}

How do we really define parasite diversity?

Diversity in:

number (taxonomic)
phylogenetic
functional
infection modes
tissue infected
impacts
host specificity
…

Diversity in numbers

Diversity in phylogenetics

A host is infected with two parasite species
- they could be closely related parasites, or quite distantly related parasites
So when quantifying parasite diversity (either within a region or within a host species), considering the phylogenetic distance between parasites can be used as a measure of diversity

Phylogenetic diversity for free-living animals

Take the tree of free-living species
Calculate some index of dispersion for species found in the local community
Mean pairwise distance is a common one

Quantifying phylogenetic diversity for parasites

For a given location or host community, what is the ‘index of dispersion’ for the parasite community?
The parasite phylogeny is used to measure phylogenetic diversity, the host phylogeny is used to calculate phylogenetic specificity

Phylogenetic diversity of parasites

What geographic location would be the most phylogenetically diverse for parasites?

Mammmal richness and phylogenetic diversity

_{a is species diversity, b is phylo diversity; Voskamp et al. 2017 J Biogeography}

Host and parasite diversity often related

_{Dallas et al. 2018 GEB}

Phylogenetic specificity across parasite groups

What parasites would be most (or least) phylogenetically specific?

Phylogenetic specificity across parasite groups

This is broken down by parasite group and transmission mode
More negative values indicate higher phylo-specificity

_{Park et al. 2018 PRSB}

Phylogenetic specificity versus phylogenetic diversity

The last slide was phylogenetic specificity (single parasite in host community)
Phylogenetic diversity could be defined at the parasite community level, so it would use the parasite phylogeny
So keep in mind the distinction here between diversity and specificity

Functional diversity

Scientists have been obsessed with functional diversity for the last 15 years or so
Argument: quantifying the differences in species traits provides information that the phylogeny may not
In free-living species, this would be the variance in host body size or plant height or feeding mode

Functional diversity/specificity

For parasite species, it is some measure of the variance in the traits of infected host species ( specificity )
For entire parasite communities, it is the variance in traits of the parasites ( diversity )

Can you give me an example of both of these?

Diversity in infection modes

macroparasites versus microparasites
direct versus indirect transmission
simple versus complex life cycle

Env-transmitted pathogen (simple)

Complex life cycle

Diversity in infection modes

Six parasite strategies:
- parasitic castration
- directly transmitted parasitism
- trophically-transmitted parasitism
- vector-transmitted parasitism
- parasitoidism
- micropredation

parasitic castrators

remove the host’s ability to reproduce
take that energy and/or space
tradeoff between consumption and longevity faced by parasites

parasitic castrators

directly transmitted parasitism

do not require vector
this includes environmentally-transmitted pathogens (e.g., cholera)

trophically-transmitted parasitism

transmitted through predation of the host
complex life cycle parasites
can modify host behavior (why?)

Trophically-transmitted parasites are transmitted by being eaten by a host. They include trematodes (all except schistosomes), cestodes, acanthocephalans, pentastomids, many round worms, and many protozoa such as Toxoplasma (Poulin 2015). They have complex life-cycles involving hosts of two or more species. In their juvenile stages they infect and often encyst in the intermediate host. When the intermediate-host animal is eaten by a predator, the definitive host, the parasite survives the digestion process and matures into an adult; some live as intestinal parasites. Many trophically-transmitted parasites modify the behavior of their intermediate hosts, increasing their chances of being eaten by a predator. As with directly transmitted parasites, the distribution of trophically transmitted parasites among host individuals is aggregated (Poulin 2015).

vector-transmitted parasitism

Rely on other organisms for transmission (e.g., mosquitos, ticks, lice, fleas, etc.)
Sometimes reproduce in vector, sometimes only reproduce in definitive host

parasitoidism

Insects that kill their hosts (so more like predation)
Larvae live as parasites within infected host

Parasitoids are insects which sooner or later kill their hosts, placing their relationship close to predation (Stevens 2010). Most parasitoids are parasitoid wasps or other hymenopterans; others include dipterans such as phorid flies. They can be divided into two groups, idiobionts and koinobionts, differing in their treatment of their hosts (Gullan and Cranston 2010).

Idiobiont parasitoids sting their often large prey on capture, either killing them outright or paralyzing them immediately. The immobilized prey is then carried to a nest, sometimes alongside other prey if it is not large enough to support a parasitoid throughout its development. An egg is laid on top of the prey and the nest is then sealed. The parasitoid develops rapidly through its larval and pupal stages, feeding on the provisions left for it

micropredation

attacks more than one host (reducing each host individual fitness by small amount)
e.g., leeches, mosquitos, fleas, ticks, lice

Diversity in tissue infected

Tissue tropism: range of host tissue types which the pathogen can infect
e.g., viruses tht must bind to specific cell surface receptors to enter a cell

How much diversity is there in tissue tropism?

A fair bit, often related to transmission mode
Tissue specialist: mumps (parotid salivary glands)
Tissue generalist: ebola (monocytes, macrophages, dendritic cells, endothelial cells, fibroblasts, hepatocytes, adrenal cortical cells, and epithelial cells)

Defining tissue tropism is hard

Could define by system (e.g., circulatory, hepatic, respiratory, etc.)
By organ (e.g., stomach)
Or by cell type (e.g., endothelial)
Or probably some other ways

Diversity in impacts

Some parasites have little impact (e.g., some parasitic worms), some have pronounced impact (e.g., anthrax)
Impacts quantified as
- morbidity/mortality
- energetic cost to host
- fitness cost
- etc.

Diversity in host specificity

Host specificity: range and diversity of types of hosts a parasite can infect
Generalism versus specialism
We’ve talked about specialism in a couple of ways (taxonomic, phylogenetic, and functional)

What’s the most generalist parasite you can think of?

End of lecture 1

What have we learned

Parasites are cool
Parasite diversity can be defined in a bunch of different ways
Parasites can be specialists or generalits in different ways

today we will dive into parasite specificity

Why specialize?

High infectivity/transmission in preferred host

Why generalize?

Need a host to reproduce
Potential for invasion of new habitats
Co-extinction is bad

How do we quantify parasite specialism?

number of host species infected (host range; taxonomic)
functional dispersion of host community (functional)
phylogenetic dispersion of host community (phylogenetic)

relative utilization of different host species (tropism)?

Specialism-generalism tradeoffs

Jack of all trades, master of none?
- Proposes a relationship between ability to infect and host specificity
- Generalist parasites should tend to infect with low success (reduced prevalence or intensity)

But do we see evidence for this relationship?

Animal species with larger local populations tend to be widespread across many localities, whereas species with smaller local populations occur in fewer localities. This pattern is well documented for free-living species and can be explained by the resource breadth hypothesis: the attributes that enable a species to exploit a diversity of resources allow it to attain a broad distribution and high local density. In contrast, for parasitic organisms, the trade-off hypothesis predicts that parasites exploiting many host species will achieve lower mean abundance on those hosts than more host-specific parasites because of the costs of adaptations against multiple defense systems. We test these alternative hypotheses with data on host specificity and abundance of fleas parasitic on small mammals from 20 different regions. Our analyses controlled for phylogenetic influences, differences in host body surface area, and sampling effort. In most regions, we found significant positive relationships between flea abundance and either the number of host species they exploited or the average taxonomic distance among those host species. This was true whether we used mean flea abundance or the maximum abundance they achieved on their optimal host. Although fleas tended to exploit more host species in regions with either larger number of available hosts or more taxonomically diverse host faunas, differences in host faunas between regions had no clear effect on the abundance-host specificity relationship. Overall, the results support the resource breadth hypothesis: fleas exploiting many host species or taxonomically unrelated hosts achieve higher abundance than specialist fleas. We conclude that generalist parasites achieve higher abundance because of a combination of resource availability and stability.

http://dx.doi.org/10.1086/423716

Not really (at least for fleas)

Why does parasite type matter here?

_{Krasnov et al. 2004 Am Nat}

We don’t see it for Plasmodium in birds either

But there’s a caveat here

These figures differ a bit
- First was mean abundance of flea parasite
- Second was maximum prevalence in most common host
The distribution of prevalence is important here
- If I infect one host really well, but 5 other hosts less well, how much of a generalist am I?

The costs of being a generalist are difficult to clearly define and test

Host-parasite coevolution

Infection is costly to hosts in terms of fitness, leading to evolution of host defenses
Parasites want to infect, leading to evolution of novel infection strategies

Host-parasite coevolution

Possible trajectories of host-parasite coevolution

_{Buckingham & Ashby 2022 J Evol Biol}

Host-parasite coevolution

The difference between deterministic and stochastic systems

_{Buckingham & Ashby 2022 J Evol Biol}

Host-parasite coevolution

Resistance evolution as a function of the cost on host fitness

_{Buckingham & Ashby 2022 J Evol Biol}

Host-parasite coevolution

This cyclic pattern of selection/evolution is often referred to as Red Queen dynamics
Idea comes from Through the Looking Glass, where the Alice was running just to keep her place

What happens when resistance is either cheap or hugely beneficial?

_{Cooke et al. 2023 Epidemiol Infect}

Why is this not a great example of Red Queen dynamics?

What is the “goal” of the parasite?

To reproduce. So it doesn’t really want to kill the host, right?
But it also has to reproduce and consume some aspect of the host, which comes at a fitness consequence for the host.
There’s a conflicting balance between
- trying to reproduce (which causes harm to host)
- flying under the radar (transmission to the next host)

optimal virulence

Virulence: pathogen-induced mortality of infected host
Pathogen needs to grow in infected host, but dead hosts don’t transmit
So the optimal strategy is not maximal virulence, but some intermediate (or even low) virulence

What examples do you know of related to changes in virulence in an evolving pathogen?

Many SARS-COV2 strains through time

Initial strain had highest pathogenicity (even though we saw greatest mortality with Alpha)
Omicron has the lowest pathogenicity

How have we used virulence evolution to our benefit?

the creation of live attenuated vaccines
live vaccines use avirulent strains of the pathogen to induce host immune memory
e.g., Sabin (oral) polio vaccine; the measles, mumps, rubella, yellow fever, and chicken pox (varicella) vaccines; one of the influenza vaccines (flu mist); the tuberculosis (BCG) vaccine; etc. etc.

What parasites would not follow this general pattern of virulence attenuation?

Fungal pathogens, generally
Pathogens with a long-lived environmental stage (e.g., anthrax)

optimal virulence

Essentially a balance between parasite growth and host exploitation
Idea in this tradeoff model is to maximize lifetime transmission success (LTS)
This leads to a non-linear relationship between LTS and virulence

the ideal parasite maximizes LTS

optimal virulence

LTS is y-axis, virulence is x-axis

_{Jensen et al. 2006 PLoS Biology}

But we’ve only been thinking about parasite evolution

It takes two to Red Queen, so we might expect hosts to evolve resistance
And they do, but sometimes they don’t

Why would a host not evolve resistance to a parasite?

parasite does not impact host fitness too much

resistance is costly

they simply can’t (it’s not really a choice, right?)

Resistance-tolerance tradeoffs

A host can evolve to resist the effects of a parasite or to reduce parasite impacts
These are often depicted as two separate responses to parasite pressure
Resistance : infected hosts actively reduce parasite burden
Tolerance : infected hosts try to limit damage to host fitness

Resistance-tolerance tradeoffs

This happens at individual level, but with implications to evolutionary trajectories
Host fitness at one generation determines the allele frequency in the next
So if tolerant hosts have highest fitness, it might result in evolution towards tolerating the parasite
But at the population-level, this is a bad strategy (unless you’re a bat)

Why is tolerance a bad population-level strategy?

Let’s end on a community note

Parasites can exert pressures on host communities
Differential effects on host species can drive interesting dynamics

_{Rohr & Best 2010 Functional Ecology}