Parasite infection alters host behavior

• Behavioral defense (e.g., grooming)

• Parasite manipulation (e.g., parasite-induced changes to host behavior)

• Sickness behavior (e.g., fever)

Grooming

• Societal benefits

• Removal of ectoparasites

  • which can vector some rough parasites

Humans groom, but what are other related activities that we do?

Desert rodent grooming behavior and flea mortality

Preening

Birds will use their beaks to reorient their feathers, clean plumage, and check for ectoparasites.

Preening can actually completely clear birds of feather lice

_{Bush & Clayton 2023 J of Parasitology}

Uropigeal gland

This gland contains oil that the birds use during preening, distributing it among their feathers.

• good for waterproofing
• anti-parasitic
• anti-bacterial

Bird bill size influences ability to remove parasites

• Parasites specialize on certain host species.

• Lice specialize on birds they can parasitize.

• Tends to lead a relationship where bigger birds have bigger lice.

Bigger host, bigger parasite

This is called “Harrison’s rule” and has mixed support.

What’s driving this?

• Differences in attachment rate? (no)

• Differences in feeding success? (no)

• Escaping from preening (yes)

Medicinal plant use

Hosts will change their diet to combat parasites

Monarchs and medicinal plant use (ish)

(ish) because used for anti-predator and anti-parasite

• Monarch butterflies are a classic example
  • sequester cardenolides from milkweed plants
  • deters predators
  • reduces spore load of OE parasite

If infected, preferentially lay eggs on toxic plant

Medicinal plant use is just one type of self-medication

Using the environment in your favor

• Hosts may preferentially occupy different environments to avoid parasite encounter or infection

Entomophthora muscae, fungal pathogen of house flies

Behavioral fever

• Flies can’t generate their own body heat to change internal temperature.

• If infected, prefer warmer environments

_{Kalsbeek et al. 2001. Biological control, 21:264-273.}

Behaviors to avoid encounter

Just go where the parasites are not, right?

Typically manifests in two ways:

• uninfected individuals spending more time “away” from parasites

• uninfected individuals avoid infected individuals

Behavioral avoidance driven by chemical signals

• Behavioral avoidance in terrestrial systems relies more on visible signs of infection

• In aquatic systems, a lot of it may be chemo-sensory

Behavioral avoidance driven by chemical signals

Cues for behavioral avoidance

• visual cues

• chemical cues

• auditory cues

_{see Behringer et al. 2018 Phil Trans B for a 4 page long table of examples}

Host behavior responses to infection risk

• Parasite removal

• Grooming

• Medicinal plant use

• Behavioral fever

• Behavioral avoidance

  • Self-annointing / swatting
  • Seeking low-risk habitats
  • Avoid infected conspecifics

Parasite manipulation of host behavior

Some behaviors predispose host to things that benefit the parasite

• increased growth rate of parasite inside host

• increased predation risk for trophically-transmitted parasite

Let’s go through some cool examples of this

Cordyceps sp. (fungi) in insect hosts

Leucochloridium paradoxum (trematode) infecting snails

Myrmeconema neotropicum (nematode) infecting ants

Host behavior can

• reduce parasite burden (e.g., grooming)

• enhance parasite burden (e.g., parasite manipulation)

What types of parasites would benefit most from manipulating host behavior?

And what parasites would really not want to directly manipulate host behavior?

Sickness behaviors

• Typically include anorexia, fatigue, and reduction in social and reproductive activities

• Hypothesized to be adaptive changes for host

• Incidental though, as some of these behaviors are result of body fighting parasite

Incidental changes in behavior

• Sleepiness results in reduced contact with others
  • could aid in recovery
  • but could also increase transmission of some parasites

What hypothesis could we pose around the expression of sickness behaviors across parasite species?

Decreased cognitive ability

+ COVID brain fog (jk)

• Bombus impatiens infected by Crithidia bombi (protozoan)

Questions to think about

• When are sickness behaviors maladaptive to the parasite?

• What parts of the transmission process (encounter + susceptibility) do each of these behaviors (grooming, sickness, manipulation) affect?

• Where would self-medication of hosts fall in the continuum of resistance and tolerance tradeoffs?

End of lecture 1

Host immunological responses to infection

• Adaptive and innate immune defenses

  • innate: general non-specific response to anything (generally larger extracellular things)

  • adaptive: responds to specific antigens (targeted response)

Innate immunity

• generalist immune response to any invader, including sensing wounds or trauma

• the immune system you are born with

• includes physical structures in the loosest definition (skin and mucous)

• activate general cells to attack invader and initate repair of damaged tissue

Adaptive immunity

• specficity: ability to recognize and attack specific cell types.

• memory: ability to remember cells that have invaded previously

• diversity: ability to respond to wide range of invasive organisms

• self-tolerance: ability to recognize and not attack self (e.g., auto-immune disorders)

Immune priming

• Insects do not have adaptive immunity, so no immunity for them.

• However, they exhibit something called immune priming , in which previous exposure to a pathogen upregulates their innate immune system, giving them a waning protection from exposure to similar pathogen challenges

Immune priming

_{Sułek et al. 2021 J Invert Path}

Immune priming can be transgenerational

_{Sułek et al. 2021 J Invert Path}

Some jargon before we dive into adaptive immunity

Antigen

• each pathogen generates multiple antigens, or molecule that stimulates an immune response

Antibodies

• immune molecules that bind to antigens

Self-antigens or autoantigens

• Thing that the body makes (totally normal), but that immune system responds to

• Leads to autoimmune disease

• You want your immune system to recognize outside attacks, but to be cool with the normal everyday stuff

Major histocompatiability complex

• labels foreign bodies for immune system to decide ‘self’ or ‘not self’

• reason why skin grafts and transplanted organs get rejected

• wide variation in MHC (2-3 people will share be close match out of every 100,000 people)

Variation in MHC

• There are hundreds of MHC alleles (MHC is fairly conserved across vertebrates, but allele frequency and copy number have changed)

• More helminths, more MHC gene copies (for birds)

_{Minias et al. 2020 Biol Letters}

The two branches of adaptive immunity

• Cell-mediated (intracellular)

• Humoral (extracellular)

Cell-mediated

• necessary to destroy pathogens within host cells

2 types of T-lymphocytes

• T-helper cells recognize antigens presented on surface of macrophages

  • Th1: assist with intracellular immunity

  • Th2: assist with extracellular immunity

• cytotoxic T-cells

  • bind and destroy infected host cells (also called “killer T-cells”)

Humoral

• attacks pathogen outside of host cells

• produced by B-cells (lymphocytes) activated by T-helper cells (Th2 response)

• activated B-cells also produce memory cells

• bind to antigens to block active sites

• agglutination: clumping of immune cells around pathogens

Major histocompatiability complex

Class 1: tagging intracellular pathogens

Class 2: tagging extracellular pathogens

What MHC class was that avian-helminth paper I referenced earlier focused on?

How effective is immune system at combating different types of parasites?

• complete removal and lasting immunity (classic microparasite response)

• partial control with longer-term persistence or reinfection (classic macroparasite)

• total failure to control pathogen (novel pathogens, immuncompromise)

Multiple challenges and tradeoffs

• Co-infection (being infected by two or more parasites at the same time) can be bad

• Mounting a Th1 (cell-mediated) and Th2 (humoral) response is demanding

• So challenges of a macroparasite and a microparasite might be worse off than two microparasites, right?

_{See work from Amy Pederson and Vanessa Ezenwa looking at some cool natural examples of coinfection}

Host resistance evolution

• Selective force is on the parasite to evolve ways to bypass host immune defenses

• Selective force is on the host to effectively respond to parasites

Definition of host resistance

• ability to prevent or limit parasite infection (inverse of susceptibility)

• ‘resistant’: rarely or never infected

• susceptible: commonly infected

• tolerance: perform well despite infection (in terms of survival/growth/reproduction)

Note that resistant is differently defined than how we previously talked about

• A resistant host is rarely infected, but when we talk about resistance-tolerance tradeoffs, it is assumed that the parasite has infected the host, and the host can respond to this in at least two ways; resistance or tolerance

• Try to keep this straight. Maybe even just think of ‘resistant’ as defined in the last slide as ‘not susceptible’ would probably be easier

Tolerance example

Low elevation birds had lower mortality and higher weight despite having higher parasitemia

resistance-tolerance tradeoffs

Imagine the host has a choice in how it can respond to a pathogen

Does the host focus on fighting the negative effects of pathogen?

Does the host focus on reducing damage of pathogen, allowing more focus on survival/growth/reproduction?

_{Not inherently a tradeoff, but often presented as such}

In what ways could this not be a tradeoff?

Parasite facilitation through host immune costs

One paper you read this week was from Ezenwa et al. Am Nat. This is a clear empirical demonstration of apparant facilitation between two coinfecting parasites (Tuberculosis and an intestinal helminth in African buffalo).

Anybody want to summarize this paper for the class?

Why don’t have more examples of evolution of host resistance?

Given strong selection, why don’t all hosts evolve resistance?

Tasmanian devil facial tumor disease

• Transmissible cancer from intraspecific interactions

“Genetic impoverishment has made the immune system blind”

_{Siddle et al. 2007 PNAS}

Does this disease follow frequency or density dependent transmission?

Why do the devils not mount an immune response?

• MHC in devils fails to recognize the cancer cells as foreign

So MHC is important, but there is also genetic variation in innate immunity

• This variation is important, and pathogen presence may shape the resulting genetic diversity of a given host population

• How would this work?

Strain-specific immunity

Costs of resistance

• Traits that confer resistance could lower other fitness components

• Some good papers on when these should occur and if they are even really a thing.

Cost = S fitness - R fitness

_{reviewed in Burrington 2000; good critique from Lenormand et al. 2018 Rethinking Ecology}

Costs of resistance versus cost of exposure

Costs of resistance: S - R
Costs of exposure: S - E

What happens when we do see the evolution of host resistance?

We tend to see the co-evolution of the parasite.

Red-queen dynamics: co-evolutionary arms race between host and parasite.

_{We went over this previously in week 2}

The importance of snail sex

In summary

• Hosts can proactively (grooming) or reactively (immune) respond to pathogen challenges

• Host individuals vary in their ability to respond, shaping genetic diversity

• Resistance and tolerance are two mechanisms for host responses to a pathogen, with varying outcomes