Coevolution:

1. Coevolution: a pattern of reciprocal adaptation, caused by two species evolving in close association. coevolution is a change in the genetic composition of one species (or group) in response to a genetic change in another. More generally, the idea of some reciprocal evolutionary change in interacting species is a strict definition of coevolution

2. Coevolution, Coexistence, Conflict ? Conventional thought: the good, or better adapted, parasite does not unduly harm its host. Any exceptions can be viewed as new or more recent associations compared with benign interactions Therefore are all the parasites we have seen new associations? When hosts encounter “harmful” parasites, that drain resources and take actions to counter the effect of the parasites- is this peaceful coexistence or a stalemate? Should the relationship develop towards commensalism- or can a certain level of pathogenicity be tolerated?

3. R0: The basic reproductive rate The fundamental epidemiological quantity R0 represents the average number of secondary infections generated by one primary case in a susceptible population Can be used to estimate the level of immunization or behavioural change required to control an epidemic R0 = βH α + µ + b β =transmission rate, H= number of hosts α = parasite induced host mortality (a measure of virulence) µ= parasite mortality rate within the host, b=natural host death

4. Parasite-imposed and host-imposed selection can operate together in determining features of parasite-host interactions. Parasite virulence can incur costs for parasite and host- if parasites incur too much suffering on their hosts. Anderson and May: R0= βH α + µ + b Parasite net reproductive rate (R0) and virulence (α) are inversely related If parasite virulence brings no benefit to parasite, there is nothing to stop virulence from evolving to zero (commensalism) or even a positive relationship (mutualism). If the parameters were independent of each other the predictions derived in this equation would suggest that parasites to become benign.

5. Lizard malaria reduces clutch size. Infected males interact less with females and other males, results in maintenance of inferior territories, decreased ability to compete for females, inability to attract females. Infection may be associated with significant reduction in fitness, although no direct effect on survival.

6. Genetically controlled resistance mechanisms also have a cost: 1) Immune responses may be harmful themselves 2) Structures for passive immunity or infrastructure for a response (thymus and spleen) are expensive to produce and maintain 3) Mounting an immune response may be energetically expensive Examine a scenario: R and S hosts in the presence and absence of a parasite 1) Parasite present: R hosts should be fitter 2) Parasite absent: ?? Is R cost fixed or facultative? What are the costs for developing an immune response? Does this depend on the probability of encountering a parasite or the costs of having a parasite?

7. Hypothetical differences in reproductive success between R and S hosts in the presence and absence of parasites. A-D differ in whether the costs are paid regardless of the presence of parasites (fixed) or only in the presence of parasites (facultative)

8. Digenean infections of snails: Snails are castrated: physiologically or physically Selected snails to be S or R to a parasite: R snails + parasite S snails + parasite R snails – parasite S snails – parasite Reproductive costs are paid by S snails - castrated Reproductive costs are paid by R snails whether or not the parasite is present

9. Questions: How do parasites and hosts evolve? Do parasites evolve to lose virulence? Should they? Do parasites cause less disease because hosts mount counter measures? Are we in an arm’s race or in a negotiated settlement? Can the parasite increase virulence and the host increase defences indefinitely? Can this continue forever? Should parasites be virulent or avirulent? Can Virulence be altered easily…. or predictably, or on a regular pattern?

10. Parasite virulence can incur costs for parasite and host- if parasites incur too much suffering on their hosts. Anderson and May: R0 = βH α + µ + b α = parasite induced host mortality (a measure of virulence) Parasite net reproductive rate (R0) and virulence (α) are inversely related If parasite virulence brings no benefit to parasite, there is nothing to stop virulence from evolving to zero (commensalism) or even a positive relationship (mutualism) Link between virulence and increased fitness is transmission.

11. If killing your parasites is expensive in terms of energy BUT your parasites castrate you: Where does the cost-benefit analysis kick in? When is it better to expend large amounts of energy and when not? Allocation of resources in mounting a strong response to a parasite may reduce fitness. However the return- (survival, long term reproductive output) should be justified even if it costs other fitness components. = priority scheme = tradeoffs.

12. Trade offs are linkages between traits that constrain the simultaneous evolution of two or more traits. Physiological trade offs: energy allocations between ≥2 functions requiring the same energy Evolutionary trade offs: are identified by manipulation experiments on phenotype and by observed responses to selections on populations. The effects of mating on longevity, fecundity on parental survival, Reproduction on growth, offspring size vs offspring number Some costs and benefits of high reproductive rates are known. Improved prospects for transmission would be positive (unless all parasites were successful- host killed) If a parasite can kill its host then for a stable situation, overinfection should be avoided

13. In evolutionary biology a trade-off between two traits is said to occur when an increase in fitness due to a change in one trait is opposed by a decrease in fitness due to a concomitant change in the second trait. The belief that evolutionary change is modulated and constrained by such trade-offs is a central pillar of evolutionary thought. The existence of trade-offs is not disputed, but there is still relatively little understanding of how trade-offs evolve, or indeed if they can evolve.

14. Host Finding: How do you complete your life cycle? As a parasite, how can you increase your chances of transmission?

15. As a parasite- can you alter your behaviour or the behaviour of your host so as to get an advantage? If everything else is the equal, then an increase in transmission rate results in an increase in Ro. If parasites induce such behavioural differences, they may be favoured by natural selection. If this occurs then several aspects of parasite epidemiology- including host population levels required for their establishment may diverge from those predicted in models.

16. Altered host behaviour can be found in direct and indirect life cycles, and there are many transmission modes. Many involve predation on intermediate hosts, direct transmission, or vector transmission. • The most dramatic is the ingestion of the intermediate host: when predators eat the int. host- the cost to that int. host is very high. • Demonstrating the effect of altered behaviour on transmission is not easy, representatives of every major taxon of predation-transmitted parasites have been shown to enhance the risk of predation of the int. hosts. • Gastropods infected with digeneans may behave differently • Vectors infected with Plasmodia may feed differently • If this increases transmission, then Ro for these parasites will be greater than if contact with their hosts was random • But can we prove that these behavioural modifications • actually increase transmission or • 2) are “designed” to increase transmission

17. Parasite effects on host behavior General issues Extending "fitness effects of parasites on hosts" beyond simple mortality or decrease in fecundity. Just as in the case of virulence and resistance, we have to figure out which behavioral aspects of the host in the presence of the parasite are caused by the parasite, which are caused by the host, and which are accidental.

18. Parasites “wish” to increase their fitness by inducing host activities that allow them to interact with potential hosts. Host Space: defined by the ecological requirements of the host Host Time: parasite emergence/existence should be timed to coincide with the presence of a suitable host (examples: cercariae from snails infected with Schistosoma at noon- humans, night:rats. May be induced by photoperiod, host signals, etc) Adaptive value: enhance parasite transmission in placing the short-lived cercariae in the Host space and Host Time Should cercariae that penetrate hosts have a defined pattern? Should cercariae that encyst on vegetation have a defined pattern or a general emission from the snail host?

19. Categories of behavioral change Change in activity (up or down): reduction in speed/distance travelled/etc. (mice with Trichinella), increased activity, exploration etc.: increased predation (have to be careful to test whether behavior leads to parasitism, rather than vice versa) Many examples of changes in fish behavior Acanthocephalans in invertebrates (good to test difference in activity patterns rather than just increase/decrease, which can be caused by pathology) Vectors can be affected: fly less (mosquitoes with filaria) or bite more, or change host preferences Conspicuous behavior: height-seeking behavior: fish, ants side effect of pathology (e.g. hypoxia in fish)? photophilia, heat-seeking behavior: "behavioral fever" (Hart, 1988; Boorstein and Ewald, 1987; McClain et al 1988). changes in color, changes in size Changes in social behavior: castration, changes in mating behavior (host or parasite or compensation?), changes in dominance; do parasites drive host social behavior (group size, etc.)?

20. Testing hypotheses about parasite-induced behavior changes Testing behavioral changes Host behavioral changes in the presence of parasites are relatively easy to document, and relatively well documented. One caveat, though, is that ecological (correlational) studies might get the direction of causality wrong: do hosts change their behavior when they are infected, or are they more likely to be infected if they behave in a certain way? Possible solutions are: laboratory studies of infection; before-and-after studies of individuals; parasitized behaviors that are completely outside the range of unparasitized behavior (although this may still overestimate the size of behavior changes).

21. Testing effects on host and parasite fitness A common assumption is that host behavior changes are driven by and for parasites, to increase parasite survivorship and transmission. However, their fitness consequences for the parasite or the host can be either positive, neutral, or negative: these behavioral changes can constitute adaptations by either the host or the parasite, or they can be "coincidental" side-effects of the host-parasite relationship. In many cases behavioral changes of hosts are side-effects of parasite pathology, or host reactions, and do not necessarily enhance parasite fitness. For example: increased predation rates of parasitized hosts (assumed to be an adaptation for transmission to the next host) is not necessarily by the right host. Parasites may select particular host organs (that have strong effects on host behavior) for reasons other than influencing host behavior. For example, parasites in host CNS tissues are often isolated from host defenses: `immunological privilege'. Behavioral changes may be host-driven, either as part of host defense or just as compensation for parasite-caused pathology. Behavioral changes can be completely coincidental (although if they affect parasite or host fitness in any way they should be subject to selection)

22. Beyond a certain point, it's very hard to disentangle causality evolution. For example, suppose a parasite species inhabits the CNS and changes host behavior. Is the parasite in the CNS to avoid host defenses, with changes in behavior being a coincidental result of tissue damage, or are they actively changing host behavior? Probably the best way to answer these questions is simply to look at the changes in parasite and host fitness. • Parasite fitness Host fitness Explanation • + (transmission) - Parasite manipulation • + (survivorship) 0/- Parasite site selection • (survivorship) + Host behavioral resistance • - (transmission) ? Host inclusive-fitness reactions? • 0/- - Host pathology? • 0/ ++ Host compensation • This field is famous for "just-so stories" - host behaviors that are just too weird and incredible to believe are anything but parasites driving their hosts to do things that enhance parasite fitness - but we have to figure out where and how to draw the line. Intuitively, behavioral changes that are complex and ones that we have a hard time explaining as simple pathogenic effects are the ones that we usually ascribe to parasite manipulation.

23. Transmission by intermediate hosts Immature stages of parasite ingested with intermediate host Amphipod intermediate hosts: uninfected amphipods avoid bright light, and burrowed if disturbed, to escape predators. Amphipods infected with juvenile Polymorphous paradoxus (acanthocephalan) demonstrated similar behaviour Amphipods infected with infective stages of the parasite showed behavioural changes: stayed in lighted areas, stayed at the surface, and grasped floating objects – eaten by ducks. Infected int. hosts eaten at 4 fold increase over uninfected int. hosts Behaviour only altered when parasite is infective. This is a case where if a parasite can kill, weaken, or derange its int. host it may be favoured by natural selection.

24. Transmission by vectors: Bloodfeeding insects that contain parasites in salivary glands may have trouble probing to get a blood meal- stay longer to feed, will jump off one host onto another This may lower fitness: vectors may not get enough nutrients, fecundity decreases, longer feeding means more danger Transmission to vectors: Enhanced transmission if host shows decreased defensive responses, increased attractiveness Lethargy: conserves energy- docile host more easily fed upon reduced defensive behaviour (slapping) reduces vector mortality

25. Transmission of parasite propagules: The right Place: In Aedes sierrensis: infected by a ciliate L. clarki: Mosquito induced to have behaviours that mimic oviposition: ciliate released into water- infects larvae The right Time: Emergence of cercariae from a snail to coincide with host presence Movement of microfilariae (Brugia malayi) from visceral to peripheral blood to coincide with the feeding behaviour of a suitable vector

26. Cercariae: Swim (energetically costly, reduces longevity) or stay (competition?) Swim=dispersal from habitat of first int. host Highly elaborate host finding is required Swim towards host signals How can parasite conserve energy- yet ensure it emerges to coincide with the presence of its next host? Bring a host to a site suitable for parasite emergence Make an intermediate host more susceptible to predation Interfere with the chemical communication in hosts- aberrant behaviour Evolutionary origins of host manipulation go back as far as the origins of complex life cycles: changing the existing conditions to favour your transmission would be favoured over conspecifics by natural selection.

28. The cercaria are released from the snails embedded in the snails mucus slime balls which form in the snails respiratory chamber and are eventually deposited on vegetation. Ants eat the slime balls. Within the ant most of the cercaria encyst in the ant's abdomen. However, one or two of the cercaria first undergo a migration to the head of the ant to the sub-oesophageal ganglion where they encyst. These metacercaria do not become infective but instead substantially alter the behaviour of the ant, such that when the temperature drops as evening approaches, the infected ants, instead of returning to their nests, climb to the top of the vegetation and clamp on to the leaves with their mandibles. They stay there immobile until the next morning. When the temperature warms up the ants then resume there normal behaviour. This very strange behaviour places the ants in a region where they are likely to be eaten by browsing herbivores.

29. "zombie ants".

30. Describe how this happens • Are some cercariae altruistic? How selected? • How would this have developed? • What benefits are there for brain metacercariae? • What costs are there for brain metacercariae? • What benefits are there for abdominal metacercariae? • What costs are there for abdominal metacercariae?

31. Can Parasites alter behaviour in other ways? Sex… Do parasites influence sex? Why do animals have sex? Can parasites affect mate selection? Can one gender determine the parasite status of a potential mate before deciding? males usually larger, more colorful, loud... typically costly in males