Chapter Three – Host–Parasite Interactions and the Evolution of Immune Defense

Parasites and pathogens are ubiquitous and act as an important selection pressure on animals. Here, drawing primarily on our own research, mostly on insects, we illustrate how host-parasite interactions have played a role in the evolution of a range of phenomena, including animal coloration, social behavior, foraging ecology, sexual selection, and life-history tradeoffs, as well as how variation in host behavior and ecology can drive variation in parasitism risk and host allocation of resources to immunity and other antiparasite defenses. We conclude by identifying key areas for future study.

Parasite neuropeptide biology:Seeding rational drug target selection?

The rationale for identifying drug targets within helminth neuromuscular signalling systems is based on the premise that adequate nerve and muscle function is essential for many of the key behavioural determinants of helminth parasitism, including sensory perception/host location, invasion, locomotion/orientation, attachment, feeding and reproduction. This premise is validated by the tendency of current anthelmintics to act on classical neurotransmitter-gated ion channels present on helminth nerve and/or muscle, yielding therapeutic endpoints associated with paralysis and/or death. Supplementary to classical neurotransmitters, helminth nervous systems are peptide-rich and encompass associated biosynthetic and signal transduction components - putative drug targets that remain to be exploited by anthelmintic chemotherapy. At this time, no neuropeptide system-targeting lead compounds have been reported, and given that our basic knowledge of neuropeptide biology in parasitic helminths remains inadequate, the short-term prospects for such drugs remain poor. Here, we review current knowledge of neuropeptide signalling in Nematoda and Platyhelminthes, and highlight a suite of 19 protein families that yield deleterious phenotypes in helminth reverse genetics screens. We suggest that orthologues of some of these peptidergic signalling components represent appealing therapeutic targets in parasitic helminths.

Eaten alive: cannibalism is enhanced by parasites.

Cannibalism is ubiquitous in nature and especially pervasive in consumers with stage-specific resource utilization in resource-limited environments. Cannibalism is thus influential in the structure and functioning of biological communities. Parasites are also pervasive in nature and, we hypothesize, might affect cannibalism since infection can alter host foraging behaviour. We investigated the effects of a common parasite, the microsporidian Pleistophora mulleri, on the cannibalism rate of its host, the freshwater amphipod Gammarus duebeni celticus. Parasitic infection increased the rate of cannibalism by adults towards uninfected juvenile conspecifics, as measured by adult functional responses, that is, the rate of resource uptake as a function of resource density. This may reflect the increased metabolic requirements of the host as driven by the parasite. Furthermore, when presented with a choice, uninfected adults preferred to cannibalize uninfected rather than infected juvenile conspecifics, probably reflecting selection pressure to avoid the risk of parasite acquisition. By contrast, infected adults were indiscriminate with respect to infection status of their victims, probably owing to metabolic costs of infection and the lack of risk as the cannibals were already infected. Thus parasitism, by enhancing cannibalism rates, may have previously unrecognized effects on stage structure and population dynamics for cannibalistic species and may also act as a selective pressure leading to changes in resource use.

Home-range size in juveniles of the temperate reef fish, the common triplefin (Forsterygion lapillum)

An organism’s home range dictates the spatial scale on which important processes occur (e.g. competition and predation) and directly affects the relationship between individual fitness and local habitat quality. Many reef fish species have very restricted home ranges after settlement and, here, we quantify home-range size in juveniles of a widespread and abundant reef fish in New Zealand, the common triplefin (Forsterygion lapillum). We conducted visual observations on 49 juveniles (mean size = 35-mm total length) within the Wellington harbour, New Zealand. Home ranges were extremely small, 0.053 m2 ± 0.029 (mean ± s.d.) and were unaffected by adult density, body size or substrate composition. A regression tree indicated that home-range size sharply decreased ~4.5 juveniles m–2 and a linear mixed model confirmed that home-range sizes in high-density areas (>4.5 juveniles m–2) were significantly smaller (34%) than those in low-density areas (after accounting for a significant effect of fish movement on our home-range estimates). Our results suggest that conspecific density may have negative and non-linear effects on home-range size, which could shape the spatial distribution of juveniles within a population, as well as influence individual fitness across local density gradients.

Temperament test for re-homed dogs validated through direct behavioral observation in shelter and home environment

This study was the first attempt to carry out a validation of a temperament test (TT) for shelter dogs that addressed the topics of inter- and intra-raters agreements, test-retest reliability, and validity. The TT consisted of 22 subtests. Each dog was approached and handled by an unfamiliar person and made to interact with a same- and an opposite-gender conspecific. Dogs were tested twice in the shelter and once in their new homes 4 months after adoption to evaluate consistency in behavioral assessment. Playfulness, trainability, problem solving abilities, food possessiveness, and reactivity to sudden stimuli were also evaluated. Testers scored dogs' responses in terms of confidence, fearfulness, and aggressiveness. Results highlighted strengths and limits of this TT that was devised to help shelter staff in matching dogs' personality and owners' expectations. Methodological constraints when working with sheltered dogs are unavoidable; however, the test proved to be overall feasible, reliable, and valid although further studies are needed to address the critical issues that emerged. © 2011 Elsevier Inc.

Laterality as an indicator of emotional stress in ewes and lambs during a separation test

We assessed motor laterality in sheep to explore species-specific brain hemi-field dominance and how this could be affected by genetic or developmental factors. Further, we investigated whether directionality and strength of laterality could be linked to emotional stress in ewes and their lambs during partial separation. Forty-three ewes and their singleton lambs were scored on the (left/right) direction of turn in a y-maze to rejoin a conspecific (laterality test). Further, their behavioural response (i.e. time spent near the fence, vocalisations, and activity level) during forced separation by an open-mesh fence was assessed (separation test). Individual laterality was recorded for 44.2 % ewes (significant right bias) and 81.4 % lambs (equally biased to the left and the right). There was no significant association in side bias between dams and offspring. The Chi-squared test revealed a significant population bias for both groups (p < 0.05). Evolutionary adaptive strategies or stimuli-related visual laterality may provide explanation for this decision-making process. Absolute strength of laterality (irrespective of side) was high (Kolmogorov–Smirnov test, dams: D = 0.2; p < 0.001; lambs: D = 0.36, p < 0.0001). The Wilcoxon test showed that lateralised lambs and dams spent significantly more time near each other during separation than non-lateralised animals (p < 0.05), and that lateralised dams were also more active than non-lateralised ones. Arguably, the lateralised animals showed a greater attraction to their pair because they were more disturbed and thus required greater reassurance. The data show that measures of laterality offer a potential novel non-invasive indicator of separation stress.

Reproductive success of parasitized males in a marine reef fish

Parasitism is hypothesized to reduce reproductive success in heavily parasitized males because females
may preferentially mate with less parasitized males (parasite-mediated sexual selection) or parasites may compromise
male competitiveness. In marine systems, this hypothesis is largely unexplored. This paper provides the first confirmed record of a copepod ectoparasite (Caligus buechlerae Hewitt 1964) on the common triplefin (Forsterygion lapillum) and evaluates the hypothesis that males parasitized with C. buechlerae experience lower reproductive success than unparasitized males (as determined
by the presence and area of eggs within male nests). We found that 38 % of males we surveyed were infected with
at least one C. buechlerae, with a median of two individuals per infected male. About 32 % of males were defending
eggs, with 62.5 % of those males infected with at least one parasite. Males of greater total length (TL) were both
more likely to be infected and more likely to be defending eggs. However, when statistically accounting for the effects
of TL, parasite infection had no effect on the probability of defending eggs, or the average surface area of eggs when
present. Positive covariation in fish length, the presence of eggs and parasite infection observed here potentially suggest
that the importance of parasitic infection on reproductive success may depend upon the strength of selection for larger male body size. Our study is one of the few studies to investigate the effects of ectoparasites on reproductive success in reef fish and also provides a quantitative measure of infection for a widespread species within New Zealand.