Consequences of inbreeding on invertebrate host susceptibility to parasitic infection.
Extreme susceptibility of cotton-top tamarin (Saguinus oedipus) to viruses is hypothesized to result from their unusual lack of nucleotide sequence variation in the MHC class I loci (Watkins et al. 1991). Levels of trematode infection in fish are correlated with allozyme variability (Lively et al. 1990), and empirical evidence demonstrates that for a number of both plants and animals, host genotypes vary in susceptibility to pathogens (Blackwell 1985; Wakelin 1985; Burdon 1987; Malo and Skamene 1994; Severson et al. 1994; Strauss and Karban 1994). In examining the relative importance of plant host genetic variability per se versus host genotype, Strauss and Karban (1994) found that host genotype was an important determinant of thrip infestation level, whereas self versus outcrossed progeny did not vary in infestation. The study presented here examined the effect of increased homozygosity on parasite susceptibility, although we did not examine the direct genetic mechanisms responsible.
Correlations between host genetic variability and susceptibility may be taxonimically variable, certainly differences may exist between plants and animals and even within the animal kingdom between vertebrates and invetebrates. Invertebrates lack an adaptive immune response, that is, the production of highly specific antibiodies through gene segment recombination and somatic mutations. Insect immune systems have two components, biochemical and cellular (Miller et al. 1996). Perhaps the best studied immune biochemicals are the proteins produced in response to bacterial infections, whereas cellular responses include phagocytosis, nodulation, and encapsulation.
We examined the effect of insect host genotype and host genetic variability on susceptibility to a tapeworm parasite by comparing parasitism among 31 inbred Tribolium lineages and their ancestral population that was continuously maintained with a large population size. The host strain had not been exposed to the parasite for at least 70 generations prior to our experiment. Thus, we investigate the relationship between host heterozygosity and host genotype on parasite susceptibility in the absence of coevolution between host and parasite.
There is extensive evidence for the deleterious consequences of inbreeding in both plants and animals (e.g., Charlesworth and Charlesworth 1987; Falconer and Mackay 1996). The causes of inbreeding depression are ambiguous, with two major hypotheses being: (1) the overdominance hypothesis, in which homozygosity per se reduces fitness; and (2) the dominance hypothesis, in which the exposure of deleterious recessive alleles causes inbreeding depression. Results from the cSM strain of the flour beetle Tribolium castaneum, the host used in the present study, suggest inbreeding depression is a mix of these two phenomena (Pray et al. 1994; Pray and Goodnight 1995, 1997; Pray 1997). Using the same inbred lineages as the present study, Pray and Goodnight (1995) found inbreeding depression to be genetically variable. Five of seven traits showed inbreeding depression (egg-to-adult viability, female and male relative fitness, female and male adult dry weight); two traits (male and female development time) did not. Although the overall trend was toward decreased fitness, lineages from the same ancestral population show genetic variation for inbreeding depression, with some increasing in fitness following inbreeding. Inbreeding depression in one environment cannot predict the level of inbreeding depression in another environment (Pray et al. 1994). There is a significant genotype-by-environment interaction for inbreeding depression for both males and females measured as a difference in rank fitness order of lineages between environments. The knowledge about inbreeding depression and infection with the tapeworm parasite in its recent history makes cSM strain a unique asset in a genetic study of invertebrate parasite susceptibility.
The genetic basis of susceptibility and the relationship between parasite loads and genetic variability are of general interest to evolutionary biologists because parasites are widespread and effective agents of natural selection. Studies on the genetics of interactions between hosts and pathogens are a starting point to understanding the influence of inbreeding on infection patterns (e.g., Burdon 1987; Parker 1990; Frank 1992, 1994); however specific theory that considers the effect of inbreeding on susceptibility is lacking. Parasites can result in evolutionary change by affecting overall levels of genetic variation as well as allele frequencies in a population. Parasite-induced mortality reduces population size and thus can reduce overall genetic variability through genetic drift. Alternately frequency-dependent selection resulting from parasites preferentially infecting the more common host genotype can increase genetic variation. When susceptibility to parasites is determined by recessive alleles (Severson et al. 1994, 1995; Vernick et al. 1995), parasite-imposed selection may result in increased frequency of the alleles coding for resistance. However, fitness costs associated with resistance (e.g., May and Anderson 1983; Ferdig et al. 1993; Simms and Triplett 1994) may prevent fixation of resistant alleles in a population. Stable equilibria with both susceptible and resistant alleles present may result from the interaction of the negative fitness effect of parasite infection and fitness costs associated with resistance. Thus, both the pattern of genetic variation for parasite susceptibility and the relationship between susceptibility and homozygosity will determine whether postselection populations have more or less genetic variation and are more or less susceptible to infection.
Conservation biologists are particularly concerned with the relationship between inbreeding and parasite susceptibility because endangered and threatened species often have reduced population size, which result in inbreeding. Information on the relationship between inbreeding and parasitism is particularly useful when species are being "genetically" managed through captive breeding programs (e.g., Templeton and Read 1984; Hughes 1991; Vrijenhoek and Leberg 1991). Most of the literature on genetic variation and parasite susceptibility deals exclusively with vertebrates. Because there are vast immune system differences between mammals and insects, the mammal data may not provide appropriate information about the effects of inbreeding on insect parasite susceptibility. Insect species do undergo events reducing population size and thus total genetic variation; however, because bottlenecks convert nonadditive genetic variation into additive variation, their effects on phenotypes might not be straight-forward (Bryant and Meffert 1988; Goodnight 1988). To help understand the consequences of such population bottlenecks, we empirically examined the relationship between inbreeding and susceptibility using an insect-tapeworm host-parasite model system.
The experiment described below addresses three questions: (1) Does decreased host genetic variability increase parasite susceptibility? (2) Is there genetic variation for parasite susceptibility? (3) Is the fitness of uninfected hosts related to their susceptibility, for example, is there either a cost of resistance or is susceptibility related to overall vigor?
MATERIALS AND METHODS
The host was the cSM strain of the red flour beetle, T. castaneum (Wade 1977). The parasite was the rat tapeworm, Hymenolepis diminuta. Much is known of the effect of this parasite on Tribolium beetles, including the effect of the parasite on "total" fitness (Yan and Stevens 1995; Yan 1997) as well as individual components (Keymer and Anderson 1979; Keymer 1980; Maema 1986; Yan and Stevens 1995). The effect on fitness is influenced by infection intensity and host environment (Yan and Stevens 1995; Yan 1997). Tribolium castaneum is a natural intermediate host of H. diminuta; however, infection intensities and prevalence have not been examined in natural populations. Thirty-one inbred lineages were derived by five generations of full-sib mating from a single stock population ([ILLUSTRATION FOR FIGURE 1 OMITTED]; Pray et al. 1994; Pray and Goodnight 1995). Using standard quantitative genetic convention, we assumed F = 0 for the ancestral population and the inbreeding coefficient of the 31 inbred lineages, F = 0.67, reflects their inbreeding relative to the ancestral population (Wright 1922). Adults were infected as described in Yan and Stevens (1995). Fresh rat feces infected with H. diminuta eggs were obtained from Carolina Biological Supply Co., Burlington, North Carolina. (Carolina has maintained rats infected with the tapeworm for the past 25 years.) The rat feces were collected from a cage of four infected rats within eight hours of deposition (Carolina Biological Supply Co., pers. comm.). The beetles were exposed to the tapeworm eggs within 48 hours of deposition. A single batch of tapeworm eggs was used to infect all the beetles in this experiment, and all beetles were infected concurrently. Hosts were maintained in 25 X 95 mm shell vials as single-sex groups of 10 beetles. Prior to exposure to rat feces, beetles were starved for one week. At the age of four weeks posteclosion, the beetles were exposed to 0.3 g of infected rat feces mixed with 0.2 g of distilled water on a 2 x 6.5 mm strip of filter paper for 24 hours. The feces were stirred to increase homogeneity before they were pasted to the filter paper. In addition, we randomized vials containing beetles to diminish the effects of uneven distribution of tapeworm eggs (Yan and Norman 1995). Because the vial effect is random with respect to lineage and sex, the heterogeneity of the vials is accounted for in the observed among-lineage and between-sex variation. Yan and Norman (1995) reported a marginally significant vial effect (P = 0.045) using a similar experimental design but with a larger number (20) of beetles per vial. F-values for the effects of sex, strain, and species were three, eight, and 250 times larger, and their associated probabilities were 1/3 to 1/500 those of the vial effect. Therefore, any vial effect would not nullify the observed variation in susceptibility to the tapeworm infection. Estimates of prevalence are particularly sensitive to sample size. Because of the unequal and small number of vials per lineage, the reduced number of beetles per vial, and previous results that sex and strain effects were much larger than vial effects, we did not test for a vial effect. After 24 hours the filter paper was removed and beetles were exposed to a fresh mixture of infected rat feces and distilled water on filter paper. The second filter paper was removed after 24 hours and 8 g flour medium (95% by weight fine sifted whole wheat flour plus 5% dried powdered brewer's yeast) was added to each vial. In two weeks when the tapeworm eggs had developed into cysticercoids, the beetles were dissected and the number of cysticercoids in each host recorded.
Two measures of parasitism, prevalence and infection intensity, were used to examine different aspects of parasite susceptibility. Prevalence is the proportion of hosts infected and measures the overall tendency to become parasitized. Once parasitized, a particular host may harbor few or several parasites. Infection intensity, defined as the number of parasites per infected host, measures the severity of individual parasite infections. In calculating infection intensity, only parasitized hosts are considered. We use the terms parasitism and susceptibility as more general terms. Tapeworm infection reduces fitness, and in cSM females, the fitness cost is correlated with infection intensity (Yan 1997).
Statistical analyses were done using the JMP[R] statistical software package (SAS Institute 1995). Only lineages with two or more beetles of each sex were included in the analyses. Lineages included in the prevalence analysis had at least two beetles. Inclusion in the intensity measure required at least two infected beetles. Thus, two of the 31 lineages (lines 35 and 46) were included in the prevalence dataset but not in the intensity analyses. The average and total sample sizes per lineage were for females: prevalence average = 24.2, total = 750; intensity average = 13.6, total = 394; for males: prevalence average = 27.1, total = 786; intensity average = 18.9, total = 548. Seventy percent of the males became infected [TABULAR DATA FOR TABLE 1 OMITTED] but only 53% of the females. We compared males and females to determine whether this difference was statistically significant. Female and male beetles differ in behavioral responses to the tapeworm infection (Yan et al. 1994) and fitness consequences of parasite infection (Yan and Stevens 1995; Yan 1997). Intensity data were natural log-transformed to improve normality. Means were back-transformed for presentation.
The two measures of infection, prevalence and intensity, were significantly correlated among the inbred strains for both sexes (Table 1A). Relative fitness for females from each inbred lineage (except lineage 9) in generation t - 1 (where t represents the generation in which parasitism was assayed; [ILLUSTRATION FOR FIGURE 1 OMITTED]) was reported in an earlier paper (Pray and Goodnight 1995). Two females from each lineage were assayed. For both sexes, we tested for a correlation between female fitness and parasite susceptibility. Note that we are comparing the fitness of females with the tendency of the lineage to become infected. In each case the correlation was not statistically significant (Table 1B,C). Fitness measured in the absence of parasites is not correlated with susceptibility or prevalence.
Males had significantly higher prevalence than females in both the stock population (Table 2A) and inbred lineages (Table 2E). Infection intensities were not significantly different between males and females from the stock population (Table 2B); however inbred females had higher infection intensities [TABULAR DATA FOR TABLE 2 OMITTED] than inbred males (Table 2F). To examine the mean response to inbreeding, we compared the average of the inbred lineages with the ancestral population using ANOVA followed by Dunnett's test to determine whether individual inbred lineages are significantly more or less susceptible than the ancestral stock population. Dunnett's test controls for multiple comparisons and considers the sample size of each lineage, thus inbred lineages with low variance and small sample size (e.g., three infected beetles) are not statistically significantly different from the noninbred stock population (SAS Institute 1995).
ANOVA indicates that inbreeding resulted in significant differences in prevalence and infection intensity among the ancestral stock population and inbred lineages (Table 2C, D). Figure 2 shows the mean prevalence and intensity by lineage for each sex. Lineages significantly different from the ancestral population as indicated by Dunnett's test are circled. For prevalence in females [ILLUSTRATION FOR FIGURE 2A OMITTED] two lineages (6, mean = 0.79; 28, mean = 0.13) were significant (ancestral population mean = 0.56). Note that one of the inbred lineages was significantly more susceptible and the other less. There were no significant differences among females in infection intensity [ILLUSTRATION FOR FIGURE 2C OMITTED].
Among the males, with respect to prevalence, four lineages (11, mean = 0.23; 17, mean = 0.43; 28, mean = 0.31; 42, mean = 0.42) were significantly different from the control (mean = 0.74; [ILLUSTRATION FOR FIGURE 2B OMITTED]). Two of these same lineages were significantly different in terms of intensity ([ILLUSTRATION FOR FIGURE 2D OMITTED]; 17, mean = 1.43; 28, mean = 1.92; control, mean = 4.08). With males the significant differences are all toward lower susceptibility. The lineage that decreased in female prevalence was also significantly different for both measures of parasitism in males.
Because we have replicate inbred lineages we can examine both the mean and the variance in the effect of inbreeding on parasite susceptibility. To examine the variance in the response to inbreeding, we considered only the inbred lineages, excluding the ancestral population, and performed the likelihood-ratio [[Chi].sup.2] test on both sexes and both measures of parasitism. There is significant variation among the inbred lineages for both sexes in both prevalence and infection intensity (Table 2E,F). This result adds the information that even though no lineages are significantly different from the ancestral population in female infection intensity, there are significant differences among the lineages in this parasitism measure as well as the other three measures.
Our experiment used a fairly high level of inbreeding (F = 0.67) and did not detect an overall decrease in parasite resistance among inbred lineages as has been hypothesized. For two closely related hosts Tenebrio molitor and Tenebrio obscurus, reports of infection intensities in natural populations are 10.5 and 82.3, respectively, and prevalence is 47% and 88% (Rau 1979). Considering the sizes of these hosts (T. castaneum, 4.0-4.5 mm; T. molitor, 13-16 mm; T. obscurus, 14-17 mm; Blatchley 1910) our parasite loads from laboratory infections are probably within natural ranges. We found the average effect of inbreeding varies between sexes and depends on the measure of susceptibility. Inbreeding affected the tendency to become infected (prevalence); however, among those individuals that became infected, inbred beetles did not have significantly different infection intensities than noninbred individuals. Inbred females showed significantly higher prevalence than beetles from the ancestral population. In contrast to what is commonly predicted, inbred males showed significantly lower prevalence of tapeworm infection than noninbred beetles.
Inbreeding changes parasite susceptibility on average, but there is significant among-lineage variation with the result that generalizations about the effect of inbreeding on parasite susceptibility cannot be made, For both sexes there was highly significant variation among the inbred lineages in both prevalence and infection intensity. Some lineages became more sensitive to parasites through inbreeding, and some became less. More lineages differ from the ancestral population with respect to prevalence than intensity, and males were more likely to be affected by inbreeding than females. These differences may reflect differences in sensitivity to inbreeding depression. In addition, prevalence may be more genetically variable than intensity.
In contrast to prior expectation, most lineages that differed from the ancestral population were significantly less susceptible to parasitism, although some inbred lineages were significantly more susceptible. Prevalence in males from the stock population was so high (0.74) that it is unlikely we could detect higher prevalence in an inbred lineage. However, there is no restriction on intensity, and none of the male lineages is significantly higher in infection intensity. This supports the conclusion that, in contrast to prior expectation, inbreeding lowers parasitism in males. Finally, the lack of correlation between fitness and prevalence or infection intensity shows that susceptibility is not related to inbreeding depression as measured by Pray and Goodnight (1995). The inbred lineages do show substantial inbreeding depression. The relative fitness of inbred lineages ([w.sub.i]) to the control ([w.sub.c]) is [w.sub.i]/[w.sub.c] = 0.74. Thus, parasite susceptibility is not necessarily a manifestation of inbreeding depression.
Parasite susceptibility can be a combination of behavioral, physiological, and ecological traits. The genetic basis can include a single gene with large effect for the appeal of parasite eggs to feeding beetles or the ability of parasite eggs to penetrate the gut lining and move into the hemocoel. Polymorphism in the stock population for a simple genetic basis could result in fixed allelic differences among the inbred lineages yielding significant among-lineage variation and some significant differences from the ancestral population. Ewald (1994) argued for more attention to the role of ecology and, in particular, transmission dynamics in host parasite biology. Although Ewald mainly discussed vertebrates and humans, his ideas have been extended to include invertebrates (Myers and Rothman 1995). Previous studies with Tribolium-Hymenolepis system suggest host ecology and behavior affect parasite susceptibility (e.g., Yan et al. 1994; Yan and Stevens 1995). Beetles need to encounter and ingest eggs to become parasitized. More active beetles may encounter more macroparasites and thus have higher rates of parasitism. Tribolium emigration rate, a measure of activity level, and prevalence are positively correlated (Yan et al. 1994). Thus, inbreeding could affect parasitism indirectly by modifying behaviors that are correlated with parasite susceptibility. Data on the genetics of susceptibility and effect of inbreeding on either activity level or our measure of emigration rate are necessary to establish this for our system. It is likely that the ancestral population was polymorphic for genes affecting parasite susceptibility and genetic drift through inbreeding altered allele frequencies. Discerning between the possibilities of a major gene or several minor genes requires further experimentation.
Evidence from other studies corroborates the observed sex difference in both parasite susceptibility (e.g., Yan and Norman 1995) and the response to inbreeding. Pray and Goodnight (1995, experiment 2) reported male relative fitness was more sensitive to inbreeding depression than that of females. Our results are consistent with this observation in that we also found male parasitism to be more responsive to inbreeding. Male Drosophila melanogaster also appear to be more sensitive to inbreeding (Miller and Hedrick 1993). The sex difference suggests that even if there is a simple genetic basis to parasite susceptibility, sex-dependent factors modify its expression. Further study is required to understand this observation.
Our results may be of interest to conservation biologists working with inbred species or populations. The conservation literature to date has dealt mostly with vertebrates, and mammals in particular, reflecting the sentiment that "conservation ethic applied differently to different taxonomic groups" (Dobson and May 1986, p. 345). Our results stress the need to recognize taxonomic-level differences in developing conservation strategies. There are important immune system differences between vertebrate and invertebrate hosts. Vertebrate immune systems are well developed and involve complex systems such as MHC and several other genes specifically identified for their role in resistance (Malo and Skamene 1994). The complexity of insect immune systems is just beginning to be appreciated (Stanley-Samuelson and Webb 1996), and genetic differences influencing susceptibility have been identified (e.g., Severson et al. 1994). The genetic basis of parasite susceptibility as well as ecology, physiology, and behavior interact to determine parasite loads These factors contribute to immune system differences and may explain why our beetles did not respond as predicted based on vertebrate biology. An alternative explanation is that a correlation between parasite susceptibility and heterozygosity does not in fact exist. Caughley (1994, p. 234) suggests a correlation between homozygosity and susceptibility may not be accurate even for mammals and suggests that "establishing a link between susceptibility to disease and heterozygosity requires more disciplined data." Our more disciplined data with a relatively high amount of inbreeding (F = 0.67) and inbreeding depression ([w.sub.i]/[w.sub.c] = 0.74) do not support the link.
The invertebrate host Tribolium flour beetles do not follow the predicted relationship between inbreeding and parasite susceptibility. Our results should not be taken as evidence that the relationship is not important for vertebrate populations; rather, that taxonomic-level considerations with respect to disease as a potential threat need to be considered. Our results suggest genetics, as well as ecology and behavior, are important factors in invertebrate parasite susceptibility.
We thank K. S. Omland for help with the dissections, C. J. Goodnight for suggestions on the statistical analyses, L. and S. Stevens-Goodnight for an excellent job of enlivening the lab, and R. Fialho, J. M. Schwartz, L. Meffert and an anonymous reviewer for comments on the manuscript. This research was supported by National Science Foundation grant BSR-9209695 to LS, a Sigma Xi grant to YG, and National Science Foundation grant DEB-9321689 to LAP.
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|Author:||Stevens, Lori; Yan, Guiyun; Pray, Leslie A.|
|Date:||Dec 1, 1997|
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