Role of chemical cues and natal rearing effect on host recognition by the parasitic wasp Melittobia digitata

Parasitoids are expected to have the ability to find, recognize, and perhaps to discern potential hosts that can best support the development of their progeny. Melittobia Westwood (Hymenoptera: Eulophidae) are gregarious ectoparasitoids, which primarily attack mud daubers (Hymenoptera: Sphecidae). How Melittobia females locate their host is not well known, but the process may involve host‐related chemical signals. In this study, we investigated the roles of host chemical cues and natal rearing effect in host recognition by Mel. digitata Dahms. In an olfactometer that contained prepupae of Trypoxylon politum Say (Hymenoptera: Sphecidae), Megachile rotundata (Fabricius) (Hymenoptera: Megachilidae), puparia of Neobellieria bullata (Parker) (Diptera: Sarcophagidae), empty or intact host cocoons, or nest mud, Mel. digitata females spent significantly more time in air fields that contained T. politum (prepupae + cocoon) and Meg. rotundata (prepupae + cocoon) than in N. bullata and control fields. Nest mud and natal host had no attraction for parasitoid host choice. Most first and last choices of Mel. digitata females in the olfactometer were not consistent, suggesting an initial random dispersion, although they responded positively towards hosts in cocoons.     

The origin and genetic differentiation of the socially parasitic aphid Tamalia inquilinus

Social and brood parasitisms are nonconsumptive forms of parasitism involving the exploitation of the colonies or nests of a host. Such parasites are often related to their hosts and may evolve in various ecological contexts, causing evolutionary constraints and opportunities for both parasites and their hosts. In extreme cases, patterns of diversification between social parasites and their hosts can be coupled, such that diversity of one is correlated with or even shapes the diversity of the other. Aphids in the genus Tamalia induce galls on North American manzanita (Arctostaphylos) and related shrubs (Arbutoideae) and are parasitized by nongalling social parasites or inquilines in the same genus. We used RNA sequencing to identify and generate new gene sequences for Tamalia and performed maximum‐likelihood, Bayesian and phylogeographic analyses to reconstruct the origins and patterns of diversity and host‐associated differentiation in the genus. Our results indicate that the Tamalia inquilines are monophyletic and closely related to their gall‐forming hosts on Arctostaphylos, supporting a previously proposed scenario for origins of these parasitic aphids. Unexpectedly, population structure and host‐plant‐associated differentiation were greater in the non‐gall‐inducing parasites than in their gall‐inducing hosts. RNA‐seq indicated contrasting patterns of gene expression between host aphids and parasites, and perhaps functional differences in host‐plant relationships. Our results suggest a mode of speciation in which host plants drive within‐guild diversification in insect hosts and their parasites. Shared host plants may be sufficient to promote the ecological diversification of a network of phytophagous insects and their parasites, as exemplified by Tamalia aphids.     

Survival, growth, and reproduction of two aphid species on sucrose solutions containing host or non-host honeydews

Aphids, like most phloem-feeding insects, commonly exhibit a high degree of host specificity. Plant-specific chemical compounds are likely to serve as important host selection cues for monophagous aphids and such substances could be present in aphid honeydew. Apterous virginoparae ofMyzus persicae (Sulzer) andPhorodon humuli (Schrank) were reared on a buffered sucrose solution containing various aphid honeydews or a mixture of amino acids. In two separate experiments, the host-specificP. humuli (hop aphid) could grow and reproduce only on diets containing honeydew collected from hop (Humulus lupulus L.).M. persicae (the green peach aphid, GPA) did not perform well on diets containing hop honeydew, perhaps because hop is a poor GPA host. Honeydew collected from preferred GPA host plants rape,Brassica napus L., and jimsonweed,Datura stramonium L., allowed GPA growth and reproduction. Hop aphids, however, performed poorly on rape and jimsonweed honeydew diets. Bell pepper,Capsicum annuum L., honeydew supported neither the hop aphid nor GPA. The study of aphid honeydew components may contribute towards a more complete understanding of host preference and selection phenomena in aphids.     

The hosts of Nemeritis canescens a problem in the host specificity of insect parasitoids

• 1 Published records of the hosts of N.canescens have been collected and critically examined.
• 2 It is accepted that canescens has developed on twenty-three species; on one of them perhaps accidentally, on two with some doubt.
• 3 Twelve species were parasitized in nature; nine species in the laboratory. Two species served as hosts when artificially infected.
• 4 The natural hosts belong in the Pyralidae, Tinaeidae and Yponomeutidae; the laboratory hosts in the Pyralidae, Oecophoridae and Gelechiidae. One individual was reared from a Tortricid, perhaps accidentally.
• 5 The host specificity of N.canescens is not easily explained on either a systematic or an ecological basis. It offers interesting problems for research.

     

Divergence before the host shift? Prezygotic reproductive isolation among three varieties of a specialist fly on a single host plant

1. Although divergence via host‐plant shifting is a common theme in the speciation of some phytophagous insects, it is not clear whether host shifts are typically initiators of speciation or if they instead contribute to divergence events already in progress. While host shifts appear to be generally associated with speciation events for flies in the genus Strauzia, three sympatric varieties of the sunflower fly [Strauzia longipennis (Wiedemann)] co‐occur on the same host plant in the Midwestern United States and may have evolved reproductive barriers without a host shift. 2. The strength of two prezygotic reproductive barriers was compared among the three S. longipennis varieties: one barrier that is often associated with divergent ecological selection (allochronic isolation), and another that is more likely to be independent of ecological selection (pre‐copulatory sexual isolation). The presence and relative strength of each barrier between fly varieties were evaluated using microsatellites, no choice mating experiments, studies of allochronic isolation, and field collection data. 3. Evidence for both allochronic isolation and pre‐copulatory sexual isolation was detected between the three varieties of S. longipennis. The measure of isolation calculated for each barrier between the three varieties was lower than measures calculated between different species of Strauzia found on different hosts, suggesting that subsequent host shifts may increase the degree of reproductive isolation. For Strauzia and other specialist insects, some reproductive isolation may evolve prior to, and indeed may facilitate, host shifts.     

Effects of anthropogenic habitat disturbance and Giardia duodenalis infection on a sentinel species' gut bacteria

Habitat disturbance, a common consequence of anthropogenic land use practices, creates human–animal interfaces where humans, wildlife, and domestic species can interact. These altered habitats can influence host–microbe dynamics, leading to potential downstream effects on host physiology and health. Here, we explored the effect of ecological overlap with humans and domestic species and infection with the protozoan parasite Giardia duodenalis on the bacteria of black and gold howler monkeys (Alouatta caraya), a key sentinel species, in northeastern Argentina. Fecal samples were screened for Giardia duodenalis infection using a nested PCR reaction, and the gut bacterial community was characterized using 16S rRNA gene amplicon sequencing. Habitat type was correlated with variation in A. caraya gut bacterial community composition but did not affect gut bacterial diversity. Giardia presence did not have a universal effect on A. caraya gut bacteria across habitats, perhaps due to the high infection prevalence across all habitats. However, some bacterial taxa were found to vary with Giardia infection. While A. caraya's behavioral plasticity and dietary flexibility allow them to exploit a range of habitat conditions, habitats are generally becoming more anthropogenically disturbed and, thus, less hospitable. Alterations in gut bacterial community dynamics are one possible indicator of negative health outcomes for A. caraya in these environments, since changes in host–microbe relationships due to stressors from habitat disturbance may lead to negative repercussions for host health. These dynamics are likely relevant for understanding organism responses to environmental change in other mammals.     

SELECTION AND STRAIN SPECIFICITY OF COMPATIBILITY BETWEEN SNAIL INTERMEDIATE HOSTS AND THEIR PARASITIC SCHISTOSOMES

Many theoretical models of host-parasite coevolution assume that variation in host resistance to parasite infection is, at least partially, genetically determined and specific to the strain of infecting parasite. However, very few experimental studies have been conducted to test this assumption in animal-parasite systems. Biomphalaria glabrata snails serve as the intermediate hosts of Schistosoma mansoni. Although some snails are resistant to infection, there is no evidence of fixation of resistance in field populations. Two possible explanations for this are high fitness costs associated with resistance and a dynamic coevolution between parasite and host, perhaps involving matching alleles or gene-for-gene interactions. Two strains of B. glabrata were artificially selected for either resistance or susceptibility to each of two strains of S. mansoni parasite for three generations. Third-generation snails were then were exposed to either the parasite strain to which they had been selected or to a different parasite strain. In both host strains, resistance and susceptibility (compatibility) were found to be heritable. Moreover, compatibility to one parasite strain was not associated with compatibility to another strain, implying no genetic trade-off. Our results are discussed in terms of potential mechanisms of resistance in this host-parasite system and their implications to general coevolutionary theory.     

Molecular Characterization of Parabasalian Symbionts Coronympha clevelandii and Trichonympha subquasilla from the Hawaiian Lowland Tree Termite Incisitermes immigrans

An important and undervalued challenge in characterizing symbiotic protists is the accurate identification of their host species. Here, we use DNA barcoding to resolve one confusing case involving parabasalian symbionts in the hindgut of the Hawaiian lowland tree termite, Incisitermes immigrans, which is host to several parabasalians, including the type species for the genus Coronympha, C. clevelandii. We collected I. immigrans from its type locality (Hawaii), confirmed its identity by DNA barcoding, and characterized the phylogenetic position of two symbionts, C. clevelandii and Trichonympha subquasilla. These data show that previous molecular surveys of “I. immigrans” are, in fact, mainly derived from the Caribbean termite I. schwarzi, and perhaps also another related species. These results emphasize the need for host barcoding, clarify the relationship between morphologically distinct Coronympha species, and also suggest some interesting distribution patterns of nonendemic termite species and their symbionts.     

Insect herbivores as potential causes of mortality and adaptation in gallforming insects

Summary Recent studies have suggested that plant galls benefit only the insects living in them and not the host plants, and that galls are induced by insects primarily to improve the plant as a microenvironment or a food source. The potential advantage to insects of protection from their predators and parasitoids has been considered unclear and perhaps minor in importance. However, the potential threat to gallforming insects from other insect herbivores has usually been relatively neglected. This paper notes literature and observations which suggest that herbivores may either consume or be deterred by galls. Even soft leaf galls produced by Hormaphis and Phylloxera aphids appeared to deter some herbivores in the field. The threat of herbivory to galls might help explain general patterns of gall ecology and morphology, and deserves closer attention.     

Invasion of <Emphasis Type="Italic">Rhynchosporium commune</Emphasis> onto wild barley in the Middle East

Rhynchosporium commune was recently introduced into the Middle East, presumably with the cultivated host barley (Hordeum vulgare). Middle Eastern populations of R. commune on cultivated barley and wild barley (H. spontaneum) were genetically undifferentiated and shared a high proportion of multilocus haplotypes. This suggests that there has been little selection for host specialization on H. spontaneum, a host population often used as a source of resistance genes introduced into its domesticated counterpart, H. vulgare. Low levels of pathogen genetic diversity on H. vulgare as well as on H. spontaneum, indicate that the pathogen was introduced recently into the Middle East, perhaps through immigration on infected cultivated barley seeds, and then invaded the wild barley population. Although it has not been documented, the introduction of the pathogen into the Middle East may have a negative influence on the biodiversity of native Hordeum species.     

Climate,host phylogeny and the connectivity of host communities govern regional parasite assembly

Aim

Identifying barriers that govern parasite community assembly and parasite invasion risk is critical to understand how shifting host ranges impact disease emergence. We studied regional variation in the phylogenetic compositions of bird species and their blood parasites (Plasmodium and Haemoproteus spp.) to identify barriers that shape parasite community assembly.

Location

Australasia and Oceania.

Methods

We used a data set of parasite infections from >10,000 host individuals sampled across 29 bioregions. Hierarchical models and matrix regressions were used to assess the relative influences of interspecies (host community connectivity and local phylogenetic distinctiveness), climate and geographic barriers on parasite local distinctiveness and composition.

Results

Parasites were more locally distinct (co‐occurred with distantly related parasites) when infecting locally distinct hosts, but less distinct (co‐occurred with closely related parasites) in areas with increased host diversity and community connectivity (a proxy for parasite dispersal potential). Turnover and the phylogenetic symmetry of parasite communities were jointly driven by host turnover, climate similarity and geographic distance.

Main conclusions

Interspecies barriers linked to host phylogeny and dispersal shape parasite assembly, perhaps by limiting parasite establishment or local diversification. Infecting hosts that co‐occur with few related species decreases a parasite's likelihood of encountering related competitors, perhaps increasing invasion potential but decreasing diversification opportunity. While climate partially constrains parasite distributions, future host range expansions that spread distinct parasites and diminish barriers to host shifting will likely be key drivers of parasite invasions.     

THE EVOLUTION OF PARASITES FROM THEIR HOSTS: A CASE STUDY IN THE PARASITIC RED ALGAE

Morphological similarities of many parasites and their hosts have led to speculation that some groups of plant, animal, fungal, and algal parasites may have evolved directly from their hosts. These parasites, which have been termed adelphoparasites in the botanical literature, and more recently, agastoparasites in the insect literature, may evolve monophyletically from one host and radiate secondarily to other hosts or, these parasites may arise polyphyletically, each arising from its own host. In this study we compare the internal transcribed spacer regions of the nuclear ribosomal repeats of species and formae specialis (host races) included in the red algal parasite genus Asterocolax with its hosts, which all belong to the Phycodrys group of the Delesseriaceae and with closely related nonhost taxa of the Delesseriaceae. These analyses reveal that species of Asterocolax have evolved polyphyletically. Asterocolax erythroglossi from the North Atlantic host Erythroglossum laciniatum appears to have evolved from its host, whereas taxa included in the north Pacific species Asterocolax gardneri have had two independent origins. Asterocolax gardneri from the host Polyneura latissima probably arose directly from this host. In contrast, all other A. gardneri formae specialis appear to have originated from either Phycodrys setchellii or P. isabelliae and radiated secondarily onto other closely related taxa of the Phycodrys group, including Nienburgia andersoniana and Anisocladella pacifica. Gamete crossing experiments confirm that A. gardneri from each host is genetically isolated from both its host, and from other A. gardneri and their hosts. Cross-infection experiments reveal that A. gardneri develops normally only on its natural host, although some abberrant growth may occur on alternate hosts. The ability of red algal parasites to radiate secondarily to other red algal taxa, where they may become isolated genetically and speciate, suggests that this process of speciation is not a “genetic dead end” but one that may give rise to related clusters of parasite species.     

Limited female dispersal predicts the incidence of Wolbachia across ants (Hymenoptera: Formicidae)

The endosymbiotic bacterium Wolbachia is perhaps the greatest panzootic in the history of life on Earth, yet remarkably little is known regarding the factors that determine its incidence across species. One possibility is that Wolbachia more easily invades species with structured populations, due to the increased strength of genetic drift and higher initial frequency of infection. This should enable strains that induce mating incompatibilities to more easily cross the threshold prevalence above which they spread to either fixation or a stable equilibrium infection prevalence. Here, we provide empirical support for this hypothesis by analysing the relationship between female dispersal (as a proxy for population structure) and the incidence of Wolbachia across 250 species of ants. We show that species in which the dispersal of reproductive females is limited are significantly more likely to be infected with Wolbachia than species whose reproductive ecology is consistent with significant dispersal of females, and that this relationship remains after controlling for host phylogeny. We suggest that structured host populations, in this case resulting from limited female dispersal, may be an important feature determining how easily Wolbachia becomes successfully established in a novel host, and thus its occurrence across a wide diversity of invertebrate hosts.     

Conservatism and stability of the symbiotic system of the invasive alien treehopper Stictocephala bisonia (Hemiptera,Cicadomorpha, Membracidae)

1. Nutritional symbiosis between insects and microorganisms (bacteria and/or yeast-like symbionts) that provide amino acids and vitamins which are lacking in the diet of host insects is widespread in nature. Auchenorrhyncha are usually host to two ancient bacterial symbionts – bacterium Sulcia (Bacteroidetes) and a betaproteobacterium – which, in some groups, were lost or replaced by other bacteria. 2. The aim of this research was to: (i) identify the symbiotic microorganisms associated with the invasive treehopper Stictocephala bisonia; (ii) describe their localisation as well as the mode of inheritance; and (iii) address the issue of whether individuals of S. bisonia, living in different areas and feeding on various plants, possess identical, similar or perhaps different symbiotic microbial systems. 3. Individuals of S. bisonia collected in their native range in North America (U.S.A.) and in 11 localities in Europe were investigated using molecular, histological and ultrastructural methods. 4. The results indicate that all the examined specimens are characterised by the same conservative symbiotic system. All of them are host to only two types of bacterial symbiont: Sulcia and the betaproteobacteria belonging to the Nasuia lineage. No other symbionts in any of 36 individuals examined were detected. 5. Both symbionts are localised in a common bacteriome and are transovarially transmitted between generations.     

Divergent host phenotypes create opportunities and constraints on the distribution of two wing‐dwelling feather mites

The diversity of symbionts (commensals, mutualists or parasites) that share the same host species may depend on opportunities and constraints on host exploitation associated with host phenotype or environment. Various host traits may differently influence host accessibility and within‐host population growth of each symbiont species, or they may determine the outcome of within‐host interactions among coexisting species. In turn, phenotypic diversity of a host species may promote divergent exploitation strategies among its symbiotic organisms. We studied the distribution of two feather mite species, Proctophyllodes sylviae and Trouessartia bifurcata, among blackcaps Sylvia atricapilla wintering in southern Spain during six winters. The host population included migratory and sedentary individuals, which were unequally distributed between two habitat types (forests and shrublands). Visual mite counts showed that both mite species often coexisted on sedentary blackcaps, but were seldom found together on migratory blackcaps. Regardless of host habitat, Proctophyllodes were highly abundant and Trouessartia were scarce on migratory blackcaps, but the abundance of both mite species converged in intermediate levels on sedentary blackcaps. Coexistence may come at a cost for Proctophyllodes, whose load decreased when Trouessartia was present on the host (the opposite was not true). Proctophyllodes load was positively correlated with host wing length (wings were longer in migratory blackcaps), while Trouessartia load was positively correlated to uropygial gland size (sedentary blackcaps had bigger glands), which might render migratory and sedentary blackcaps better hosts for Proctophyllodes and Trouessartia, respectively. Our results draw a complex scenario for mite co‐existence in the same host species, where different mite species apparently take advantage of, or are constrained by, divergent host phenotypic traits. This expands our understanding of bird–mite interactions, which are usually viewed as less dynamic in relation to variation in host phenotype, and emphasizes the role of host phenotypic divergence in the diversification of symbiotic organisms.     

GENETIC CONSTRAINTS AND THE PHYLOGENY OF INSECT-PLANT ASSOCIATIONS: RESPONSES OF OPHRAELLA COMMUNA (COLEOPTERA: CHRYSOMELIDAE) TO HOST PLANTS OF ITS CONGENERS

We ask whether patterns of genetic variation in a phytophagous insect's responses to potential host plants shed light on the phylogenetic history of host association. Ophraella communa feeds chiefly, and in eastern North America exclusively, on Ambrosia (Asteraceae: Ambrosiinae). Using mostly half-sib breeding designs, we screened for genetic variation in feeding responses to and larval survival on its own host and on seven other plants that are hosts (or, on one case, closely related to the host) of other species of Ophraella. We found evidence for genetic variation in feeding responses to five of the seven test plants, other than the natural host. We found no evidence of genetic variation in feeding responses to two plant species, nor in capacity for larval survival on six. These results imply constraints on the availability of genetic variation; however, little evidence for constraints in the form of negative genetic correlations was found. These results are interpreted in the context of a provisional phylogeny of, and a history of host shifts within, the genus. Ophraella communa does not present evidence of genetic variation in its ability to feed and/or survive on Solidago, even though it is probably descended from a lineage that fed on Solidago or related plants, possibly as recently as 1.9 million years ago. Genetic variation in performance on this plant may have been lost. Based on evidence for genetic variation and on mean performance, by far the greatest potentiality for adaptation to a congener's host was evinced in responses to Iva frutescens, which not only is related and chemically similar to Ambrosia, but also is the host of a closely related species of Ophraella that may have been derived from an Ambrosia-associated ancestor. Genetic variation in O. communa's capacity to feed and/or survive on its congeners' hosts is less evident for plants that do not represent historically realized host shifts (with one exception) than for those that may (but see Note Added in Proof). The results offer some support for the hypothesis that the evolution of host shifts has been guided in part by constrained genetic variation.     

EVOLUTIONARY GENETICS OF OVIPOSITION PREFERENCE IN SWALLOWTAIL BUTTERFLIES

Models of the evolution of host shifts and speciation in phytophagous insects are often built upon the assumption that host selection is under simple genetic control, perhaps even a single locus. The genetic basis for differences in host-plant preference by ovipositing insects was investigated using two closely related species of swallowtail butterfly, Papilio oregonius and P. zelicaon, which differ in the plant families on which females oviposit. Both species had been shown previously to vary within populations in host selection. A combination of analyses using reciprocal interspecific crosses and isofemale strains within populations indicated that oviposition preference in these species is determined significantly by one or more loci on the X chromosome, which female Lepidoptera inherit only paternally. Hence, preferences in hybrid females tended toward the paternal species. This is the first insect group for which partial control of oviposition preference has been localized onto a particular chromosome. In addition, one or more loci on another chromosome(s) appear to contribute to preference, as indicated by the partially intermediate preferences of some hybrid crosses. The overall differences in preference in the reciprocal interspecific hybrids were restricted to differences in the distribution of eggs laid among the local host plants of these two Papilio species; the reciprocal crosses did not differ in the small percentage of eggs laid on a novel potential host species. The variation in host selection found among the isofemale strains reinforces earlier results for these strains, indicating that there is genetic variation in host selection within these populations. Overall, the results indicate that the evolution of oviposition preference in these species involves genetic changes at two or more chromosomes with the X chromosome playing an important role in determining preference.     

The influence of space and time on the evolution of altruistic defence: the case of ant slave rebellion

How can antiparasite defence traits evolve even if they do not directly benefit their carriers? An example of such an indirect defence is rebellion of enslaved Temnothorax longispinosus ant workers against their social parasite Temnothorax americanus, a slavemaking ant. Ant slaves have been observed to kill their oppressors' offspring, a behaviour from which the sterile slaves cannot profit directly. Parasite brood killing could, however, reduce raiding pressure on related host colonies nearby. We analyse with extensive computer simulations for the Temnothorax slavemaker system under what conditions a hypothetical rebel allele could invade a host population, and in particular, how host–parasite dynamics and population structure influence the rebel allele's success. Exploring a wide range of model parameters, we only found a small number of parameter combinations for which kin selection or multilevel selection could allow a slave rebellion allele to spread in the host population. Furthermore, we did not detect any cases in which the reduction of raiding pressure in the close vicinity of the slavemaker nest would substantially contribute to the inclusive fitness of rebels. This suggests that slave rebellion is not costly and perhaps a side‐effect of some other beneficial trait. In some of our simulations, however, even a costly rebellion allele could spread in the population. This was possible when host–parasite interactions led to a metapopulation dynamic with frequent local extinctions and recolonizations of demes by the offspring of few immigrants.     

Associative learning of host presence in non‐host environments influences parasitoid foraging

1. Parasitoids are known to utilise learning of herbivore‐induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non‐suitable herbivores (non‐hosts). Simultaneous infestation of plants by hosts and non‐hosts has been found to result in induction of HIPVs that differ from host‐infested plants. Each non‐host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non‐host herbivore also contain the host. 2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non‐hosts in the laboratory and in semi‐field experiments. 3. In two‐choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant–host–non‐host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non‐host caterpillar Mamestra brassicae or the non‐host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non‐host caterpillars or aphids in a semi‐field situation. 4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.     

Simple sequence repeat (SSR)-based gene diversity in <Emphasis Type="Italic">Burkholderia pseudomallei</Emphasis> and <Emphasis Type="Italic">Burkholderia mallei</Emphasis>

Pathogens Burkholderia pseudomallei (Bp) and Burkholderia mallei (Bm) contain a large number (> 12,000) of Simple Sequence Repeats (SSRs). To study the extent to which these features have contributed to the diversification of genes, we have conducted comparative studies with nineteen genomes of these bacteria. We found 210 genes with characteristic types of SSR variations. SSRs with nonamer repeat units were the most abundant, followed by hexamers and trimers. Amino acids with smaller and nonpolar R-groups are preferred to be encoded by the variant SSRs, perhaps due to their minimal impacts to protein functionality. A majority of these genes appears to code for surface or secreted proteins that may directly interact with the host factors during pathogenesis or other environmental factors. There also are others that encode diverse functions in the cytoplasm, and this protein variability may reflect an extensive involvement of phase variation in survival and adaptation of these pathogens.