Geographical variation in host specificity of fleas (Siphonaptera) parasitic on small mammals: the influence of phylogeny and local environmental conditions

The evolution of host specificity remains a central issue in the study of host‐parasite relationships. Here we tackle three basic questions about host specificity using data on host use by fleas (Siphonaptera) from 21 geographical regions. First, are the host species exploited by a flea species no more than a random draw from the locally available host species, or do they form a taxonomically distinct subset? Using randomization tests, we showed that in the majority of cases, the taxonomic distinctness (measured as the average taxonomic distances among host species) of the hosts exploited by a flea is no different from that of random subsets of hosts taken from the regional pool. In the several cases where a difference was found, the taxonomic distinctness of the hosts used by a flea was almost always lower than that of the random subsets, suggesting that the parasites use hosts within a narrower taxonomic spectrum than what is available to them. Second, given the variation in host specificity among populations of the same flea species, is host specificity truly a species character? We found that host specificity measures are repeatable among different populations of the same flea species: host specificity varies significantly more among flea species than within flea species. This was true for both measures of host specificity used in the analyses: the number of host species exploited, and the index measuring the average taxonomic distinctness of the host species and its variance. Third, what causes geographical variation in host specificity among populations of the same flea species? In the vast majority of flea species, neither of our two measures of host specificity correlated with either the regional number of potential host species or their taxonomic distinctness, or the distance between the sampled region and the center of the flea's geographical range. However, in most flea species host specificity correlated with measures of the deviation in climatic conditions (precipitation and temperature) between the sampled region and the average conditions computed across the flea's entire range. Overall, these results suggest that host specificity in fleas is to a large extent phylogenetically constrained, while still strongly influenced by local environmental conditions.     

Distribution of fleas (Siphonaptera) among small mammals: mean abundance predicts prevalence via simple epidemiological model

We used data on the abundance and distribution of fleas parasitic on small mammals in Slovakia and aimed: (i) to confirm a positive relationship between abundance and distribution fleas within and across host species; and (ii) to test if prevalence of fleas can be reliably predicted from a simple epidemiological model that takes into account flea mean abundance and its variance. Prevalence of a flea species increased with an increase in its mean abundance both within and across host species. We calculated prevalences both for each flea-host association and for each flea species across all hosts. Observed prevalences did not differ significantly from those predicted by the epidemiological model using parameters of Taylor's power relationship between mean abundance of fleas and its variance. Regressions of predicted prevalences against observed prevalences produced slope values that did not differ significantly from unity and were independent of scale (within or across host species). Our results demonstrated that up to 96% of variance in flea prevalence can be explained solely by their mean abundance. We concluded that, in general, there is no need to invoke other, more complex factors for the explanation of the variation in flea prevalence.     

Relationships between parasite abundance and the taxonomic distance among a parasite's host species: an example with fleas parasitic on small mammals

Opportunistic parasite species, capable of exploiting several different host species, do not achieve the same abundance on all these hosts. Parasites achieve maximum abundance on their principal host species, and lower abundances on their auxiliary host species. Taxonomic relatedness between the principal and auxiliary host species may determine what abundance a parasite can achieve on its auxiliary hosts, as relatedness should reflect similarities among host species in ecological, physiological and/or immunological characters. We tested this hypothesis with fleas (Siphonaptera) parasitic on small Holarctic mammals. We determined whether the abundance of a flea in its auxiliary hosts decreases with increasing taxonomic distance of these hosts from the principal host. Using data on 106 flea species from 23 regions, for a total of 194 flea-locality combinations, we found consistent support for this relationship, both within and across regions, and even after controlling for the potentially confounding effect of flea phylogeny. These results are most likely explained by a decrease in the efficiency of the parasite's evasive mechanisms against the host's behavioural and immune defences with increasing taxonomic distance from the principal host. Our findings suggest that host switching over evolutionary time may be severely constrained by the coupling of parasite success with the relatedness between new hosts and the original host.     

Aggregation and species coexistence in fleas parasitic on small mammals

The aggregation model of coexistence states that species coexistence is facilitated if interspecific aggregation is reduced relative to intraspecific aggregation. We investigated the relationship between intraspecific and interspecific aggregation in 17 component communities (the flea assemblage of a host population) of fleas parasitic on small mammals and hypothesized that interspecific interactions should be reduced relative to intraspecific interactions, facilitating species coexistence. We predicted that the reduction of the level of interspecific aggregation in relation to the level of intraspecific aggregation would be positively correlated with total flea abundance and species richness of flea assemblages. We also expected that the higher degree of facilitation of flea coexistence would be affected by host parameters such as body mass, basal metabolic rate (BMR) and depth and complexity of burrows. Results of this study supported the aggregation model of coexistence and demonstrated that, in general, a) conspecific fleas were aggregated across their hosts; b) flea assemblages were not dominated by negative interspecific interactions; and c) the level of interspecific aggregation in flea assemblages was reduced in relation to the level of intraspecific aggregation. Intraspecific aggregation tended to be correlated positively to body mass, burrow complexity and mass-independent BMR of a host. Positive interspecific associations of fleas tended to occur more frequently in species-rich flea assemblages and/or in larger hosts possessing deep complex burrows. Intraspecific aggregation increased relative to interspecific aggregation when species richness of flea infracommunities (the flea assemblage of a host individual) and component communities increased. We conclude that the pattern of flea coexistence is related both to the structure of flea communities and affinities of host species.     

Host distribution and pathogen infection of fleas (Siphonaptera) recovered from small mammals in Pennsylvania

The number of recognized flea‐borne pathogens has increased over the past decade. However, the true number of infections related to all flea‐borne pathogens remains unknown. To better understand the enzootic cycle of flea‐borne pathogens, fleas were sampled from small mammals trapped in central Pennsylvania. A total of 541 small mammals were trapped, with white‐footed mice (Peromyscus leucopus) and southern red‐backed voles (Myodes gapperi) accounting for over 94% of the captures. Only P. leucopus were positive for examined blood‐borne pathogens, with 47 (18.1%) and ten (4.8%) positive for Anaplasma phagocytophilum and Babesia microti, respectively. In addition, 61 fleas were collected from small mammals and tested for pathogens. Orchopeas leucopus was the most common flea and Bartonella vinsonii subspecies arupensis, B. microti, and a Rickettsia felis‐like bacterium were detected in various flea samples. To the best of our knowledge, this is the first report of B. microti DNA detected from a flea and the first report of a R. felis‐like bacterium from rodent fleas in eastern North America. This study provides evidence of emerging pathogens found in fleas, but further investigation is required to resolve the ecology of flea‐borne disease transmission cycles.     

Abundance patterns and coexistence processes in communities of fleas parasitic on small mammals

The abundance of a given species in a community is likely to depend on both the total abundance and diversity of other species making up that community. A large number of co-occurring individuals or co-occurring species may decrease the abundance of any given species via diffuse competition; however, indirect interactions among many co-occurring species can have positive effects on a focal species. The existence of diffuse competition and facilitation remain difficult to demonstrate in natural communities. Here, we use data on communities of fleas ectoparasitic on small mammals from 27 distinct geographical regions to test whether the abundance of any given flea species in a community is affected by either the total abundance of all other co-occurring flea species, or the species richness and/or taxonomic diversity of the flea community. At all scales of analysis, i.e. whether we compared the same flea species on different host species, or different flea species, two consistent results emerged. First, the abundance of a given flea species correlates positively with the total abundance of all other co-occurring flea species in the community. Second, the abundance of any given flea species correlates negatively with either the species richness or taxonomic diversity of the flea community. The results do not support the existence of diffuse competition in these assemblages, because the more individuals of other flea species are present on a host population, the more individuals of the focal species are there as well. Instead, we propose explanations involving either apparent facilitation among flea species via suppression of host immune defenses, or niche filtering processes acting to restrict the taxonomic composition and abundance of flea assemblages.     

A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations

Siphonaptera (fleas) is a highly specialized order of holometabolous insects comprising ～2500 species placed in 16 families. Despite a long history of extensive work on flea classification and biology, phylogenetic relationships among fleas are virtually unknown. We present the first formal analysis of flea relationships based on a molecular matrix of four loci (18S ribosomal DNA, 28S ribosomal DNA, Cytochrome Oxidase II, and Elongation Factor 1‐alpha) for 128 flea taxa from around the world representing 16 families, 25 subfamilies, 26 tribes, and 83 flea genera with eight outgroups. Trees were reconstructed using direct optimization and maximum likelihood techniques. Our analysis supports Tungidae as the most basal flea lineage, sister group to the remainder of the extant fleas. Pygiopsyllomorpha is monophyletic, as are the constituent families Lycopsyllidae, Pygiopsyllidae, and Stivaliidae, with a sister group relationship between the latter two families. Macropsyllidae is resolved as sister group to Coptopsyllidae with moderate nodal support. Stephanociricidae is monophyletic, as are the two constituent subfamilies Stephanocircinae and Craneopsyllinae. Vermipsyllidae is placed as sister group to Jordanopsylla. Rhopalopsyllidae is monophyletic as are the two constituent subfamilies Rhopalopsyllinae and Parapsyllinae. Hystrichopsyllidae is paraphyletic with Hystrichopsyllini placed as sister to some species of Anomiopsyllini and Ctenopariini placed as sister to Carterettini. Ctenophthalmidae is grossly paraphyletic with the family broken into seven lineages dispersed on the tree. Most notably, Anomiopsyllini is paraphyletic. Pulicidae and Chimaeropsyllidae are both monophyletic and these families are sister groups. Ceratophyllomorpha is monophyletic and includes Ischnopsyllidae, Ceratophyllidae, and Leptopsyllidae. Leptopsyllidae is paraphyletic as are its constituent subfamilies Amphipsyllinae and Leptopsyllinae and the tribes Amphipsyllini and Leptopsyllini. Ischnopsyllidae is monophyletic. Ceratophyllidae is monophyletic, with a monophyletic Dactypsyllinae nested within Ceratophyllinae, rendering the latter group paraphyletic. Mapping of general host associations on our topology reveals an early association with mammals with four independent shifts to birds. © The Willi Hennig Society 2008.     

Scale‐invariance of niche breadth in fleas parasitic on small mammals

The resource specialization or niche breadth of a species is not fixed across populations, but instead varies over geographical space. A species may be a local specialist but a regional generalist, if it uses locally few resources that are substitutable across locations. In contrast, a species is a local generalist and a regional specialist if it uses locally many resources that cannot be substituted from 1 location to the next. Scale‐dependence can thus be a major factor in estimation of niche breadth. Here, we test for relationships between local and global estimates of host specificity (a measure of niche breadth for parasites) in fleas (Siphonaptera) parasitic on small mammals from 49 different regions within the Holarctic. Across all fleas, we found a strong, positive relationship between the number of host species that a flea uses in 1 locality and the number of different host species that can serve as the flea's principal host (i.e. the one supporting the most fleas in a region) among all regions. Also, we observed a strong positive relationship between the taxonomic distinctness of the host species used in 1 locality and that of all known principal hosts among all localities. These relationships held after correcting for potentially confounding phylogenetic influences. We discuss the implications of scale‐independent host specificity and its association with geographical range size and species‐specific patterns of host use.     

Diversification of ectoparasite assemblages and climate: an example with fleas parasitic on small mammals

Aim We studied the relationships between the numbers of species and numbers of higher taxa (genera, tribes, subfamilies and families) in flea assemblages of small mammalian hosts with the aims of: (a) comparing these relationships across different regions, and (b) testing the hypothesis that flea assemblages in warmer regions diversify mainly via intrahost speciation, whereas those in colder regions diversify mainly via host switching. Location The study used previously published data on flea assemblages on small mammalian hosts from 25 different regions of the Holarctic. Methods The number of flea genera, tribes, subfamilies or families in an assemblage (host species) was plotted against the number of flea species in this assemblage for each region separately, and a power function was fitted to the resulting relationships. Then, the values of the exponent of the power function for a region were regressed against the mean annual temperature in this region, across all regions. Results The relationships between the number of flea species and the numbers of flea genera, tribes, subfamilies or families on a host species in each region were found to be well described by simple power functions. The exponent of the power function of the relationship between the number of flea species and the number of flea genera per host tended to decrease with increasing local mean annual temperature. When two apparent outliers from the trend (corresponding to regions where sampling was not performed as in other regions) were omitted from the analysis, the negative relationship between temperature and the exponent of the power function between the number of flea species and number of flea genera per host became highly significant. No relationship was found between the values of the exponents of the power functions between the number of flea species and the number of flea tribes, subfamilies or families per host, and the mean local annual temperature. Main conclusions The results suggest that the diversification of flea assemblages is associated with climatic variables. In warm regions, the greater number of congeneric species per flea assemblage, reflected by the lower exponent of the power function, may well be the outcome of intrahost speciation. This indicates that, as regional temperature increases, intrahost speciation becomes a relatively more important mode of diversification than acquisition of fleas via host switching.     

Wolbachia endosymbionts in fleas (Siphonaptera)

Intracellular endosymbionts, Wolbachia spp., have been reported in many different orders of insects and in nematodes but not previously in fleas. This is the first conclusive report of Wolbachia spp. within members of the Siphonaptera. Using nested polymerase chain reaction (PCR) targeting of the 16S ribosomal RNA gene, we screened for Wolbachia spp. in fleas collected from 3 counties in Georgia and 1 in New York. The prevalence of Wolbachia spp. detected varied among the 6 different species screened: 21% in the cat flea Ctenocephalides felis (n = 604), 7% in the dog flea C. canis (n = 28), 25% in Polygenus gwyni (n = 8), 80% in Orchopeas howardi (n = 15), 94% in Pulex simulans (n = 255), and 24% in the sticktight flea Echidnophaga gallinacea (n = 101). Wolbachia spp. infection in fleas was confirmed by sequencing positive PCR products, comparing sequenced 16S ribosomal DNA (rDNA) with Wolbachia spp. sequences in GenBank using BLAST search, and subjecting sequence data to phylogenetic analysis. For further confirmation, 16S rDNA-positive samples were reamplified using the wsp gene.     

Biogeography of parasite abundance: latitudinal gradient and distance decay of similarity in the abundance of fleas and mites,parasitic on small mammals in the Palearctic,at three spatial scales

We tested whether biogeographic patterns characteristic for biological communities can also apply to populations and investigated geographic patterns of variation in abundance of ectoparasites (fleas and mites) collected from bodies of their small mammalian hosts (rodents and shrews) in the Palearctic at continental, regional and local scales. We asked whether (i) there is a relationship between latitude and abundance and (ii) similarity in abundance follows a distance decay pattern or it is better explained by variation in extrinsic biotic and abiotic factors. We analysed the effect of latitude on mean intraspecific abundance using general linear models including proportional abundance of its principal host as an additional predictor variable. Then, we examined the relative effect of geographic distance, biotic and abiotic dissimilarities among regions, subregions or localities on the intraspecific dissimilarity in abundance among regions, subregions or localities using Generalized Dissimilarity Modelling. We found no relationship between latitude and intraspecific flea or mite abundance. In both taxa, environmental dissimilarity explained the largest part of the deviance of spatial variation in abundance, whereas the effect of the dissimilarity in the principal host abundance was of secondary importance and the effect of geographic distance was minor. These patterns were generally consistent across the three spatial scales, although environmental variation and dissimilarity in principal host abundance were equally important at the local scale in fleas but not in mites. We conclude that biogeographic patterns related to latitude and geographic distance do not apply to spatial variation of ectoparasite abundance. Instead, the geographic distribution of abundance in arthropod ectoparasites depends on their responses, mainly to the off-host environment and to a lesser extent the abundance of their principal hosts.     

Do fleas (Insecta: Siphonaptera) parallel their mammal host diversification in the Mexican transition zone?

Aim The Mexican transition zone is a complex area where Neotropical and Nearctic biotic elements overlap. A previous study on mammal species has shown a great diversification in the area. We analyse the diversification of their flea species (Insecta: Siphonaptera), in order to determine if a diversification similar to their mammal host species has occurred. Location The area analysed corresponds to Mexico. Methods The panbiogeographical or track analysis was based on the comparison of the individual tracks of 112 species belonging to 48 genera and eight families of the order Siphonaptera. Generalized tracks were obtained based on the comparison of the individual tracks. Nodes were found in the areas where generalized tracks overlapped. Results Thirty‐four generalized tracks were obtained, distributed within the Mexican transition zone (20), the Nearctic region plus the Mexican transition zone (8), the Nearctic region (4) and the Neotropical region plus the Mexican transition zone (2). In the areas where they intersected, 26 nodes were identified: 23 in the Mexican transition zone and 3 in the Nearctic region. Main conclusions The nodes are concentrated in the Transmexican Volcanic Belt (14), Sierra Madre Oriental (5) and Sierra Madre del Sur (4) provinces of the Mexican transition zone. These results show a significant diversification of the flea taxa, in parallel with the diversification of their mammal hosts.     

Ecological correlates of body size in gamasid mites parasitic on small mammals: abundance and niche breadth

We studied ecological correlates of body size (abundance and niche breadth) in gamasid mites parasitic on small mammals in 28 regions of the Palearctic. We predicted that smaller species would be characterized by higher abundance than larger species, all else (e.g. host species) being equal. We also predicted that host specificity of mites would decrease (that is, number of host species they use would increase) with an increase in their body size. We focused on mites collected from host bodies that include a) species that feed solely on host’s blood (obligate exclusive haematophages), b) species that feed on both host’s blood and small arthropods (obligate non‐exclusive haematophages), and c) facultative haematophages. We expected that the relationship between body size and abundance and/or host specificity would be more pronounced in obligate exclusively haematophagous mites than for obligate non‐exclusively and facultative haematophagous mites. Across all mite species across regions, mean abundance correlated negatively with body size. The same was true for obligate haematophagous species, but not for facultative haematophages. When mite communities on the same host in a location were considered, the negative body mass–abundance relationship was found in only 3 of 44 communities. Nevertheless, a meta‐analytic (across host species) estimate of the slope of this relationship appeared to be significantly negative. No significant relationship between mite body size and host specificity was found in the analyses across all mite species as well as in obligate exclusive or obligate non‐exclusive haematophages. However, the number of hosts used by facultative haematophagous mites decreased significantly with an increase in their body size. We explain the relationships between morphological (body size) and ecological (abundance and niche breadth) properties of ectoparasites by their interactions with hosts or physical environment.     

The seasonal dynamic of fleas (Siphonaptera) abundance on apodemus uralensis in the northen part of Novgorod Region

Seven fleas species were revealed on Apodemus uralensis. Only three of them (Ctenophthalmus agyrtes, Ct. uncinatus, Megabothris turbidus) are the main parasites of this rodent species and have similar phenology of imago. They appear in April, parasitise during spring and summer periods and disappear in autumn, in September-October. The abundance of all three species shows two peaks in a year, which correspond to two generations. Four species (Amalaraeus penicilliger, Ct. bisoctodentatus, Peromyscopsylla bidentata, P. silvatica) are not peculiar to Apodemus uralensis. They pass on this host species occasionally from other animals inhabiting forest biotopes.     

Detection of Rickettsia spp. and host and habitat associations of fleas (Siphonaptera) in eastern Taiwan

Rickettsia typhi and Rickettsia felis (Rickettsiales: Rickettsiaceae) are two rickettsiae principally transmitted by fleas, but the detection of either pathogen has rarely been attempted in Taiwan. Of 2048 small mammals trapped in eastern Taiwan, Apodemus agrarius Pallas (24.5%) and Mus caroli Bonhote (24.4%) (both: Rodentia: Muridae) were the most abundant, and M. caroli hosted the highest proportion of fleas (63.9% of 330 fleas). Two flea species were identified: Stivalius aporus Jordan and Rothschild (Siphonaptera: Stivaliidae), and Acropsylla episema Rothschild (Siphonaptera: Leptopsyllidae). Nested polymerase chain reaction targeting parts of the ompB and gltA genes showed six fleas to be positive for Rickettsia spp. (3.8% of 160 samples), which showed the greatest similarity to R. felis, Rickettsia japonica, Rickettsia conorii or Rickettsia sp. TwKM01. Rickettsia typhi was not detected in the fleas and Rickettsia co-infection did not occur. Both flea species were more abundant during months with lower temperatures and less rainfall, and flea abundance on M. caroli was not related to soil hardness, vegetative height, ground cover by litter or by understory layer, or the abundance of M. caroli. Our study reveals the potential circulation of R. felis and other rickettsiae in eastern Taiwan, necessitating further surveillance of rickettsial diseases in this region. This is especially important because many novel rickettsioses are emerging worldwide.     

Facultative imaginal diapause in Xenopsylla conformis (Siphonaptera) fleas

The factors favouring the cessation of reproduction in X. conformis are laid in the preimaginal state. The drop in temperature during the formation of imago at the pupal stage is a signal for the cessation of reproduction. Imagos hatched at a temperature lower than that of developmental conditions of preimaginal stages do not start reproduction and enter facultative imaginal diapause state. With further decrease in temperature the state of fleas intensifies. With the rise of temperature fleas come out of diapause. In autumn coming out of diapause begins at a temperature higher than 20 degrees, on the 8th--9th day. The lower air temperature the more rapid is coming out of diapause, at a rise of temperature of 3 to 5 degrees.     

The longevity of Leptopsylla segnis fleas (Siphonaptera: Leptopsyllidae)

In experiments, the mean life duration of fleas Leptopsylla segnis on white mice (abundance of fleas within natural limits, up to 10 fleas per mouse) was 22.7 days in females and 18.8 day in males. Maximum life duration was 51 and 37 days respectively. In cases, when the initial numbers of fleas were 20 and 28-34 fleas, the duration of life was decreased. The maximum limit decreased greater than the mean duration of life. A survival dynamics of fleas depended upon the flea number. It was found out, that in cases of high abundance of fleas in the beginning of experiments, the mortality rate of males was lower than in females. During the stay on a host the fleas lost gradually an ability to endure a starvation. Possible mechanisms of the regulation of flea abundance are discussed.     

Peculiarities of thoracic and abdominal combs of fleas (Siphonaptera)

The structure of pseudosetae, spinelets, and spines of combs (ctenidia) was studied by means of light and SE microscopy in 80% of genera and subgenera of the World fauna. It is found out that peculiarities of ctenidiae in the prothorax and in tergites of the abdomen are characteristics of families and infraorders of fleas. Some characters of ctenidiae found in certain flea genera are reductions and apparently caused by habitation in some extremal conditions. An absence of ctenidiae in the unfraorder Pulicomorpha is compensated by more developed posterior margin of prothorax and general abbreviation of all thoracal segments. Reasons of ctenidiae absence, which is observed in certain genera of the infraorders Ceratophyllomorpha, Pygiopsyllomorpha and Hystricopsillomorpha associated with the same hosts, is not clear. It is confirmed, that distance between ctenidiae in different flea species associated with the same species host species, however it is recovered, that this distance correlates with the diameter of most thin hair of host. In some flea species the distance between ctenidia spices in females is larger, than in males. It is found, that sexual dimorphism by this character may not be expressed in certain species of closely related species group of fleas. It is suggested that ctenidiae were present even in the common ancestor of fleas. The hypothesis on origin of spines and pseudosetae from setae of the posterior walls of toracal and abdominal segments in the common ancestor of fleas is proposed.     

New Wolbachia endosymbionts from Nearctic and Neotropical fleas (Siphonaptera)

Several species of fleas (Siphonaptera), ectoparasites of mammals and birds, have recently been shown to harbor species of Wolbachia. Here, we extend this data set to 20 more species of Siphonaptera (Rhopalopsyllidae, Stephanocircidae, Pulicidae, Ceratophyllidae, Ctenophthalmidae, Ischnopsyllidae, Leptopsyllidae, and Malacopsyllidae) from sylvatic populations throughout the Nearctic and Neotropical regions. Using polymerase chain reaction, we targeted the Wolbachia 16S ribosomal DNA (rDNA) gene. Applying maximum parsimony- and maximum likelihood-based algorithms, as well as statistical parsimony, we conducted a phylogenetic analysis of Wolbachia 16S rDNA to evaluate its position within the known Wolbachia spp. The analysis recovered the siphonapteran Wolbachia 16S rDNA sequences as a monophyletic group and shows multiple haplotype connections between the Neotropical and Nearctic Wolbachia strains of fleas.