Michael W. Hastriter

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 arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks

Bacterial community composition in blood-sucking arthropods can shift dramatically across time and space. We used 16S rRNA gene amplification and pyrosequencing to investigate the relative impact of vertebrate host-related, arthropod-related and environmental factors on bacterial community composition in fleas and ticks collected from rodents in southern Indiana (USA). Bacterial community composition was largely affected by arthropod identity, but not by the rodent host or environmental conditions. Specifically, the arthropod group (fleas vs ticks) determined the community composition of bacteria, where bacterial communities of ticks were less diverse and more dependent on arthropod traits—especially tick species and life stage—than bacterial communities of fleas. Our data suggest that both arthropod life histories and the presence of arthropod-specific endosymbionts may mask the effects of the vertebrate host and its environment.

ADDITIONAL RECORDS OF FLEAS (SIPHONAPTERA) ON WILD RODENTS IN THE SOUTHERN PART OF ISRAEL

ABSTRACT Results, of a survey of fleas on small rodents of southern Israel conducted from 1992 to 1998 are presented. From 18 localities, 14 rodent species were sampled, yielding 14 species of fleas. Nosopsyllus iranus theodori is reported from Gerbillus gerbillus, Gerbillus henleyi, and Mus musculus in Israel for the first time. Additional records of Coptopsylla africana in Israel substantiate the presence of this species in Israel. Other distributional records and host preferences are reported and discussed.

Associations between innate immune function and ectoparasites in wild rodent hosts

Immune function is an important component of host fitness, and high investment in immunity should occur when the benefits outweigh the costs, such as when risk of parasitism is high. We sampled two rodent hosts, white-footed mice (Peromyscus leucopus), and prairie voles (Microtus ochrogaster), and their tick, flea, and mite ectoparasites. A bacterial killing assay was used to measure the host’s innate immune function. We hypothesized that classes of hosts (species, sexes, or age classes) with overall higher tick burdens would have a higher innate immune function as an evolutionary response to historically greater exposure. We hypothesized a weaker relationship between the fleas and mites and immune function because of high host specificity in fleas and the absence of known vector function in North American mites. Ectoparasites were significantly overdispersed on hosts. In accordance with our hypothesis, Peromyscus that had higher tick burdens also exhibited significantly higher bacterial killing ability compared to Microtus. There was no significant difference in total flea burden between rodent species and no relationship with bacterial killing ability. Microtus had higher burdens of mites in each order than Peromyscus, and female rodents had higher mite burdens than males. The benefits of maintaining high levels of innate immune factors appear to be greater than the energetic costs for Peromyscus compared to Microtus.

A Description of Two New Species of Ectinorus (Siphonaptera: Rhopalopsyllidae) from Laguna Blanca National Park, Neuquén Province, Argentina

Abstract Two new species of rhopalopsyllid fleas: Ectinorus lareschiae, n. sp. and Ectinorus morenoi, n. sp. are described from Laguna Blanca National Park, Neuquén Province, Argentina. Ectinorus lareschiae was collected from the sigmodontid rodents Phyllotis xanthopygus (Waterhouse) and Reithrodon auritus (Fischer), while E. morenoi was also collected from P. xanthopygus in addition to the sigmodontid rodent Abrothrix longipilis (Waterhouse) and the didelphid marsupial Thylamys pallidior (Thomas). The female sex of E. lareschiae is unknown. During these studies, it was noted that Beaucournu and Gonzalez (2005) did not include Ectinorus alejoi Hastriter, 2002 (in Hastriter et al. 2002) in their diagnosis of Ectinorus lagidium. A diagnostic character is therefore provided to distinguish males of E. alejoi from males of E. lagidium. A listing of all known species of Ectinorus is included to facilitate future work.

Description of a new species of Ectinorus (E. spiculatus) (Siphonaptera, Rhopalopsyllidae) from Argentina and a review of the subgenus Ichyonus Smit, 1987

Abstract A new species, Ectinorus spiculatus, is described from Phyllotis xanthopygus (Waterhouse) and Akodon iniscatus Thomas from Neuquén Province, Argentina. Habitat characteristics are presented for the type locality. A change in status of four additional subspecies of the Ectinorus subgenus Ichyonus Smit is provided. Ectinorus onychius onychius Jordan and Rothschild, Ectinorus onychius deplexus Smit and Ectinorus onychius angularis Smit & Rosický were elevated to specific status. Ectinorus (Ichyonus) onychius fueginus was relegated as a junior synonym of the nominate species. Phyllotis xanthopygus, Abrothrix olivaceus xanthorhinus, Loxodontomys micropus Waterhouse, and Euneomys chinchilloides (Waterhouse) are new host records for Ectinorus onychius. A key to the three species of Ichyonus is included.

Notes and new records of fleas (Insecta: Siphonaptera) from birds and mammals collected in southern China

Abstract During 2004–2007, 1,222 birds comprising 184 species and 540 small mammals comprising 61 species were examined for ectoparasites as part of a broader biodiversity survey and inventory program conducted in Guangxi and Guizhou Provinces in southern China. A collection of 87 fleas was obtained. They included eight species representing seven genera and four families: Dasypsyllus gallinulae gallinulae (Dale), Macrostylophora jiangkouensis Li and Huang (Ceratophyllidae); Palaeopsylla incurva Jordan, Palaeopsylla remota Jordan (Ctenophthalmidae); Nycteridopsylla iae Beaucournu and Kock, Thaumapsylla breviceps Rothschld (Ischnopsyllidae); and Aviostivalius klossi Jordan and Rothschild, and Lentistivalius insolli Traub (Pygiopsyllidae). Illustrations are provided to supplement those in the original description of M. jiangkouensis. The host preference for L. insolli for passerine birds is established with certainty and its derivation and distribution are discussed. The potential impact of predatory ants on flea populations at low elevations in tropical latitudes is considered.

Nycteridopsylla quadrispina Lu and Wu, a junior synonym of Nycteridopsylla iae Beaucournu and Kock (Siphonaptera: Ischnopsyllidae) as determined by morphological and DNA analyses.

Abstract Nycteridopsylla iae Beaucournu and Kock, 1992 and Nycteridopsylla quadrispina Lu and Wu, 2003 have heretofore been known only by the male and female sexes, respectively. The morphological differences in these two species are striking; however, a recent collection of male N. iae and female N. quadrispina from a single host individual of the Great Evening Bat (I. io Thomas), led us to suspect that N. iae and N. quadrispina represented the same species. Morphological similarities were noted and male and female exemplars were sequenced using five genes (18S, 28S, 16S, 12S, and COII). Across the five sequenced genes from both specimens (male and female), sequence identity was 100%. Considering morphological characteristics and DNA analysis, N. quadrispina is indisputably a junior synonym of N. iae. Myanmar is a new country record for N. iae, Harpiocephalus harpia (Temminck) is a new host record for N. iae and the preferred host is the Great Evening Bat, I. io.

Description of two new species of bat fleas of the genus Araeopsylla (Siphonaptera) from Kenya and Madagascar with notes on miscellaneous bat fleas

Abstract The flea genus Araeopsylla Jordan and Rothschild, 1921 contains nine species distributed throughout the Palaearctic, Ethiopian and Oriental Regions primarily on mollosid bats. A new species of bat flea, Araeopsylla goodmani, is described. This new species is represented by three females collected from one male specimen of the mollosid bat Chaerephon jobimena Goodman & Cardiff, 2004 from Fianarantsoa Province, Madagascar. A second new species, Araeopsylla smiti, is described from one male from the Rift Valley, Kenya. It was collected from the molossid bat Chaerephon bivittatus (Heuglin, 1861). This represents the first record of Araeopsylla in Kenya. Previous records of Araeopsylla in the Malagasy region included Araeopsylla martialis (Rothschild, 1903) from Reunion Island and Madagascar. One hundred fifty-eight specimens (64♂, 94♀) of Araeopsylla martialis were collected from 67 specimens (flea intensity of 2.4 fleas per host) of Mormopterus jugularis (Peters, 1865) across three provinces of Madagascar (Fianarantosa, Toamasina, and Toliara). Mormopterus jugularis is clearly a common host for Araeopsylla martialis. Dampfia grahami grahami (Waterston, 1915) is also reported from Eptesicus matroka (Thomas & Schwann, 1905) which is the first record from this host species and the first time the genus Dampfia has been documented in Madagascar. Although Lagaropsylla consularis Smit, 1957 and Lagaropsylla idae Smit, 1957 have been reported in Madagascar previously, Mops leucostigma Allen, 1918 is a new host record for Lagaropsylla idae. The flea intensity of Lagaropsylla idae (64♂, 83♀) on 28 specimens of Mops leucostigma was extremely high at 5.3 fleas per host. A key to the genus Araeopsylla is provided.

Description of Medwayella independencia (Siphonaptera, Stivaliidae), a new species of flea from Mindanao Island, the Philippines and their phoretic mites, and miscellaneous flea records from the Malay Archipelago.

Abstract Medwayella independencia, a new species of flea, is described from the tupaiid host Urogale everetti (Thomas) from Mindanao Island, Philippines. Several other species of fleas are also recorded from the Philippines including a single male of Lentistivalius philippinensis Hastriter and Bush, 2013 (previously known only from two males), the bat fleas Thaumapsylla breviceps orientalis Smit and Thaumapsylla longiforceps Traub, a single unidentified female species of Macrostylophora Ewing collected from the murid Bullimus bagobos Mearns, and a pair of Medwayella robinsoni ssp. from Sundasciurus hoogstraali (Sanborn) from Busuanga Island, Philippines. Representatives of Medwayella Traub, 1972 and Macrostylophora have not previously been recorded from the Philippines. A key to the male sex of Medwayella is provided. Phoretic mites of the genus Psylloglyphus (family Winterschmidtiidae) were present under the abdominal sclerites of several male and female specimens of M. independencia. This is the second report of a phoretic mite on a species of Medwayella Traub. The co-evolutionary implications between phoretic mites and fleas are discussed.