Sex-biased parasitism is not universal: evidence from rodent–flea associations from three biomes

The distribution of parasites among individual hosts is characterised by high variability that is believed to be a result of variations in host traits. To find general patterns of host traits affecting parasite abundance, we studied flea infestation of nine rodent species from three different biomes (temperate zone of central Europe, desert of Middle East and tropics of East Africa). We tested for independent and interactive effects of host sex and body mass on the number of fleas harboured by an individual host while accounting for spatial clustering of host and parasite sampling and temporal variation. We found no consistent patterns of the effect of host sex and body mass on flea abundance either among species within a biome or among biomes. We found evidence for sex-biased flea infestation in just five host species (Apodemus agrarius, Myodes glareolus, Microtus arvalis, Gerbillus andersoni, Mastomys natalensis). In six rodent species, we found an effect of body mass on flea abundance (all species mentioned above and Meriones crassus). This effect was positive in five species and negative in one species (Microtus arvalis). In M. glareolus, G. andersoni, M. natalensis, and M. arvalis, the relationship between body mass and flea abundance was mediated by host sex. This was manifested in steeper change in flea abundance with increasing body mass in male than female individuals (M. glareolus, G. andersoni, M. natalensis), whereas the opposite pattern was found in M. arvalis. Our findings suggest that sex and body mass are common determinants of parasite infestation in mammalian hosts, but neither of them follows universal rules. This implies that the effect of host individual characteristics on mechanisms responsible for flea acquisition may be manifested differently in different host species.     

Proteomic profiling of hepatic endoplasmic reticulum-associated proteins in an animal model of insulin resistance and metabolic dyslipidemia

Hepatic insulin resistance and lipoprotein overproduction are common features of the metabolic syndrome and insulin-resistant states. A fructose-fed, insulin-resistant hamster model was recently developed to investigate mechanisms linking the development of hepatic insulin resistance and overproduction of atherogenic lipoproteins. Here we report a systematic analysis of protein expression profiles in the endoplasmic reticulum (ER) fractions isolated from livers of fructose-fed hamsters with the intention of identifying new candidate proteins involved in hepatic complications of insulin resistance and lipoprotein dysregulation. We have profiled hepatic ER-associated proteins from chow-fed (control) and fructose-fed (insulin-resistant) hamsters using two-dimensional gel electrophoresis and mass spectrometry. A total of 26 large scale two-dimensional gels of hepatic ER were used to identify 34 differentially expressed hepatic ER protein spots observed to be at least 2-fold differentially expressed with fructose feeding and the onset of insulin resistance. Differentially expressed proteins were identified by matrix-assisted laser desorption ionization-quadrupole time of flight (MALDI-Q-TOF), MALDI-TOF-postsource decay, and database mining using ProteinProspector MS-fit and MS-tag or the PROWL ProFound search engine using a focused rodent or mammalian search. Hepatic ER proteins ER60, ERp46, ERp29, glutamate dehydrogenase, and TAP1 were shown to be more than 2-fold down-regulated, whereas alpha-glucosidase, P-glycoprotein, fibrinogen, protein disulfide isomerase, GRP94, and apolipoprotein E were all found to be up-regulated in the hepatic ER of the fructose-fed hamster. Seven isoforms of ER60 in the hepatic ER were all shown to be down-regulated at least 2-fold in hepatocytes from fructosefed/insulin-resistant hamsters. Implications of the differential expression of positively identified protein factors in the development of hepatic insulin resistance and lipoprotein abnormalities are discussed.     

Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palearctic region: persistence of northern cryptic populations during ice ages?

This study establishes the continental phylogeographical pattern of a European nematode, Heligmosomoides polygyrus (Dujardin, 1845; Heligmosomoidea). We sequenced 687 base pairs of the mitochondrial DNA (mtDNA) cyt b gene for 136 individuals collected in 22 localities. The results revealed that H. polygyrus populations are separated into five major units corresponding to the Italian, northern European (Denmark and Ireland), Iberian, western European, and Balkan populations. Different subclades were also observed within the first two groups. Based on the rate of molecular evolution of H. polygyrus cyt b gene-estimated to 3.5%-3.7% divergence per million years (Myr) in a previous study--the isolation time of the five clades was estimated between 2.5 +/- 0.24 and 1.5 +/- 0.23 million years ago. Moreover, H. polygyrus presents a higher genetic variability in the Mediterranean peninsulas as compared to northwestern Europe, highlighting the role of these regions as refuge areas. Like its specific host, the wood mouse Apodemus sylvaticus, H. polygyrus' pattern of postglacial recolonization of northwestern Europe was initiated from Iberian populations, while Italian and Balkan populations did not expand to the north. The results also suggest the existence of forested and temperate refuges in the southern British Isles during the Quaternary. Finally, the genetic diversity as well as the level of genetic divergence between the lineages of H. polygyrus are compared to those observed in other vertebrate and invertebrate phylogeographical studies: the existence of highly differentiated lineages in H. polygyrus (5%-10% of genetic divergence) highlights that the effects of Pleistocene climate changes on free-living organisms are also reflected in their obligate parasites.     

Age-dependent flea (Siphonaptera) parasitism in rodents: a host's life history matters

We studied age-dependent patterns of flea infestation in 7 species of rodents from Slovakia (Apodemus agrarius, A. flavicollis, A. sylvaticus, A. uralensis, Clethrionomys glareolus, Microtus arvalis, and M. subterraneus). We estimated the age of the host from its body mass and expected the host age-dependent pattern of flea abundance, the level of aggregation, and prevalence to be in agreement with theoretical predictions. We expected that the mean abundance and the level of aggregation of fleas would be lowest in hosts of smallest and largest size classes and highest in hosts of medium size classes, whereas pattern of variation of prevalence with host age would be either convex or asymptotic. In general, mean abundance and species richness of fleas increased with an increase in host age, although the pressure of flea parasitism in terms of number of fleas per unit host body surface decreased with host age. We found 2 clear patterns of the change in flea aggregation and prevalence with host age. The first pattern demonstrated a peak of flea aggregation and a trough of flea prevalence in animals of middle age classes (Apodemus species and C. glareolus). The second pattern was an increase of both flea aggregation and flea prevalence with host age (both Microtus species). Consequently, we did not find unequivocal evidence for the main role of either parasite-induced host mortality or acquired resistance in host age-dependent pattern of flea parasitism. Our results suggest that this pattern can be generated by various processes and is strongly affected by natural history parameters of a host species such as dispersal pattern, spatial distribution, and structure of shelters.     

The relA locus and the regulation of lysine biosynthesis in Escherichia coli

Summary The allelic state of relA influences the phenotype of Escherichia coli strains carrying the lysA22 mutation: lysA22 relA strains are Lys^– where lysA22 relA ⁺ strains grow (slowly) in the absence of lysine. This physiological effect has been related to an effect of the expression of the relA locus on the regulation of lysine biosynthesis. The fully derepressed levels of some lysine enzymes (aspartokinase III, aspartic semialdehyde dehydrogenase, dihydrodipicolinate reductase) are observed under lysine limitation only in rel ⁺ strains. And the induction of DAP-decarboxylase by DAP is much higher in rel ⁺ than in rel ^– strains when an amino acid limitation of growth is also realised. These results are in agreement with the hypothesis of Stephens et al. (1975) on a possible role of the stringent regulation as a general signal for amino acid deficiency.     

Revisiting the Central Metabolism of the Bloodstream Forms of Trypanosoma brucei: Production of Acetate in the Mitochondrion Is Essential for Parasite Viability

Background

The bloodstream forms of Trypanosoma brucei, the causative agent of sleeping sickness, rely solely on glycolysis for ATP production. It is generally accepted that pyruvate is the major end-product excreted from glucose metabolism by the proliferative long-slender bloodstream forms of the parasite, with virtually no production of succinate and acetate, the main end-products excreted from glycolysis by all the other trypanosomatid adaptative forms, including the procyclic insect form of T. brucei.

Methodology/Principal Findings

A comparative NMR analysis showed that the bloodstream long-slender and procyclic trypanosomes excreted equivalent amounts of acetate and succinate from glucose metabolism. Key enzymes of acetate production from glucose-derived pyruvate and threonine are expressed in the mitochondrion of the long-slender forms, which produces 1.4-times more acetate from glucose than from threonine in the presence of an equal amount of both carbon sources. By using a combination of reverse genetics and NMR analyses, we showed that mitochondrial production of acetate is essential for the long-slender forms, since blocking of acetate biosynthesis from both carbon sources induces cell death. This was confirmed in the absence of threonine by the lethal phenotype of RNAi-mediated depletion of the pyruvate dehydrogenase, which is involved in glucose-derived acetate production. In addition, we showed that de novo fatty acid biosynthesis from acetate is essential for this parasite, as demonstrated by a lethal phenotype and metabolic analyses of RNAi-mediated depletion of acetyl-CoA synthetase, catalyzing the first cytosolic step of this pathway.

Conclusions/Significance

Acetate produced in the mitochondrion from glucose and threonine is synthetically essential for the long-slender mammalian forms of T. brucei to feed the essential fatty acid biosynthesis through the “acetate shuttle” that was recently described in the procyclic insect form of the parasite. Consequently, key enzymatic steps of this pathway, particularly acetyl-CoA synthetase, constitute new attractive drug targets against trypanosomiasis.     

Genetic and morphological heterogeneity in small rodent whipworms in southwestern Europe: characterization of Trichuris muris and description of Trichuris arvicolae n. sp. (Nematoda: Trichuridae)

Genetic and morphological variability of whipworms Trichuris Roederer, 1761 (Nematoda: Trichuridae), parasites of small rodents in southwestern Europe, was studied. Isozyme patterns of natural populations of nematodes parasitizing rodent species of the Muridae (Apodemus sylvaticus, Apodemus flavicollis, Mus musculus) and Arvicolidae (Clethrionomys glareolus, Microtus agrestis, Microtus arvalis) were analyzed at 6 putative loci. Two diagnostic loci were found in T. muris from Muridae and from Arvicolidae. Thus, the existence of 2 species of Trichuris restricted to different host families was indicated. They included Trichuris muris Schrank, 1788, originally described as being from mice, and Trichuris arvicolae n. sp., parasitizing the above species of Arvicolidae. The morphological variability of both species was compared. Although ranges of all morphological characters of the new species overlapped with those of T. muris, stepwise discriminant analysis yielded a 100% accurate classification of females when using vagina length and egg size. Males of T. muris and T. arvicolae cannot be separated entirely. A set of 6 variables yielded 95.7% discrimination; the most discriminating variables were spicule size and body width.     

Predator inadvertent social information use favours reduced clumping of its prey

When animals forage socially, individuals can obtain prey from their own searching (producer tactic) or by using the behaviour of others (scrounger tactic) when it provides inadvertent social information (ISI) that food has been located. This ISI may either indicate the location of food (social information, SI), or it may indicate the quality of the resource (public information, PI). To date, few studies have explored the selective consequences for prey of being exploited by predators that use ISI. Prey exploited by such predators should evolve traits that favour high levels of ISI use (scrounging) because this would result in lower predator search efficiency given that fewer predators would be searching directly for the prey. Our simulations confirm that ISI‐using predators should increase their use of ISI when their prey form larger clumps resulting in higher prey survival. Our objective therefore is to explore whether prey will evolve towards higher clumpiness when their predators use ISI, using genetic algorithm simulation. The prey were subjected to one of three types of predators for over 500 prey generations. The predators either used: (1) no social information (NS), (2) SI only, or (3) PI. Surprisingly, the prey evolved the highest clumpiness for NS predators. Prey evolved towards smaller clump sizes with SI predators and the clumps were marginally larger when predators used PI. The result is due to the prey evolving the minimum clumpiness required to cause maximal ISI use by their predators. We discuss how this response by prey may favour the use of PI over SI in their ISI‐using predators.     

Order and disorder in ectoparasite communities: the case of congeneric gill monogeneans (Dactylogyrus spp.)

The measure of order and disorder in the distribution of species in fragmented habitats proposed by Atmar and Patterson (Oecologia, 96 (1993) 373-82) was applied to investigate nested patterns of Dactylogyrus species parasitising the gills of roach. Organisation in dactylogyrid assemblages was investigated at three levels: (1) host populations between localities; (2) local host populations over seasons; and (3) individual hosts over one season within a local host population. Dactylogyrid assemblages showed nested patterns when analyses were conducted at the level of localities (among host populations) and at the level of seasons (among host populations within localities). The analysis at the level of hosts (infracommunities of parasites) revealed that nested pattern is not common. We suggest that nestedness may have a variety of causes and does not necessarily imply competition.     

Descriptions of Tachygonetria africana n. sp. and T. pretoriensis n. sp. and redescriptions of two other species of Tachygonetria Wedl, 1862 (Nematoda: Pharyngodonidae), all parasitic in Geochelone pardalis (Testudinidae) from South Africa

Two new species of Tachygonetria, T. africana n. sp. and T. pretoriensis n. sp. are described. Both are parasites of Geochelone pardalis (Bell) from South Africa. In addition, two subspecies, T. longicollis fitzsimmonsi Petter, 1966 and T. macrolaimus macrolaimus (Linstow, 1899), also parasites of Geochelone pardalis (from Pretoria Zoo, South Africa), are redescribed and new information on their morphology is presented. On the basis of their morphology, these subspecies are raised to full specific level.