Mycetomes in Psocoptera

Psocids are microbial surface feeders Toothed laciniae enable them to scrape spores, fungal hyphae, lichens, algae, and films of yeast or bacteria from the surfaces of living and decaying plants Typical habitats are found under bark and stones, on leaf litter, in galleries of wood-boring insects, in caves, and in nests of paper wasps and bees, termites, ants, and vertebrates (Grimaldi and Engel, 2005) . With such a rich diet, primary or nutritional endo-symbionts are not expected . Obligate nutritional endosymbionts are normally catered for by the host through the provisions of specialized organs to hold the vitamins, cofactors, or amino acid-providing bacteria or, less common, yeasts . These mycetomes often exhibit a prominent structure . Not long after the introduction of microscopes, the first mycetomic structure was described by Robert Hooke in 1664 as the liver of human lice (Hooke, 1665) Shortly afterwards, in 1669, Jan Swammerdam illustrated details in the louse mycetome that represented the primary endosymbionts (Swammerdam, 1737) . However, it took until 1919 before these structures were recognized by Sikora and Buchner, independently of each other, as mycetomes and were associated with endosymbiosis (Sikora, 1919; Buchner, 1920). Unusual structures that could represent mycetomes had not been described in the anatomical literature for Psocoptera. Only in 2006, elaborate mycetomes have been discovered in two parthenogenetic booklice and barklice species (Perotti et al , 2006) The two species have paired mycetomes situated between the midgut and ovaries They were built of 4 to 8 big and 8 to 12 small, nucleated, rhomboid mycetocytes . The mycetomes were held together by a thin but dense, uniform, anucleate layer. Paired mycetomes in the body cavity as in these booklice are very rare in Phthiraptera Only the male lice of elephants, Haematomyzus elephantis (Rhynchophthirina), contain mycetomes between the testes and the ventral hypodermis in between fat body lobes (Ries, 1931). Booklice have a paired mycetome formed by uninuclear mycetocytes and surrounded by an anuclear membrane . Such structures have been detected in an unpaired form in the rat louse Polyplax, the dog louse, Linognathus, and in dipteran bat flies, whereas the paired form has been described in hemipteran whiteflies and the leafhopper Cicadella viridis (Cicadellidae) .

The two psocid species are quite distant to each other. Cerobasis guestfalica belongs to the family of granary booklice, Trogiidae, in the basal suborder Trogiomorpha . Its habitat is very varied; it can be found on deciduous branches, conifer and evergreen branches, tree trunks, haystacks, litter under hawthorn hedges, marram grass, palings, straw bales, walls, under dead birch bark, and under stones (New, 1987; Grimaldi and Engel, 2005) . Dietary components of arboreal psocids like C. guestfalica fall into three categories: algae like Pleurococcus (Chaetophoraceae) and algal components of lichens, fungi including fungal components of lichens and small amounts of substrate material such as bark flakes, or, more sporadically, foods such as pollen grains (Turner, 1975) C. guestfalica is quite unique among the Psocodea for its reproductive plasticity On rare occasions a form of life-bearing, ovoviviparity, through development inside the egg inside the mother is observed (Jentsch, 1936). A very few psocid species are truly viviparious .

The second species, Liposcelis bostrychophila, belongs to the familiar family of booklice, Liposcelidae, which originally was part of the suborder Troctomorpha. It is notorious for its feeding on mold and glue of damp books and papers and pinned insect specimens This species is not limited to human habitation . Like the approximately 100 described species in its family, the natural habitat of L. bostrychophila reaches outside decaying bark and leaf litter L. bostrychophila has also been found among the fur of Asian rats and African tree mice and in the nests of cliff swallows in America and weaverbirds in Africa The most interesting association is with the small African primate or bush baby Galago (Grimaldi and Engel, 2005). While some liposcelid species developed a predilection for warm-blooded vertebrates, others started feeding on insect eggs, a trait not found otherwise in the Psocoptera . L. bostrychophila is diploid. Sex determination in sexual relatives is of the X0 type.

The dietary requirements of C. guestfalica have not been experimentally investigated, but L. bostrychophila is easy to culture on natural and synthetic foods (Broadhead and Hobby, 1944a, 1944b; Green and Turner, 2005) . L. bostrychophila seems to have an interesting variety in its diet. Under natural conditions, about 5% of the eggs produced by Xyletinus peltatus (Anobiidae) or the Virginia creeper deathwatch beetle were eaten by L. bostrychophila and, under experimental conditions, the eggs were eaten whether or not any alternative food was available (Williams, 1972) Psocids are also known to eat their own eggs, especially if infertile, and have been recorded eating psocid corpses and exuviae (New, 1987) L. bos-trychophila possesses considerable cellobiase activity in the midgut and less in the foregut, hindgut, and ventral labial glands Cellulase is only found in the midgut (Sinha and Sriv-astava, 1970; New, 1987) L. bostrychophila also feeds equally well on bacteria as on fungi (Kalinovic et al ., 2006) .

We assume that under natural conditions, both species do not suffer from an impoverished diet requiring supplementation by primary endosymbionts This makes these pso-cid mycetomes the first mycetomes in arthropods that are not associated with obligate nutritional symbiosis Both species harbor as sole symbionts two disparate and new members of the genus Rickettsia (Rickettsiaceae, a-Proteobacteria) . The Rickettsia are obligate for early development of the oocytes and egg laying (Perotti et al , 2006) Curing the psocids stops reproduction The Rickettsia might play a role in restoring diploidy in the oocytes during parthenogenetic reproduction

An electron microscopic study on the pharynx of Liposcelis divinatorius recognized numerous Gram-negative bacteria in unaffected esophageal epithelial cells and in the sub-esophageal ganglion cells (Chapman, 2005) . We consider this species to be L. bostrychophila. By its morphology, the bacteria could either be Rickettsia, Wolbachia, or both . We found a similar distribution of Rickettsia in nerve cells and high levels of infection in the ventral subepidermis or hyperdermis of L. bostrychophila (Perotti et al , 2006) The distribution and intensity of Rickettsia in L. bostrychophila resembles that of the primary endosymbionts in the cattle and pig lice Haematopinus eurysternus and H. suis (Ries, 1931)

An obligate relationship of an endosymbiont with oogenesis of the host has been described for the parasitoid wasp Asobara tabida (Braconidae) and one of its three Wolbachia strains (Dedeine et al ., 2003) . Wasps are haplodiploid and psocids are diplodiploid . Wolbachia also has an obligate relationship with sexual filarial nematodes, which are diplodiploid The nature of the dependency is not known. Wolbachia is also found in the collembolan Folsomia candida (Isotomidae), which is diplodiploid and parthenogenetic The role of Wolbachia remains elusive Curing experiments in this species have remained unsuccessful so far (Riparbelli et al , 2006) The wide distribution and persistence of Wolbachia in this species favors more of a causal function during oogenesis than an opportunistic presence in a parthenogenetic species Folsomia has not been searched for mycetocytes or mycetomic structures

Parthenogenesis is common in Psocoptera (Mockford, 1971; Nokkala and Golub, 2006) . Parthenogenesis is rare in Phthiraptera The cattle biting louse Bovicola bovis (Trichodec-tidae, Ischnocera) exhibits parthenogenetic reproduction Human head lice in particular, but most likely many species in the entire order show marked female-biased sex ratios, which is usual for haplodiploid species but practically without precedence for diplodip-loid species like lice (Perotti et al , 2004a) It is not impossible but unlikely that similar mycetomic structures evolved de novo in two unrelated psocopteran species that are both parthenogenic This suggests that mycetomic structures should be found in some of the sexual species of the Psocoptera as well If this is the case, then the ancestral function of the mycetomes was to hold nutritional symbionts after all . Our assumptions about which diets will require symbiotic supplementation might need to be refined

Our current assumptions are that nutritionally poor diets require addition or enhancement from symbiotic bacteria or yeasts An evolutionary reconstruction proposes that phloem sap and blood have become nutritionally deficient to limit exploitation of plants and animals by phloem sap and blood-sucking insects upon which the insects then adopted supplementation by symbionts This might certainly be the case for many species An additional hypothesis might be that a species loses its ability to utilize or uptake certain essential nutritional factors from a rich diet Should such a loss happen early in a lineage, obligate symbiosis might become widespread if uptake is a limiting factor and patchy if utilization is the problem A deficiency in utilization or uptake of nutrients from a diet and subsequent compensation through symbiosis might have preadapted some lineages to explore nutritionally poor diets This would provide a scenario where nutritional symbiosis is already in place before a switch from a free-living to a parasitic life style and diet takes place The nutritional symbiosis has become a prerequisite for ecto-parasitism

A partial example for such a host-symbiont interaction can be found in the case of the human head and body lice Human lice depend completely on nicotinamide or vitamin B3 being supplied by their primary endosymbiont This is not because blood does not contain sufficient amounts In fact, human blood contains double to fivefold the amount required by the louse. Almost all of it resides in the blood cells . Unlike some other blood-sucking insects, human lice are practically unable to lyse human blood cells and therefore cannot utilize nutrients present in their diet It is tempting to assume that the ancestral lice might have had the ability to lyse blood cells and the genes for the enzymes responsible might have been lost All extant phthirapteran lice are parasitic This means that for the last 160 million years the genomes of lice species must have undergone profound genome reduction characteristic for parasites Human body and head lice have indeed the smallest genomes of any hemimetabolous insect reported to date (Johnston et al , 2007) The sizes are just above 100 Mb with most of the genomes noncoding The loss of the genes for lysing blood cells might have been a consequence of the genome reduction due to the parasitic life style In the end, the parasitic life style of lice enforces or even initiates obligate nutritional endosymbiosis

Our hypothesis here is that Rickettsia are obligate or primary symbionts of partheno-genetic Psocoptera enabling reproduction of their hosts and have secondarily overtaken mycetomic provisions originally evolved for nutritional symbionts This view is corroborated by several anomalies in the interaction between the obligate symbiont and its host The oocytes in booklice are infected both through the germ line and through the nurse cells . Reproductive parasites are mainly transmitted through the germ line, whereas primary endosymbionts are transmitted via secondary tissues like nurse cells Rickettsia are found in three different types of tissue Rickettsia are housed in differentiated somatic tissues of organs, in single-cell mycetocytes, and in an organ-forming mycetome. In well-established mycetomic associations, the nutritional mycetomic endosymbiont does not infect other tissues; in booklice it does . Reproductive parasites like Wolbachia often infect some of the somatic tissues Occasional duplication of one of the mycetomes and the appearance of additional Malpighian tubules might represent another transitional stage, suggesting a very recent acquisition of Rickettsia by the host Fluctuating asymmetry is quite common in insects; however, organ duplications are very rare in the ontology of insects The duplication of one of the two mycetomes might suggest that the establishment of the new organ is still experiencing genetically some instability In most cases with centralized Malpighian infections, the nonadapted part of tubules is free from infections; in booklice it is not (Perotti et al ., 2006). The Rickettsia in L. bostrychophila are both intracellular and extracellular and found in nuclei This is another indication for a probable ongoing transition and evolution from parasite to obligate developmental symbiont A Rickettsia recently described in aphids in the sheet cells of the primary mycetome and in secondary myce-tocytes might be in a similar transitional stage (Sakurai et al , 2005) The aphid Rickettsia affects the fitness of its host In whiteflies, Rickettsia have been detected inside primary mycetocytes together with the primary endosymbiont (Gottlieb et al , 2008) The booklice Rickettsia might be in the transition from pathogen and secondary symbiont to obligate reproductive parasite and primary symbiont; the Rickettsia species in aphids might be in the transition from pathogen and secondary symbiont to nutritional and primary symbi-ont (Perotti et al ., 2006; Braig et al ., 2008) .

The Best Home Remedies For Head Lice

The Best Home Remedies For Head Lice

Discover The Best All Natural, Inexpensive Home Remedies For Treating and Preventing Head Lice No Matter How Severe The Case.

Get My Free Ebook

Post a comment