Learning to fly

Sarah Diamond, Stanley Diamond's daughter, is a writer and a student of English Literature and Theater at Barnard College, New York City.     

Phagocytosis and comparative innate immunity: learning on the fly

Phagocytosis, the engulfment of material by cells, is a highly conserved process that arose before the development of multicellularity. Phagocytes have a key role in embryogenesis and also guard the portals of potential pathogen entry. They discriminate between diverse particles through the array of receptors expressed on their surface. In higher species, arguably the most sophisticated function of phagocytes is the processing and presentation of antigens derived from internalized material to stimulate lymphocytes and long-lived specific immunity. Central to these processes is the generation of a phagosome, the organelle that forms around internalized material. As we discuss in this Review, over the past two decades important insights into phagocytosis have been gleaned from studies in the model organism Drosophila melanogaster.     

Sex and immunity in the yellow dung fly Scathophaga stercoraria

The immune system is of increasing interest to evolutionary biologists. Immunity may trade-off against other fitness components, with recent work suggesting reproduction in particular impinges on immune defence. There may also be sex differences in the immune system. Additionally, while life history traits typically have low heritability, little is known about additive genetic variance of immunity. An insect's major defence against multicellular pathogens is to encapsulate the invader. Phenoloxidase (PO) is a key enzyme in the cascade resulting in the melanized capsule, and is often used to estimate resistance to an immune insult. We examined the effects of copulation, egg laying, sex and age on PO in Scathophaga stercoraria. We also measured the heritability of PO activity. The sexes differed in haemolymph PO activity and PO was significantly affected by age, but not by copulation or egg laying. There was significant heritable variation for haemolymph PO.     

Learning to protect your genome on the fly

Piwi-interacting RNAs (piRNAs) help defend host genomes against germline transposons. In this issue of Cell, Khurana et al. show how alterations in the piRNA-encoding loci within a single generation allow a naive fly genome to overcome the initially insurmountable challenge imposed by a newly encountered mobile element.     

Sand fly specificity of saliva-mediated protective immunity in Leishmania amazonensis-BALB/c mouse model

Immune response of BALB/c mice to the salivary antigens of sand flies was found to vary with different species used, i.e. Phlebotomus papatasi, Phlebotomus sergenti and Lutzomyia longipalpis. Exposure of mice to bites of these sand flies elicits production of antibodies, which are largely specific to different saliva antigens previously identified as unique to the respective fly species. When immunized intradermally (i.d.) with salivary gland lysates (SGL) of L. longipalpis, BALB/c mice developed partial protective immunity against challenges in the contralateral ears with Leishmania amazonensis plus the gland lysates. Preimmunization of these mice with the lysates from the other two species was ineffective, further indicative of the specificity of saliva-mediated immune response. The partial protective immunity observed is significant, although it is not as dramatic as reported previously in a different sand fly-mouse model. There is a correlation of this immunity with a lower number of mononuclear and polymorphonuclear phagocytes at the site of parasite inoculation. Vector species-specificity of this immunity implies its elicitation by unique saliva antigen-an issue which requires attention when designing saliva-based vaccines against leishmaniasis.     

Reactive oxygen species-mediated immunity against Leishmania mexicana and Serratia marcescens in the sand phlebotomine fly Lutzomyia longipalpis

Phlebotomine sand flies are the vectors of medically important Leishmania. The Leishmania protozoa reside in the sand fly gut, but the nature of the immune response to the presence of Leishmania is unknown. Reactive oxygen species (ROS) are a major component of insect innate immune pathways regulating gut-microbe homeostasis. Here we show that the concentration of ROS increased in sand fly midguts after they fed on the insect pathogen Serratia marcescens but not after feeding on the Leishmania that uses the sand fly as a vector. Moreover, the Leishmania is sensitive to ROS either by oral administration of ROS to the infected fly or by silencing a gene that expresses a sand fly ROS-scavenging enzyme. Finally, the treatment of sand flies with an exogenous ROS scavenger (uric acid) altered the gut microbial homeostasis, led to an increased commensal gut microbiota, and reduced insect survival after oral infection with S. marcescens. Our study demonstrates a differential response of the sand fly ROS system to gut microbiota, an insect pathogen, and the Leishmania that utilize the sand fly as a vehicle for transmission between mammalian hosts.     

The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly

Tsetse flies (Diptera: Glossinidae) are vectors for trypanosome parasites, the agents of the deadly sleeping sickness disease in Africa. Tsetse also harbor two maternally transmitted enteric mutualist endosymbionts: the primary intracellular obligate Wigglesworthia glossinidia and the secondary commensal Sodalis glossinidius. Both endosymbionts are transmitted to the intrauterine progeny through the milk gland secretions of the viviparous female. We administered various antibiotics either continuously by per os supplementation of the host blood meal diet or discretely by hemocoelic injections into fertile females in an effort to selectively eliminate the symbionts to study their individual functions. A symbiont-specific PCR amplification assay and fluorescence in situ hybridization analysis were used to evaluate symbiont infection outcomes. Tetracycline and rifampin treatments eliminated all tsetse symbionts but reduced the fecundity of the treated females. Ampicillin treatments did not affect the intracellular Wigglesworthia localized in the bacteriome organ and retained female fecundity. The resulting progeny of ampicillin-treated females, however, lacked Wigglesworthia but still harbored the commensal Sodalis. Our results confirm the presence of two physiologically distinct Wigglesworthia populations: the bacteriome-localized Wigglesworthia involved with nutritional symbiosis and free-living Wigglesworthia in the milk gland organ responsible for maternal transmission to the progeny. We evaluated the reproductive fitness, longevity, digestion, and vectorial competence of flies that were devoid of Wigglesworthia. The absence of Wigglesworthia completely abolished the fertility of females but not that of males. Both the male and female Wigglesworthia-free adult progeny displayed longevity costs and were significantly compromised in their blood meal digestion ability. Finally, while the vectorial competence of the young newly hatched adults without Wigglesworthia was comparable to that of their wild-type counterparts, older flies displayed higher susceptibility to trypanosome infections, indicating a role for the mutualistic symbiosis in host immunobiology. The ability to rear adult tsetse that lack the obligate Wigglesworthia endosymbionts will now enable functional investigations into this ancient symbiosis.     

Learning deficits occur in young mice following transfer of immunity from senescent mice

The extent to which immune processes contribute to senescence-related neurological/behavioral impairment was examined using an adoptive transfer procedure. C57BL/6 mice aged 22 to 24 months showed impaired ability for acquisition of an active avoidance response when compared with younger mice aged 3 months. An immunofluorescence assay of the sera of these mice indicated that only sera from the senescent mice reacted with brain antigen. When tested three months following irradiation and receipt of bone marrow/spleen cell suspensions from senescent mice, young mice showed senescence-like serum-brain reactivity and declines in their abilities to acquire learning. Young control mice receiving cell suspensions from age-matched donors showed no evidence of serum-brain reactivity or learning deficits, suggesting that impaired learning was related to acquisition of aged immunity and not a nonspecific effect of the transfer procedure. These findings indicate that immune processes may be involved in the etiology of senescence-related neurological/behavioral dysfunctions.     

The chemical ecology of the fly

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Converting neural signals from place codes to rate codes

 The nervous system uses two basic types of formats for encoding information. The parameters of many sensory (and some premotor) signals are represented by the pattern of activity among an array of neurons each of which is optimally responsive to a different parameter value. This type of code is commonly referred to as a place code. Motor commands, in contrast, use rate coding: the desired force of a muscle is specified as a monotonic function of the aggregate rate of discharge across all of its motor neurons. Generating movements based on sensory information often requires converting signals from a place code to a rate code. In this paper I discuss three possible models for how the brain does this. Received: 24 July 2000 / Accepted in revised form: 2 February 2001     

Dispersal of the cabbage root fly

The dispersal rates of wild and culture cabbage root flies Erioischia brassicae were determined in release-recapture experiments at Wellesbourne in 1971–3. The experiments were concerned mainly with the first 7 days of adult life. The flies, released from nine locations in the area, were recaptured in yellow water-traps. Dispersal was affected by wind, rain and the terrain the flies were crossing. The flies least often recaptured were those released into the host crop when 6–12 days old. The results indicated the following pattern of behaviour. Flies moved little during the first 2 days of adult life but by the third day both sexes had dispersed to c. 100 m from the release point. Flies are known to mate about the fourth day and after this the males continued to disperse at c. 100 m per day for the three subsequent days. ‘Wild’ females from field-collected pupae carried out a ‘migratory’ flight, however, and dispersed at c. 1000 m per day during the fifth and sixth days, the days preceding the start of oviposition. Similar rates of dispersal were recorded from flies released across host crop and non-host crop areas. Some females did not stop at the first crop they encountered. The culture females from the laboratory-reared pupae dispersed only c. one-third of the distance of the wild females. There was considerable intermingling of local populations. The percentage recapture of young culture and wild flies released during the pre-oviposition period of this species was 38 ± 4 and 19 ±4 for males, and 15 + 2 and 8+1 for females, respectively. The dispersal range of the cabbage root fly is probably within a 2000–3000 m radius of the site of infestation.