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Study of Steroidogenesis in Pupae of the Forensically Important Blow Fly Protophormia Terraenovae (Robineau-Desvoidy) (Diptera

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Study of Steroidogenesis in Pupae of the Forensically Important Blow Fly Protophormia Terraenovae (Robineau-Desvoidy) (Diptera Forensic Science International 160 (2006) 27–34 www.elsevier.com/locate/forsciint Study of steroidogenesis in pupae of the forensically important blow fly Protophormia terraenovae (Robineau-Desvoidy) (Diptera: Calliphoridae) Emmanuel Gaudry a,*, Catherine Blais b,1, Annick Maria b, Chantal Dauphin-Villemant b a Institut de Recherche Criminelle de la Gendarmerie Nationale, 1 Boulevard The´ophile Sueur, F-93111 Rosny-Sous-Bois Cedex, France b Biogene`se des ste´roı¨des, FRE 2852, CNRS, Universite´ Pierre et Marie Curie, Case 29, 7 quai St. Bernard, F-75252 Paris Cedex 05, France Received 23 August 2004; accepted 20 June 2005 Available online 23 September 2005 Abstract Protophormia terraenovae is a forensically important fly whose development time is studied by forensic entomologists to establish the time elapsed since death (post-mortem interval, PMI). Quantity and nature of ecdysteroid hormones present in P. terraenovae pupae were analysed in order to determine if they could be correlated to the age of pupae found on corpses and thereby could give information on the PMI. Ecdysteroid levels were quantified during the pupal–adult development of synchronised animals using enzyme immunoassay (EIA), a sensitive method allowing acurate quantification in one pupa. Two types of pupae were compared: ‘‘fresh’’ pupae, kept frozen until analysis and ‘‘experimentally dried’’ pupae, which were left for several weeks at ambient temperature. A peak of ecdysteroids was detected between 36 and 96 h after pupariation in fresh animals. It was not observed in ‘‘experimentally dried’’ pupae. High-pressure liquid chromatography (HPLC) analyses combined with EIA showed that 20-hydroxyecdysone (20E) was the major free ecdysteroid at various pupal ages. Enzymatic hydrolysis experiments revealed the presence of apolar conjugates at all ages tested. However, neither qualitative nor quantitative difference was detected between early and late pupae. This study gives precise information on the nature and quantity of ecdysteroids in the course of pupal development of a calliphorid fly. The limits of using ecdysteroid measurement as a tool in forensic entomology are discussed. # 2005 Elsevier Ireland Ltd. All rights reserved. Keywords: Forensic entomology; Ecdysteroids; Protophormia terraenovae; Pupal–adult development 1. Introduction Forensic entomology is described as the field where study of insects (and more generally arthropods) interacts with legal matters [1]. It can help to estimate the time elapsed * Corresponding author. Tel.: +33 1 58 66 50 92; fax: +33 1 58 66 50 27. since death, the so-called ‘‘post-mortem interval’’ (PMI) [2], E-mail addresses: [email protected] by determining the age of immature stages of necrophagous (E. Gaudry), [email protected] (C. Blais). insects collected on a human cadaver and around, from the 1 Tel.: +33 1 44 27 22 63; fax: +33 1 44 27 23 61. scene of crime and autopsy. 0379-0738/$ – see front matter # 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2005.06.014 28 E. Gaudry et al. / Forensic Science International 160 (2006) 27–34 Necrophagous insects (mainly flies) are attracted by the Thanks to the advent of immunoassays and high-perfor- odours produced by a decaying corpse. Females lay eggs or mance chromatographic methods (see ref. [10]), quantitative larvae directly into natural openings and wound sites. Me´g- and qualitative analyses of ecdysteroids have been done nin [3] described a succession pattern of insects and other during post-embryonic development of various insect spe- arthropods on a cadaver, eight ‘‘waves’’ from death until the cies, but only in a small number of calliphorid flies, mainly skeleton stage, due to modifications induced by the decom- Calliphora sp. [11]. The presence of both ecdysone and 20- position. Flies (Diptera) are the first insects to invade a hydroxyecdysone in pupae of two Calliphora species has cadaver and are predominant. This is why determination of been demonstrated [12] and ecdysteroid metabolism has when necrophagous flies started to colonise a corpse (ovi- been extensively studied in the blue blow fly Calliphora position or larviposition) gives an estimate of the PMI. vicina (review in refs. [11,13]). In P. terraenovae, only Dipterans undergo a post-embryonic development com- ecdysteroids present in adult females have so far been prising several stages separated by moults. Larvae live on or studied [14,15]. Identification and quantification of ecdys- in the corpse, which constitutes their nutritional substrate. At teroids in pupae could possibly help to determine their age the end of the third larval instar, maggots migrate away from and thus give an estimate of PMI. In order to examine this the corpse in order to find an adequate site to pupate, either in question, we studied the level and the nature of ecdysteroids the soil when outdoors or under furniture, carpets and so throughout the pupal stage of P. terraenovae. forth when indoors. Metamorphosis is achieved during the pupal stage and at its conclusion the adult fly (imago) emerges from the puparium. The duration of this develop- 2. Materials and methods ment cycle varies according to species and environmental conditions, especially temperature. 2.1. Insects Marchenko [4] reported that the embryonic and post- embryonic development rate of necrophagous flies can be P. terraenovae were bought in a fishing tackle shop near estimated using temperature summation, the accumulated Paris, and came from the south of France. Specimens were degree days (ADD) model. Above a specific threshold, each reared until adult emergence in plastic boxes (260 species needs a specific amount of degree days to develop. mm  130 mm  77 mm, with a 20–30 mm thick layer of The blow fly Protophormia terraenovae (Robineau-Des- sand) placed inside an incubator (Snijders Economic Delux) voidy) (Diptera: Calliphoridae) has a holarctic distribution at 24 8C with 75–95% relative humidity and a photoperiod of and is often associated with the necrophagous fauna, in the 12-h light:12-h dark hours. The rearing substrate was fresh first waves of insect succession [3]. This species is known to beef muscle of uniform quality. Development time from egg oviposit shortly after death and its temperature dependent to adult lasted about 330 h. About 30 adults were transferred development [5,6] can be used to estimate the PMI. Pupation into plastic cages (300 mm  500 mm  500 mm) at ambi- takes place on the surface of the nutritive medium or very ent temperature (20 Æ 2 8C) for mating and were provided close to it [7]. The duration of the pupal stage is relatively with sugar and water. After 1 week, beef blood was supplied long, representing 43% of the total developmental time, in for 2 h in the cages to stimulate maturation of eggs of adult comparison to the third larval instar: 13% for the feeding females that fed on it. One day later, sugar was replaced by a stage and 22% for the post-feeding phase [5]. piece of fresh beef muscle of uniform quality. Within 30 min Rearing pre-imaginal stages of necrophagous insects, of oviposition, eggs and substrate were transferred into species identification, study of their developmental time plastic boxes. First instar larvae were distributed to different and analysis of the temperature data, together provide an plastic boxes containing 40 g of beef muscle, which was estimation of the PMI [2]. But sometimes, forensic ento- replaced regularly, to avoid food shortage competition. mologists [8] receive dead pupae or animals which died during rearing. Dissection and examination of pupae can 2.2. Synchronisation of immature instars give some information on their age ([9]; Pasquerault, unpub- lished data). However, it would be beneficial to find an The larval instars were identified by observation of the alternative and/or complementary method to estimate the posterior spiracular slits under a binocular microscope. At age of pupae. the beginning of the third instar, larvae were transferred into Ecdysteroids are polyhydroxylated steroid hormones that new boxes (50 individuals with 100 g of beef muscle, are essential for insect development and reproduction. They supplied regularly). When they stopped feeding, they were trigger transitions between developmental stages, control- transferred into another set of plastic boxes, containing sand ling moulting and metamorphosis processes, via their per- only. iodical fluctuations. 20-Hydroxyecdysone (20E) is regarded From the first appearance of the immobile white puparia as the principal active ecdysteroid in most species. It comes until adult emergence, pupae were collected every 6 h from the transformation by peripheral tissues, of the ‘pro- (Æ1 h) and transferred into a freezer at À22 8C. Pupae were hormone’ ecdysone (E), synthesised and secreted by ecdy- not sexed, as it was not possible to remove them undamaged sial glands, the endocrine glands producing ecdysteroids. from the puparia. Experimentally dried specimens were E. Gaudry et al. / Forensic Science International 160 (2006) 27–34 29 also studied. They were obtained by leaving thawed pupae with a flow rate of 1 mL/min. Some analyses were per- from all ages, at ambient temperature (20 Æ 2 8C) for 5 formed by reverse-phase HPLC (RP-HPLC) on a Spherisorb weeks. ODS2 column (AIT), with a flow rate of 1 mL/min, using a linear gradient of solvent B (acetonitrile/propan-2-ol, 5:2, v/ 2.3. Extraction of ecdysteroids v) in solvent A (0.1% trifluoroacetic acid in water). Fractions of 0.5 mL were collected, evaporated until dry and resus- Each pupa was cleaned, weighed, cut with scissors into pended in EIA buffer for ecdysteroid quantification. two pieces and homogenised in 70% methanol (Merck) The retention times of immunoreactive fractions were (1 mL/10 mg) in Eppendorf tubes with a plastic pestle. compared to the following reference ecdysteroids: 20E, The homogenate was centrifuged and the pellet resus- ecdysone (E), 3-dehydro-ecdysone (3DE) and 3-dehydro- pended in 70% methanol, for a second extraction (see 20-hydroxyecdysone (3D20E).
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