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The Evolution of Myiasis in Humans and Other Animals in the Old and New Worlds (Part II): Biological and Life-History Studies

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The Evolution of Myiasis in Humans and Other Animals in the Old and New Worlds (Part II): Biological and Life-History Studies Review TRENDS in Parasitology Vol.22 No.4 April 2006 The evolution of myiasis in humans and other animals in the Old and New Worlds (part II): biological and life-history studies Jamie R. Stevens1, James F. Wallman2, Domenico Otranto3, Richard Wall4 and Thomas Pape5 1School of Biosciences, University of Exeter, Prince of Wales Road, Exeter, UK, EX4 4PS 2Institute for Conservation Biology, School of Biological Sciences, University of Wollongong, New South Wales 2522, Australia 3Faculty of Veterinary Medicine, University of Bari, Strada Provinciale per Casamassima km 3, 70010 Valenzano, Bari, Italy 4School of Biological Sciences, University of Bristol, Woodland Road, Bristol, UK, BS8 1UG 5Zoological Museum, Entomology Department, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark Myiasis, which is the dipteran parasitism of living the evolution of life-history traits such as myiasis. vertebrates, occurs in several forms – ranging from Additionally, such data can be supplemented by: (i) the benign to fatal, opportunistic to obligate – and seems to addition of studies of host biology to help interpret have evolved through two distinct routes: sapropha- patterns of parasite–host coevolution; and (ii) fossil gous and sanguinivorous. However, the convergent data, which can help to pinpoint the dates of divergence evolution of morphological and life-history traits events observed in phylogenies. Without fossil data, seems to have had a major role in confusing the overall tree-derived divergence times often depend on rates of picture of how myiasis evolved and this simplistic molecular evolution that are calculated from molecular division is further complicated by the existence of both clocks, the reliability and characteristics of which vary ectoparasitic and endoparasitic species of myiasis- widely among genes, taxa and timescales. causing Diptera, the evolutionary affinities of which A better understanding of the evolution of myiasis is remain to be resolved. As discussed in part I of this not only of intrinsic scientific interest but might also have review, if we are to elucidate how the different forms of applied value, as alluded to in part I [1]. For example, parasitism arose, it is essential to separate the evolution knowledge of the immunological, physiological and bio- of the various groups of myiasis-causing flies from the chemical strategies that enable the larvae of some evolution of the myiasis habit per se. Accordingly, myiasis-causing species to survive nonspecific (e.g. natu- whereas we focused on recent landmark phylogenetics ral killer cells and complement proteins) and specific (e.g. studies in part I, we use this framework to analyse antibodies and T cells) immunological responses of a host relevant biochemical, immunological, behavioural, bio- provides ideal targets for the development of immunologi- geographical and fossil evidence to elucidate the cal methods for the early detection of these species in evolution of myiasis in part II. livestock [3,4]. Similarly, an understanding of larval secretions has proven beneficial for understanding the basis of larval therapy [5]. Interpreting the evolution of myiasis through life-history The recent studies that have reconstructed evolution- characteristics ary relationships among the key lineages of myiasis- A robust phylogenetic framework enables the evolution- causing flies – Calliphoridae (blowflies), Sarcophagidae ary relationships between myiasis-causing flies to be (flesh flies) and Oestridae sensu lato (bot flies) – were interpreted and patterns of the evolution of myiasis per reviewed in part I [1]. Having established a working se to be reconstructed, as discussed in part I of this knowledge of the phylogenies available for Diptera that review [1]. Here, we adopt Zumpt’s [2] definition of parasitize vertebrates, we now focus on the diverse forms myiasis as being the infestation of the tissues of live of data available from a range of independent biological vertebrates (humans and/or animals) by dipterous and archaeological sources that are key to corroborating larvae (see Box 1 in part I for full explanation [1]). or, indeed, contradicting the relationships defined by Given such phylogenies, a wealth of morphological, these phylogenies. biochemical and immunological data can also be used to provide independent evidence with which to interpret Mechanisms of myiasis Corresponding author: Stevens, J.R. ([email protected]). Characteristically, members of the Oestridae family are Available online 28 February 2006 all obligate, host-specific gastrointestinal or subdermal www.sciencedirect.com 1471-4922/$ - see front matter Q 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.pt.2006.02.010 182 Review TRENDS in Parasitology Vol.22 No.4 April 2006 larval parasites that undergo long periods of association recent phylogenetic analysis [9] has highlighted the with the host and usually have relatively low levels of close relationships between important myiasis-causing pathogenicity. By contrast, not all species of Calliphoridae flies and non-parasitic, or facultatively parasitic, carrion- and Sarcophagidae are parasitic. However, the species of breeding sister taxa, including both Old World and New these families that are agents of myiasis are characterized World screwworm flies (see part I [1]). In the Calliphor- by lower host-specificity, shorter periods of larval feeding, idae and Sarcophagidae, the saprophagous obligate or a relatively superficial or cutaneous location in the host facultatively parasitic sister species are all morphologi- and relatively high levels of pathogenicity. Nevertheless, cally similar and are distinguished by only minor fundamental common changes in behaviour and physi- character differences. ology are likely to have been associated with the evolution It is unknown why groups of morphologically similar of all species towards parasitism. For example, the larvae and closely related species of Calliphoridae and Sarco- of all of the parasitic species must be able to survive the phagidae behave in such different ways. But, in the immune challenge, the high body-temperatures of ver- absence of obvious morphological differences between the tebrates [6] and the differences in diet presented by a larvae, it can be speculated that these distinct behaviours living vertebrate host. might be mediated by differences in temperature toler- In the Oestridae family, such general adaptations to a ance, response to immune challenge and/or the production parasitic lifestyle have been accompanied by changes in of different arrays of enzymes, particularly those associ- larval morphology and enzymic repertoire. For example, ated with feeding on the tissues of a living host. the larvae of Oestrinae and Gasterophilinae (which infest Differences between adults of parasitic (obligate and the nasopharyngeal region and the gastrointestinal tract, facultative) and strictly saprophagous species might be respectively) have characteristic, relatively large mouth- controlled by their responses to semiochemical cues that hooks and rows of well-developed spines on the dorsal enable the parasitic species to locate and oviposit on a and/or ventral side of each body segment. These spines are living host, although there is no evidence to confirm this thought to be crucial for the migration of the larvae within hypothesis at present. the host and, at an intergeneric level, their arrangement is distinctive; within genera, however, they are unreliable Morphology, convergent evolution and homoplasy for phylogenetic analyses. The proteases produced by It is usually accepted that both molecular and morpho- these larvae are involved largely in enabling them to logical characters can be subject to convergent evolution survive the host immune system [3]. Nevertheless, such and homoplasy. Certainly, the lack of congruence observed morphological features are not universal in the Oestridae, between phylogenies based on morphological characters and in the Hypodermatinae the larval stages have only [14] and molecular sequence data [9,15] can be explained vestigial mouth-hooks and poorly developed larval spinu- only by the existence of homoplasy. Within each family, lation. In contrast to the relatively limited larval protease however, the limitations of employing morphological repertoire of Oestrinae and Gasterophilinae, however, the characters for phylogenetic and taxonomic purposes first-stage larvae of Hypoderma spp. secrete three major seem different, especially with regard to immatures. serine proteases (chymotrypsin and hypodermins) during The Calliphoridae and Sarcophagidae are character- their migration through host tissue [3]. Importantly, these ized by having typical musciform larvae that are proteases are involved not only in combating the host segmented and pointed at the anterior end with no head- immune responses but also in larval migration [7,8]. Thus, capsule, whereas the posterior end is broad and usually changes in larval morphology in Oestridae complement truncate; the head and first thoracic segment contain the the development of appropriate enzymic characteristics cephaloskeleton, which bears the mouth-hooks, whereas and seem to be associated with larval migration through the last segment bears the posterior spiracles and the the tissues of the host. anus. Perhaps surprisingly, an obvious relationship Such characteristics are not seen in the parasitic between the structure and size of larval mouth-hooks Calliphoridae and Sarcophagidae, in which there is no and the life-history strategy
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