•

fl/lerl/oliol/o/ JOI/rl/o/for Parasil%gy, Vo!. 24. No. 8, pp. 1273-1283, 1994 Copyright f.) 1994 Australian Society ror Parasitology ~ Pcrg.mon Elsevier Science Lld Printed in Great Dritain. All rights reserved 0020-7519/94 S7.00 + 0.00

002Q-7519(94)OOl09-X ADAPTATION, SPECIFICITY AND HOST-PARASITE COEVOLUTION IN ()

ALEX FAIN Institut Royal des Sciences naturelles de Belgique, rue Vautier 29, B-1040 Bruxelles, Belgium,

Abstract-Fain A. 1994. Adaptation, specificity and host-parasite coevolution in mites (Acari). Interndtional Journal for Parasitology 24: 1273-1283. Parasitism by mites is widespread and involves all the ~Iass~s of vertebrates, f~om fishes to mammals. Owing to their small size and their great plasticity, mites are able to adapt to a wide range of habitats. Most of the species are ectoparasites but endopara­ sitism, especially in the respiratory tract, is common in birds and mammals. The morphological modifi­ cations appearing during the process adaptation to parasitic life, especially in Myobiidae, are analysed. Two kinds of characters are particularly important: the constructive specialized characters, consisting of the production of new structures, especially attachment organs allowing the to attach to the skin and the hail' of the host, and regressive characters, Regression of the external structures is the most important phenomenon appearing in the process of evolution of parasitic mites. The importance of the regression in the parasite is correlated with the degree of evolution of the host. Host and parasite have a parallel evolu­ tion, but they go in opposite directions. The author surmises that the regressive evolution is related to the immunological reactions of the host that tend to reject the parasite. To escape from this rejection the parasite tends to select the less antigenic and therefore the most regressed phenotype. Specificity is gener­ ally strict in permanent parasites, Coevolution of host and parastie is studied. in the family Myobiidae which parasitizes marsupials, insectivores, bats and rodents. The concordance between the radiations of the mites and that of their hosts is very high,

INDEX KEY WORDS: adaptation; specificity; coevolution; mites (Acari); mammals.

INTRODUCTION PARASITIC NICHES I would like to deal here with some aspects of Ectoparasitism parasitic life in mites (Acari), Parasitic mites, chiefly Mites are very plastic creatures, capable of adapt­ those from higher vertebrates, have been exten­ ing to very different conditions of life. Their small sively collected and researched during these last size enables them to occupy a very wide range of 3 decades and these studies have contributed sub­ habitats. Usually their body length ranges from 0.5 stantially to a better knowledge of these parasites, to 1mm, but in the smallest species this length does specially in regard to their classification, geo­ not exceed 0.1 mm. Most of the species are free graphic distributions, specificity and host-parasite living but there are also numerous parasitic forms coevolution. living on plants or on , both invertebrates and vertebrates. Among the invertebrates only 2 phyla, Le. the molluscs and the , espe­ CLASSIFICATION cially insects, are parasitized by mites, whilst in the Mites and ticks form the subclass Acari, in phylum Chordata (= Vertebrates), all the classes, the class Arachnida. They are divided into 7 from fishes to mammals, have been found to be orders, of which only 4 include parasitic forms, infected by them. Parasitism by mites is particularly i.e. the Metastigma ta, also called ticks, and the frequent in birds and mammals. A large number of Mesostigmata, and Astigmata, forming species are ectoparasitic and live on the skin or in the the group of mites (Evans, Sheals & Macfarlane, superficial layers of the skin, where they feed on the 1961). Ticks are generally distinctly larger than corneous material of the skin or on the blood or the mites and they are all obligate parasites of verte­ lymph that they suck by means of specialized pierc­ brates: The 3 orders of mites include both free-!iving ing mouth pieces. The fea thers of birds are colonized forms and parasites. In this paper I will deal only by about 2000 species. These mites are generally with mites. highly specialized and they feed on the corneous

1273 1274 A. FAIN material desquamating from the feathers (Gaud & infected. Three families of mites are completely Atyeo, 1982). Fur mites of mammals also form a restricted to this habitat: i.e. Halarachnidae (Meso­ large group. The most important are the stigmata), Pneumocoptidae (Astigmata) and Lem- Listrophoroidea (Astigmata) (about 1000 species) . urnyssidae (Astigmata). The Halarachnidae, and the Myobiidae (Prostigmata) (more than 400 represented by 6 genera and 34 species, parasitize 15 species). families of manunals (Furman, 1979). This family is homologous to the Rhinonyssidae living in birds. Endoparasitism Both groups probably derive from the ectoparasitic Endoparasitism by mites is widely distributed in Mesostigmata (Macronyssidae) living on these hosts vertebrates and it affects especially birds. Most of (Radovsky, 1985). The Pneumocoptidae are repre­ the species live in the respiratory tract of their sented by I genus and 3 species living in the lung of hosts, from the nasal cavities to the air-sacs. Until North American and European rodents (Baker, now more than 500 species have been described in 1951), and the family Lemurnyssidae, 2 genera and 4 birds from this habitat; they belong to 3 orders species, occupying the nasal cavities of the~African and 5 families of mites. Three of 'these families Ga/ago and of Neotropical monkeys (Fain, I 964b). (Turbinoptidae, Cytoditidae and Rhinonyssidae) are Another family, Gastronyssidae (Astigmata) completely restricted to this habitat (Fain, 1957, representd by 3 subfamilies, is endoparasitic in bats 1965b). In the nasal cavities of birds the various and rodents: Gastronyssinae, Rodhainyssinae and species are not distributed randomly but they occupy Yunkeracarinae. The Gastronyssinae, with 1 genus distinct sites according to the family to which they and species, GastrollYssuS bakeri, is a common para­ belong. The Turbinoptidae (Astigmata) are confined site of the stomach of the African Megachiroptera. to the superficial cutaneous parts of the nasal cavi­ The Rodhainyssinae, with 4 genera and 18 species ties and they never invade the deeper cavities. These are confined to the nasal cavities and the conjuncti­ species have strong chelicerae and feed on the val sac of bats, both Mega and Microchiroptera. The corneous layers of the skin. A second family, third subfamily, Yunkeracarinae, with 2 genera and Rhinonyssidae (Mesostigmata),' includes only 5 species is restricted to the nasal cavities of rodents blood sucking species living on the mucosa of the (Fain, 1964a, 1967). turbinates. Among this family 1 species, Sterno­ Besides the respiratory passages, mites have also stoma tracheacolum, lives in the trachea and the been found under the skin or in the deeper cellular bronchi and may cause pneumonia. A third family, tissues around the muscles, e.g. Epimyodicinae in Cytoditidae (Astigmata) includes a few very small Ta/pa europaea and rats (Fain, Lukoschus & mites living in the deeper parts of the nasal cavities Rosmalen, 1982) and in the hair follicles, e.g. including the nasal sinuses. One of these species, Demodicidae (Nutting, 1985), Rhyncoptidae CylOdites nudus infects the air-sacs where it feeds on (Lawrence, 1956; Fain, 1965a) and Audycoptidae exudate (Fain, 1960). The species of the fourth (Lavoipierre, 1964; Fain & Johnston, 1970). family, Ereynetidae (Prostigmata), do not have a Endoparasitism by mites is not restricted to higher defined niche but run freely through the entire nasal vertebrates but is also frequent in lower vertebrates cavity and they are covered by a whitish, water­ such as snakes: e.g. lung mites of the family repellant substance which prevents these mites from Entonyssidae, specific for these hosts (Fain, 1961), being caught by the mucus covering the turbinates, turtles: Cloacaridae, parasitizing the cloaca and the" The last family, Ascidae (Mesostigmata), includes muscles of their hosts (Camin, Moss, Oliver & about 40 species parasitizing the nasal cavities of Singer, 1967; Fain, 1968b), frogs and toads: hummingbirds (Trochilidae). These mites, actually, Ereynetidae parasitizing the nasal cavities (Fain, are not true parasites as they feed upon the nectar of 1962), and fishes: Histiostomatidae living in the flowers (Bromeliaceae, Heliconiaceae, Ericaceae, swim-bladder of an aquarium fish (Fain & etc.) and they are phoretically transported from Lambrechts, 1985). As a rule endoparasitic mites are flower to flower by these birds (Colwell, 1973; Fain, highly specific for both their hosts and the niche that 1992). Besides the respiratory passages, several other they occupy. endoparasitic niches are known in birds, e.g. feather The multiplicity of habitats occupied by mites follicles, in the shaft of the feathers, under the skin demonstrates their ability to adapt to various condi­ or in the deeper cellular tissues enveloping the tions of life. No other group of parasites is capable viscera. of occupying such a wide range of parasitic niches. Endoparasitism is also widespread in mammals The 'chances of finding complete phylogenetic and, as in birds, the respiratory .tract is heavily lineages, including both ectoparasites and endopara- Host-parasite coevoJution in mites 1275 sites and often their nidicolous ancestors, is therefore and in domestic mammals (e.g. cats, dogs, horse, much greater in mites than in any other group of cattle, pig, sheep, etc). This species is very rare in parasites. In insects (fleas, lice, mallophaga, flies), wild animals living in their natural habitat but it ectoparasitism is almost the only form of parasitism, becomes frequent when these animals are sheltered whilst in helminths endoparasitism is the rule, except in zoos. More than 30 species and 15 varieties have for a small group of ectoparasitic Monogenea. Mites been described in the genus Sarcoptes. From 1962 to appear, therefore, as probably the most suitable 1968 I had the opportunity to examine, not only group of parasites in the study of host-parasite single specimens, but also good series of these coevolution. described species. This study has shown that all these "species" were based on variable characters without MULTIPLE SPECIATION taxonomic value and that there is only one valid but Multiple speciation is relatively frequent in the variable species in the genus Sarcoptes. The wide fur mites Of the superfamily Listrophoroidea. variability of S. scabiei suggests that this species is In Australia, the potoroo, Potorolls tridactylus, not completely adapted to any of the present hosts hCl;rbours 21 endemic species of the genus but remains in a continuous process of adaptation. 'Cytostethum (Atopomelidae) for a total of 15 The variability is probably related to the great potoroos examined (Fain & Domrow, 1974). number of hosts that this species is capable of Multiple speciation is particularly marked in the parasitizing. The mite causes scabies in 40 different beavers Castor jiber and C. canadensis. In U.S.S.R. hosts belonging to 17 families and 7 orders of Dubinina (1964) examined 22 beavers, Castor jiber, mammals. I have surmised that the frequent inter­ from the Voronesh Reservation, and found 12 breeding of the mite in zoologically remote, mostly endemic species of the genus Schizocarpus (Chiro­ domestic mammals, has prevented speciation and at discidae) and among them 11 were new. These the same time provided new genetic characters which investigations were continued by Fain & Lukoschus have enhanced the adaptability of the mite to infect (1985) who collected from 4 beavers (Cjiber) caught new hosts. The variability of S. scabiei is probably in the river Elbe, Germany. They found 25 species of the result ofcontinuous interbreeding in these strains Sch izocarpus, of which 21 were new, raising the (Fain, 1968a, 1978a). number of species living on this beaver up to 31. The Another highly variable species is Sternostoma North American beaver, Castor canadensis, is para­ tracheacolum (Rhinonyssidae) living in the respira­ sitized by 17 species of SchizOCQlpuS, all restricted to tory tract (nasal cavities, trachea and lungs) of birds this host and clearly distinct from the species found and causing pneumonia in the canary. This species in the European beavers. In both species of beavers has been found from 24 species, belonging to 11 most of the mites occupied specific nticrohabitats on families, of birds, mostly Passeriformes (Fain & the body and the head of the beavers (Fain & Hyland, 1962). Whitaker, 1988). Such extreme speciation is prob­ ably unique in parasitology. The cause of this SPECI.F1CITY AND COEVOLUTION phenomenon is not known but Fain & Lukoschus Host specificity in parasites of vertebrates has been (1985) supposed that it might result from the combi­ extensively treated in two international symposia. nation of 2 different mechanisms. The first process is The first was organized by J. Baer in NeucMtel, the isolation of the various populations of beavers Switzerland, in 1957. No paper on mites was in separate areas. The second mechanism is the presented. The second was held in Paris, in 1981 microisolation resulting from the existence on the (proceedings published in 1982). The organizer was beavers of different microhabitats differing from A. Chabaud. Among the 40 papers presented at this each other by the texture and the thickness of the symposium 4 dealt with parasitic mites, of which 2 hairs, the differences in the skin secretions, etc. were on ticks (Hoogstraal & Aeschlimann, Morel), 1 on feather-mites (Gaud & Atyeo) and 1 on VARIABILITY Myobiidae (Fain). Most recently, Kim (1985) Individual variations, Le. variations of morpho­ published a significant amount of data concerning logical characters within a population, are not rare host-specificity and coevolution of parasitic arthro­ in parasitic mites. It is an important question, for pods and mammals. Four chapters of this book dealt certain "new" species have been based on such vari­ with Acari. All the groups of mites are not equally able characters. In this respect I would like to recall suitable for the study of specificity and coevolution, here briefly the interesting history of Sarcoptes but the permanent parasites, Le. those that remain scabiei, a common parasite causing mange in man on their host during all their stages of development, 1276 A. FAIN

can be used for this purpose. In the case of mites morphological characters they recognized a primitive that leave their host periodically, such as ticks and from an evolved parasite and they did not make many ectoparasitic mesostigmates, specificity is low reference to the regressive characters appearing in and coevolution poorly marked. Pilicolous special­ the parasites during their evolution. Several authors, ization has induced a strong specificity, not only in Jameson (1955), Dusbabek (1969a,b), Uchikawa& mites (especially Listrophoroidea and Myobiidae) Harada (1981) and Uchikawa (1986, 1987), have but also in some insects, such as lice which are both given numerous examples of specificity and host­ permanent and highly specific. In these groups the parasite coevolution in mites of the family attachment to the hairs of their hosts has induced Myobiidae, especially in the species parasitizing bats, the production of highly specialized clasping organs confirming the observations of the preceding authors which prevent the parasite from attaching to other about the relationship between hosts and their para­ hosts. As a rule, host-specificity is marked in perma­ sites, but again they did not mention the role of nent parasites but exceptions are common (Fain, regression in the evolution of the parasites. 1975, 1977). In animals kept for long periods in Mites of the family Myobiidae parasitize 4 orders zoos, parasites may be transferred from their normal of mammals of particular interest in evolutionary host to atypical hosts living in close association with studies, marsupials, insectivores, bats and rodents. them. I have reported (Fain, Mignolet & Beresnay, Up to now 4 13 species and 37 su bspecies, belonging 1958) a case of infection by lung mites in an Asiatic to 49 genera and 23 subgenera have been described macaque in the zoo of Antwerp. This was in the Myobiidae. Fain (1969, 1974, 1977, 1982, infected by 3 species of Pneumonyssus (Halarach­ 1988) studying a large collection of myobiids from nidae) normally restricted to African cercopithecids various hosts and countries concluded that the most and never reported from Asia. The macaque had important phenomenon appearing during the probably been contaminated by the heavily infected process of evolution of parasitic mites is the regres­ African cercopithecids living in association with it. sion of the external structures. These observations Low host-specificity has also been reported in are summarized below. Rhinonyssus rhinoletl'um (Rhinonyssidae), a common Complication of structures is a general trend in the nasal mite parasitic in Anseriformes, specially in evolution of animals. In parasitic mites, and that is ducks. This species has been recovered from 40 also true for many other parasites, evolution, at least species of Anatidae belonging to 20 genera (Fain, that which concerns the external structures, is of the 1'965b). According to Strandtmann (1958) the lack regressive type. That means that myobiids living on of specificity in this mite might be explained by evolved hosts show more regressive characters than the gregariousness of the aquatic birds creating those living on primitive hosts. The host and the favourable conditions for the transfer of the mites. parasite follow a parallel course of evolution, Gaud & Atyeo (1982) observed that the feather although they go in opposite directions. Moreover in mites living on aquatic birds are less specific than the same evolutionary line, the endoparasitic mites those from terrestrial birds, probably for the same always show more regressive features than their reason. Two other examples of low specificity in ectoparasites, their probable ancestors (Fain, 1969, permanent parasitic mites are those of Sarcoptes 1974). Regression in parasites probably involves scabiei and Sternostoma tacheacolum. only external structures, and there is no apparent reason that the internal organs should not follow the IMPORTANCE OF REGRESSION IN THE general trend of complication. An argument in EVOLUTION OF MYOBIID MITES favour of this view is the fact that primitive myo­ Fahrenholz (1909) during his researches on biids have never been found on evolved hosts, Anoplura and Mallophaga noted the narrow rela­ while the reverse, e.g. the occasional presence of tionships between hosts and their parasites. In 1913, an evolved species on a primitive host, is not rare. he concluded that in hosts of different species, the Evolved (regressed) parasites are probably capable parasites diverge from one another to the same of adapting to both primitive and evolved hosts, degree as their hosts are related (in Eichler, 1942, whilst primitive parasites seem to be unable to colo­ cited by Klassen, 1992). Szidat, 1940 (in Eichler, nize evolved hosts. 1942, cited by Klassen, 1992) postulated that prim­ The mechanism of regression of the external struc­ itive hosts harbour primitive parasites. This author tures of the parasites is not known. I have proposed explained the close relationship between host and the hypothesis that regression is a result of the parasite lineages by orthogenesis. (= progressive immunological reactions of the host which tends to evolution). These authors did not explain by which reject the parasite in the same way that it rejects any Host-parasite coevolution in mites 1277 other foreign antigen. To escape from the rejection and it dates probably from the time of emergence of the mite tends to select less antigenic and therefore the order hosts. the most regressed phenotype (Fain, 1979). This character of leg I allows the recognition of 3 There is generally a good correlation between the main groups in the Myobiidae but it does not degree of regression in the parasite and the degree provide valuable information concerning the degree of evolution of the host. Moreover, the regression of of evolution of the different genera of each group. the structures is gradual and quantifiable so that it Two other characters may, accordingly, be used for is possible, to some extent, to evaluate indirectly the this purpose: the first is the number and the degree respective degree of evolution of their related hosts of regression of the claws on legs II-IV, the second (Fain, 1974, 1977). The progressive regression of the is the number and the shape of setae on the legs and parasite appears to be directly related to the effi­ the body. These characters, however, are less stable, ciency of the immunological system and accordingly but more sensitive, than the shape of leg I. They can to the degree

2

.... trochcmter 5

4

_ tarsus

- ti bia

Figs 1-8: Leg I of the female ventral view, in some genera of the family Myobiidae: 1. Xenomyobia; 2. Archemyobia; 3. Aus/ralomyobia; 4. Necu)galobia; 5. ElephanlUlobia; 6. BinujJcus; 7. Pteracarus; 8. Radfol'dia. Host-parasite coevolution in mites 1279 specialized for Acrobates pygmaeus (Burramyidae). parasitizes 5 species of Microgale, the other lives on In these genera, leg I possesses a normal clasping Limnogale. The Macroscelididae are parasitized by a organ as in the Myobinae and. legs III an IV are thin single genus, Elephantulobia, with three species, each and not adapted for clasping the hairs of the host of them living on a different species of Elephantulus. (Fain & Lukoschus, 1979b). We can summarize these observations as follows: These observations may be summarized as The two most primitive genera of Myobiidae from follows: the American marsupials of the families insectivores are Nectogalobia with one species living Didelphidae and Caenolestidae are parasitized on Nectogale sinensis (Blarinini) and Protomyobia each by a different subfamily of Myobiidae, with eight species living on Soricini and Blarinini. Archemyobiinae and Xenomyobiinae, respectively. All these primitive species are confined to the The genus Dromiciops (Didelphidae: Micro­ Holarctic Region, as are their hosts. A third genus biotheriinae) is parasitized by a distinct genus in the Eadiea, more evolved, is encountered on Talpidae, as Archemyobiinae. The Myobiidae from Australia, holarctic. All the other genera are more evolved than Australomyobia and Acrobalobia, living on Eadiea. The 6 genera from Madagascar or Central Dasyuridae and Burramyidae, respectively, are more Africa parasitizing the Tenrecidae and the evolved than those from South American Didel­ Macroscelididae form a rather homogenous group phidae suggesting that a derivation Didelphidae­ distinctly more evolved than the other genera. Dasyuridae is possible. According to Hoffstetter (in Paradoxically, Blarinobia with 2 species restricted to Fain, 1982) the concordance between the radiations the North American Blarinini, is the most evolved of of the Myobiidae and that of their hosts is remark­ the group. able. In bats In insectivores Since my paper on coevolution in Myobiidae The 16 genera and 67 species of Myobiidae (Fain, 1982) the number of described species from described from the insectivores all belong to the bats has increased form 179 to 230, and that of subfamily Myobiinae. Specificity is very strict, each subspecies to 29; they are included in 21 genera and genus is endemic for a subfamily of insectivores, 7 subgenera. except for Eadiea represented by 6 species, all para­ The Megachiroptera are represented by a single sitic on Talpidae but from 4 different subfamilies: family Pteropodidae divided into 4 subfamilies 2 species from Scalopinae, two from Desmaninae, (Pteropodina, Nyctimeninae, Harpyionycterinae and one from Talpinae and one from Condylurinae Macroglossinae) and 44 genera. These hosts (Fain & Luckoschus, 1976a). Myobiidae have not harbour 3 (? 2) genera and 1 subgenus of Myobiinae, been found from Chrysochloridae, Erinaceidae, i.e. Binuncus, with one subgenus Probinuncus, includ­ Solenodontidae and Tupaiidae. The Tupaiidae were ing 19 species, all restricted to Pteropodinae, except included in the insectivores before Corbert & Hill one living on Macroglossinae. The second genus (1980) created the new order Scandentia for them. Pteropimyobia includes 5 species of which 3 live on The Soricidae are parasitized by 8 genera and Macroglossinae and 2 on Nyctimeninae. The third 36 species of Myobiidae. The Talpidae harbour 2 genus, Ugandobia is represented by 9 species from genera and 9 species: Eadiea whose 6 species are Emballonuridae, 1 (U. euthrix) from Hipposideridae represented in the four subfamilies of Talpidae and 1 (u. balionycteris) from Pteropodinae. I think (see above), and Eutalpacarus with 3 species, each that thi~ genus is restricted to the Emballonuridae of them being restricted to a different genus of and that the occurrence of 2 species on other hosts Scalopinae. The Tenrecidae include 5 genera and resulted from contamination in museum jars. Con­ 15 species. The 2 different species of the genus cerning U. balionycteris, this species has been Afromyobia infect the genera Potamogale, and recorded again, but as a new subspecies, from 3 Micropotamogale, respectively. The 4 other genera, species of Emballonul'a, which is probably the true with 13 species, are restricted to the Oryzoryctinae of host genus of this taxon (Fain, 1976a; Uchikawa, Madagascar, each of them being specialized for I O'Connor & Klompen, 1991). The 19 species of host genus. Microgalobia harbour nine species of Binuncus are all restricted to Pteropodinae, except which 6 are living on the host-genus Microgale, two for 1 species found on a Macroglossinae. Specificity on Nesogale and one on Geogale. The three other is also very strict at the genus level of the host, each genera are .. monotypic: Limnogalobia infects species being specialized for a single host genus, Limnogale and Oryzorictobia parasites Oryzoryctes. except for 1 species which was found on 2 closely The third genus Madamyobia contains 2 species, 1 related hosts (Fain, 1982). It is important to note 1280 A. FAIN that Binuncus and Ptel'opimyobia living on Mega­ totalling 26 species, i.e. Hipposidel'obia whose 12 chiroptera are more evolved than Acanthophthil'ius species live on 5 genera of Hipposideridae, each of and Ptel'acarus from Microchiroptera. The subgenus them being restricted to 1 host genus, Metabinuncus, Probinuncus is slightly more primitive and forms a with 12 species parasitizing exclusively the genus link between the 2 groups. Hipposideros and Binunculoides and Triaenomyobia, From these observations it appears that the each with 1 species parasitizing Hipposidel'os and Myobiidae living on bats do not originate in Trianeops, respectively. Two genera and 3 subgenera Megachiroptera but in some primitive genera of live on Molossidae: Schizomyobia with I species Microchiroptera, especially Vespertilionidae, and parasitizing Tadarida in the Old World and from these have passed to Megachiroptera. Another Ewingana with 2 subgenera Doreyana and Mor~ argument that confirms this opinion is the fact that momyobia, totalling 17 species; among them 13 Megachiroptera harbour only a very small number species were found on Tadarida, 2 on Cheiromeles of genera and species (2 genera and 24 species) and 2 on Molossus. In addition 2 species of compared to Microchiroptera (20 genera and 206 Ewingana have been described from other hosts, 1 species of Myobiidae). The situation is peculiar to from a Nycteridae (probably a museum contamina­ the Myobiidae for in other groups in mites such as tion) and another from the genus Amol'phochilus the Mesostigmata and the Sarcoptidae the species (Furipteridae), a family close to the Molossidae. living on Megachiroptera are more primitive than Among the species of ~wingana, 11 originated from those from Microchiroptera (Fain, 1982). One the Old World and 8 from the New World. The New might surmise that the Myobiidae originated on World families Phyllostomatidae, Desmodontidae some primitive Vespertilionidae and that from there and Mormoopidae harbour on the whole 32 species had transferred to tt~e Megachiroptera. of Myobiidae belonging to 3 genera: Eudusbabekia, Microchiroptera are parasitized by 207 species with a subgenus Eudusbabekia (Synoecomyobia), and 29 subspecies of Myobiidae. They belong to 19 Phyllostomyobia and loanella. All of these species, genera and 6 subgenera. They have been found on 9 except 3, are restricted each to 1 host-genus. The families of bats, and are speciall¥ abundant in the Pyllostomatidae have been divided into 6 subfami­ Vespertillionidae. Their specificity is generally very lies. The presence of the genus Dusbabekia in all strict, the rare exceptions to this rule result probably these families and subfamilies suggest that these from contamination in museum jars. Each genus of higher taxa are closely related to one another. myobiid is generally resticted to a family and often According to Uchikawa (1987) the 2 families to a subfamily of hosts and many species are special­ Mormoopidae and Phyllostomatidae merely repre­ ized for one host genus. Microchiropteran families sented a single family. The genus Phyllostomyobia are not equally infected by myobiids. The Old World (= ? loanella), with 4 species known from Emballonuridae harbour the genus Ugandobia with 9 Pyllostomatidae and Glossophaginae, is more primi­ species living on Taphozous, Emballonul'a, Coleura tive than Eudusbabekia (legs II-IV with 2 claws, and Saccolaimus. The genus Ugandobia also contains instead of 1 claw in the latter). The family 2 species described from Hipposideridae and Vespertilionidae harbours 76 species of Myobiidae, Pteropodidae, respectively, but I surmise that they belonging to 3 genera, i.e. Acan thophthirius, with were due to contamination (see above). The New 4 subgenera (Acanthophtirius, Myotimyobia, Chil'o­ World Emballonuridae are parasitized by the genus , Mimetillobia) , Pteracarus and Calcm'· Expletobia with 2 species living on Saccoptel'Yx and myobia. Acanthophthirius and Pteracal'us are the Rhynchiscus, respectively. The Rhinolophidae are most primitive genera found on bats. Most of the represented by the single genus Rhinolophus, which species (47 for Acanthophthirius and 21 for harbours 2 endemic genera of myobiids, the first is Pteracal'us) live on Vespertilioninae (Fain, 1982). Neomyobia, with 13 species and 3 subspecies, the The genus Calcal'myobia includes 18 species and 8 second Rhinomyobia, with one species. Radford subspecies, all confined to the genus Minioptel't1s (1952) described a new species, Calcarmyobia (Miniopterinae), except one species (c. rhinolophia) rh inolophi, from a Rhinolophus but, according to which had been described from a Rhinolophus but Uchikawa (1985), the true host of this species this host was very probably a contamination (see was probably Miniopterus natalensis arenal'ius above). Finally I mention briefly 4 small families of (Verspertilionidae, Miniopterinae). One might Chiroptera, all represented by only their type genus, consider therefore that Neomyobia and Rhinomyobia except one (Furipteridae) which includes 2 genera. are restricted to the genus Rhinolophus. The The genus Nycteris (Nycteridae) harbours I species Hipposideridae harbour 4 gene(a of myobiids of the monotypic genus Nycterimyobia, parasitizing Host-parasite coevolution in mites 1281

several species of Nyctel'is. The genus Mystacina, in able (Fain, 1976a,b; Fain & Lukoschus, 1977c, the Mystacinidae (= Mystacops, Mystacopidae) is 1979c). parasitized by the monotypic and endemic genus Mystacobia. The genus Amolphochilus (Furipteridae) Acknowledgement-I thank M.R.D. Kime who reviewed harbours I species of the genus ElVingana, special­ the English manuscript. ized for MoJossidae, which suggests close relation­ ships between the 2 families of bats (Fain, 1982). The REFERENCES genus Thyroptera (Thyropteridae) is parasitized by 1 Baker E. W. 1951. Pneumocoptes, a new genus of lung­ species of Pteracarus, specialized for Vesper­ inhabiting mite rodents (Acarina, Epidennoptidae). Journal ofParasitology 37: 583-586. tilionidae, and 1 species of Thyromyobia a genus Camin J. H., Moss W. W., OliveI' J. H. & Singer G. 1967. close to Acanthophthirius. Cloacaridae a new family of cheyletid mites from the c10aca of aquatic turtles (Acari: Acariformes: In rodents Eleutherengona). Journal of Medical Entomology 4: Rodents are parasitized by 96 species and 7 261-272. subspecies of myobiids, included in 7 genera. Among Colwell R. K. 1973. Competition and Coexistence in a these genera, 5 are restricted each to I family of simple tropical community. American Naturalist 107: rodents and 1 (Radjordia) has been divided into 11 737-760. subgenera (Fain & Lukoschus, 1977). More recently, Corbet G. B. & Hill J. E. 1980. A World List ofMammalian 3 of these subgenera have been raised to the genus Species. Trustees of the British Museum (Natural History). London. rank, Le. Cryptomyobia living on Bathyergidae, Dubinina H. 1964. Mites of the genus Histiophol'lls Lavoimyobia, parasitizing Heteromyidae and Austro­ (Listrophoridae) parasites of the' beavers. Zoological myobia, from Gerbillinae and Dendromurinae Instilute of Academy of Sciences, USSR. Leningrad. (Muridae) and Dipodidae. The 8 remaining subgen­ Paper No. 22: 111-152 (in Russian). era live on Gliridae, Zapodidae and Muridae Dusbabek F. 1969a. To the phylogeny and zoogeography (M urinae, Cricetinae and Microtinae) (Fain, 1982). of bats (Chiroptera) based on the study of their parasitic The 2 most primitive genera are ProradJoria,' with 2 mites (Acarina). Lynx 10: 19-24. species living on Echimyidae (Neotropical Hystricho­ Dusbabek F. 1969b. To the phylogeny of genera of the morphes), and Idiurobia, more evolved and parasitic family Myobiidae (Acarina). Acarologia 11: 537-574. Eichler W. 1942. Die Entfaltungsregel und andere Gesetz­ on Idiurus (Anomaluridae). The genus Cryptomyobia, massigkeiten in den parasitogenetischen Beziehungen del' living on Cryptomys (Bathyergidae), is monotypic Mallophagen und anderer sUindiger Parasiten zu ihren and more evolved than Idiurobia. The genus Wirten. Zoologischer Anzeiger 137: 77-83. Austromyobia includes 10 species, of which Evans G. 0., Sheals J. G. & Macfarlane D. 1961. The 6 live on Gerbillinae (Muridae), 2 on Dipodidae and Terrestrial Acari of the British Isles. Vol. 1. Introduction 2 on the genus Dendromus (Muridae, Dendro­ and Biology. Trustees of the British Museum, Natural murinae). The presence of Austromyobia on History, London. Gerbillinae and Dendromurinae suggests the exis­ Fain A. 1957. Les acariens des families Epidermoptidae et tence of close affinities between these 2 subfamilies. Rhinonysssidae parasites des fosses nasales d'oiseaux au The 10 species of Autromyobia form a rather Ruanda-Urundi et au Congo beIge. Annales du Musee homogenous group intermediate in evolution royal du Congo beIge, Tervuren, 8. Sciences Zoologiques 60: 1-156. Cryptomyobia RadJordia between and s.str. The Fain A., Mignolet G. & Bel'esnay Y. 1958. L'acariase des subgenus Radjordia (Graphiurobia) is represented in voies respiratoires chez les singes du Zoo d'Anvers. Gliridae by 4 species and in the Zapodidae by 2 Bulletin de la Societe royal de Zoologie d'Anvers 9: species, which suggests the existence of affinities 15-19. between these families. The hypothesis is confirmed Fain A. 1960. Revision du genre Cytodiles (Megnin) et by the discovery in both families of an astigmatic description de deux especes et un genre nouveaux dans la genus of mite, Gliricoptes (Myocoptidae) which is famille Cytoditidae Oudemans. Acarologia 2: 238-249. represented by 7 species in Gliridae and by 2 species Fain A. 1961. Les acariens parasites endopulmonaires des in the Zapodidae (Fain, 1974, 1975). The most serpents (Entonyssidae: Mesostigmata). Bulletin de evolved genera of the family Myobiidae are l'Institut royal des sciences nalurelles de Belgique 37: 1-135. Radjordia (RadJordia) and Myobia. They live on Fain A. 1962. Les acariens parasites nasicoles des Muridae (Murinae). Batraciens. Revision des Lawrencarinae Fain, 1959 One may conclude from these observations that (Ereynetidae: ). Bulletin de I'Institlit the concordance between the radiations of the royal des sciences naturelles de Belgique 38: 1-69. Myobiidae and that of their rodent hosts is remark- Fain A. & Hyland K. E. 1962. The mites parasitic in the 1282 A. FAIN

lung of birds. The variability of Slernosloma trachea­ Fain A. 1977. Observation sur la specificite des acariens de colum Lawrence, 1948 in domestic and wild birds. la famille Myobiidae. AI/nales de Parasitologie humaine Parasitology 52: 401-424. et comparee 52: 339-351. Fain A. 1964<1. Chaetotaxie et classification des . Fain A. & Lukoschus F. S. 1977. Nouvelles observations Gastronyssidae avec description d'un nouveau genre sur les Myobiidae parasites de rongeurs (Acarina: parasite nasicole d'un ecureuil sudafricain (Acarina: Prostigmata). Acta Zoologica et Pathologica Sarcoptiformes). Revue de zoologie et de botanique Antverpiensia 69: 11-98. . africaines 70: 40-54. Fain A. 1978a. Epidemiological problems of scabies. Fain A. 1964b. Les Lemumyssidae parasites nasicoles des Imernalional Journal ofDermatology 17: 20-30. Lorisidae et des Cebidae sudamericains. Description Fain A. 1978b. Mites of the family Myobiidae (Acarina: d'une espece nouvelle (Acarina: Sarcoptiformes). Annales Prostigmata) from mammals in the collection of the de la Societe royale beIge de Medecine tropicale 44: British Museum (Natural History). Bulletin of British 453-458. Museum (Natural History), Zoology series 33: 193-229. Fain A. 1965a. A review of the family Rhyncoptidae Fain A. 1979. Specificity, adaptation and parallel evolution Lawrence parasItic on porcupines and monkeys host-parasite in acarines especiaJIy Myobiidae, with a (Acarina: Sarcoptiformes). Advances in Acarology 2: tentative explanation for the regressive evolution caused 135-158. by the immunological reactions of the hosts. Recellt Fain A. 1965b. Quelques aspects de I'endoparasitisme par Advances in Acarology 2: 321-327. les acariens. Annales de Parasitologie humaine et Fain A. & Lukoschus F. S. 1979a. Parasites of Western comparee 40: 317-327. Australia VI. Myobiidae parasitic on Bats (Acarina: Fain A. 1967. Observations sur les Rodhainyssinae, Prostigmata). Records ofthe Western Australian Museum acariens parasites des voies respiratoires des chauves­ 7: 61-107. souris (Gastronyssidae: Sarcoptiformes). Acta Zoologica Fain A. & Lukoschus F. S. 1979b. Parasites of Western et Pathologica Antverpiensia 47: 3-35. Australia. VllI. Myobiidae parasitic on Marsupials Fain A. 1968a. Etude de la variabilite de Sarcoptes scabiei (Acarina: Prostigmata). Records of the Western avec une revision des Sarcoptidae. Acta Zoologica et Australian Museum 7: 287-299. Pathologica Antverpiensia 47: 1-96. Fain A. & Lukoschus F. S. 1979c. Parasites of Western Fain A. 1968b. Notes sur les acariens de la famille Australia. IX. Myobiidae parasitic on Rodents (Acarina: Cloacaridae Camio et al. parasites du cloaque et des Prostigmata). Records ofthe Western Australian Museum tissus profonds des tortues (: Trom­ 7: 301-316. bidifonnes). Bulletin de l'Insti/ut royal des Sciences Fain A. 1982. Specificite et evolution parallele hotes-para­ natl/relles de Belgique 44: 1-33. sites chez les Myobiidae (Acari). Memoires du Museum Fain A. 1969. Adaption to parasitism in Mites. Acarologia National d'Histoire naturelle. Nouvelle Serie A. Zoologie 11: 429-449. 123: 77-85. Fain A. & Johnston D.E. 1970. Un nouvel acarien de la Fain A., Lukoschus F. S. & Rosmalen P. G. 1982. famille Audycoptidae chez I'ours noir Ursus americanus. Observations on the genus Epimyodex Fain & Orts, 1969 Acta zoologica et Pathologica Antverpiensia 50: 179-181. with description of two new species. Transfer of this Fain A. 1974. Observations sur les Myobiidae parasites des genus to the Cloacaridae (Acari: Prostigmata). Bulletin rongeurs. Evolution paralleIe hotes-parasites (Acariens: de I'Institut royal des sciences naturelles de Belgique. Trombidiformes). Acarologia 16: 441-475. Entomologie 54: 1-10. Fain A. & Domrow R. 1974. The subgenus Cystostethl/In Fain A. & Hyland K. E. 1985. Evolution of astigmatic Domrow (Acari: Atopomelidae). Multiple speciation on mites and mammals. In: Coel'olution of Parasitic the marsupial Potorous tridactylus (Kerr). Australian Arthropods and Mammals (Edited by Ke Chung Kim), Journal ofZoology 22: 549-572. pp. 641-660. Wiley-Interscience, New York. Fain A. 1975. Anciennete et specificite des acariens para­ Fain A. & Lambrechts L. 1985. A new Anoetid mite para­ sites. Evolution parallele hOtes-parasites. Acarologia 17: sitic in the swimming bladder of the aquarium fish 369-374. Pangasius sutchi. Bulletin & Annales de la Societe royale Fain A. 1976a. Notes sur les Myobiidae parasites de beIge d'El/lomologie 121: 119-126. rongeurs, d'insectivores et de chiropteres (Acarina: Pros­ Fain A. & Lukoschus F. S. 1985. The genus Schizocarpus tigmata). Acta Zoologica et Pathologica AllIverpiensia 64: Trouessart, 1896 (Acari: Chirodiscidae) from the Beaver 3-32. Castor fiber L.: an example of multiple speciation. Fain A. 1976b. Les acarieos parasites des chauves-souris. Entomologische Abhandlungen Staatliches Museum far Biologie, role pathogene, specificite, evolution parallele Tierkun de. Dresden 49: 35-68. parasites-hotes. Annales de Speleologie 31: 3-25. Fain A. 1988. Evolution et adaptations chez les acariens Fain A. & Lukoschus F. S. 1976a. Myobiidae parasites parasites. Annales de la Societe royale Zoologique de d'Insectivores. Acta Zoologica et Pathologica Belqique 118: 13-27. Antverpiensia 66: 121-188. Fain A. & Whitaker J. O. Jr. 1988. Mites of the genus Fain A. & Lukoschus F. S. 1976b. A new genus and species SchizocarjJus Trouessart, 1896 (Acari: Chirodiscidae) of Myobiidae from the marsupial LeSlOros inca (Acarina: from Alaska and Indiana, U.S.A. Acarologia 29: Prostigmata). Acarologia 18: 489-195. 339-409. Host-parasite coevolution in mites 1283

Fain A. 1992. Notes on the flower-mites of the genus coevo1utionary phylogenies. In: Coevolution of Parasitic Rhinoseius Baker & Yunker, 1964 (Acari: Ascidae) Arthropods and Mammals (Edited by Ke Chung Kim), phoretic in the nares of hummingbirds with a key to the pp, 569-640. Wiley-Interscience, New York. known species. Bulletin de 1'lnstUut royal des sciences Radfol'd C. D. 1952. Revision of the fur miles Myobiidae naturelles de Belgique. Entomologie 62: 117-136. (Acarina). Bulletin du Museum d'Histoire naturel/e. 2bne Fahrenholz H. 1909. Aus dem Myobiiden-Nachlass des serie 24: 371-381. Herrn Poppe. Abhandlungen des Naturwissenchaftlichen Radovsky F. J. 1985. Evolution of mammalian mesostig­ Vereins zu Bremen 19: 359-370. mate mites. In: Coevolution of Parasitic Arthropods and Fahrenholz H. 1913. Ectoparasiten und Abstam­ Mammals (Edited by Ke Chung Kim), pp. 441-504. mungsIehre. Zoologischer Anzeiger 41: 371-374. Wiley-Interscience, New York. Furman D. P. 1979. Specificity, adaption and parallel­ Strandtmann R, W. 1958. Host specificity of bird nasal evolution in the endoparasitic Mesostigmata of mites (Rhinonyssidae) is a function of the gregariousness mammals. Recent Advances in Acarolory 2: 329-337. of the host. Proceedings of the 10th International Gaud J. & Atyeo W. T. 1982. Specificite parasitaire chez Congress ofEntomology, Montreal 1: 901-911. les Acariens Sarcoptiformes plumicoles. Memoires du Szidat L. 1940. Beitri:ige zum Aufbau eines nattirlichen Museum National d'Histoire naturelle, Nouvelle Serie A. Systems del' Trematoden. I. Die Entwicklung von Zoologie 123: 247-254. Echinocercaria choanophila U. Szida t zu Cathaemania Hoffstetter R. 1982a. Introduction sur les hotes. I. hians und die Abteilung del' Fasciolidae von den Phylogenie des mammiferes. Methodes d'etude, resultats, Echinostomidae. Zeitschrift fill' Parasitenkunde 11: problemes. Mbnoires du Museum National d'Histoire 239-283. nalurelles, Nouvelle Serie A. Zoologie 123: 13-20. Uchikawa K. & Harada M. 1981. Evaluation of bat-infest­ Hoffstetter R. 1982b. Discussions In: Fain A. 1982. ing Myobiidae (Acarina: Trombidiformes) as indicators Specificite et evolution parallele hotes-parasites chez 1es in and phylogeny of host bats (Chiroptera). Myobiidae (Acari). Memoires du Museum National Zoological Magazine 90: 351-361. d'Hisloire naturelle. Nouvelle Serie A. Zoologie 123: 85. Jameson E. W. 1955. A summary of the genera of Uchikawa K. 1985. Mites of the genus Calcarmyobia (Acarina: Myobiidae) with information on the taxonomy Myobiidae (Acarina). Journal of Parasitology 41: 407-416. of their host bats of the genus Miniopterus (Chiroptera, Kim K. C. 1985. Coevolution of Parasitic Arthrop"ods and Miniopteridae). Bulletin of the British Museum (Natural Mammals (Edited by K. C. Kim). John Wiley, New History). Zoology 48: 15-25. York. Uchikawa K. 1986. Mites of the genus Pteropimyobia Fain KJassen G. J. 1992. Coevolution: a history of the macro­ (Trombidiformes, Myobiidae) and information on host evolutionary approach to studying host-parasite associ­ taxonomy deduced from them. Journal of Parasitology ation. Parasitology 78: 573-587. 72: 249-256. Lavoipierre M. M. J. 1964. A new family of Acarines Uchikawa K. 1987. Myobiid mites (Trombidiformes: belonging to the suborder Sarcoptiformes parasitic in the Myobiidae) associated with the Vampire bats hair folicles of primates. Annals ofthe Natal Museum 16: (Chiroptera: Phyllostomatidae) and information on host 191-208. taxonomy deducted from them. Journal of Parasitiology Lawrence R. F. 1956. Studies on South African fur mites 73: 640-645. (Trombidiformes and Sarcoptiformes). Annals of the Uchikawa K., OConnor B. M. & Klompen H. 1991. New Natal Museum 13: 337-375. Myobiidae (Acarina: Trombidiformes) from Philippine Nutting W. B. 1985. Prostigmata-mammalia. Validation of Mammals. Zoological Science 8: 157-168.