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Laboulbeniales: Phylogenetic Studies


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EVOLUTION OF LABOULBENIALES (from an hyphal ascomycete with indeterminate growth to a determinate ascomycete thallus derived from an ascospore)
Laboulbeniales have had a controversial taxonomic history and have played a central role in phylogenetic arguments on the origin of higher fungi. Some mycologists believed them to be derived from floridean red algae. In addition one genus of these fungi was considered to be an insect-parasitic worm when it was first discovered. Members of four families (Herpomycetaceae, Laboulbeniaceae, Ceratomycetaceae, Euceratomycetaceae) are obligate biotrophs of insects, mites, and millipedes. A fifth family that has been included in the order by some workers, Pyxidiophoraceae, is morphologically distinct because the species produce mycelium and are mycoparasites in the filamentous stage with an arthropod-associated phoretic stage that may be biotrophic. The link between Laboulbeniales and Pyxidiophoraceae first was suggested on the basis of comparative life histories and common morphology of asci development and ascospores (Blackwell and Malloch 1989). More recently phylogenetic analysis of molecular characters has supported the relationship (Bllackwell 1994), but, although the clade is excluded from the main group of perithical ascomycetes, its position among loculoascomycetes and discomycetes is not well resolved.

Alternative hypotheses of relationships of the group include a proposal by Cavalier-Smith (1998) that the Laboulbeniales are not ascomycetes, but rather relatives of other invertebrate-associated fungi, including Trichomycetes, Entomophthorales and Zoopagales in his SubKingdom Eomycota, Phylum Archemycota, Class Zoomycetes. This hypothesis has been refuted on the basis of phylogenetic analysis of partial sequences of ssu rDNA including parsimony analysis and maximum likelihood ratio tests applied to trees constructed using different topological constraints (Weir and Blackwell, submitted).

Although their placement within the filamentous ascomycete clade is well-supported a robust phylogeny of Laboulbeniales taxa must await further molecular work and integration of this with a morphologically-based cladistic analysis. The ancestral form in the Laboulbeniales and subsequent evolutionary trends within the order are still matters of some debate. Thaxter (1908) "...found himself unable to arrive at any satisfactory conclusions," and the more recent treatise by Tavares (1985) also concludes with uncertainty regarding these important questions. Once again preliminary molecular data provide possible clues to a number of the questions that have been raised. In particular, members of the Ceratomycetaceae including representatives from the genera Rhynchophoromyces,Autoicomyces, and Ceratomyces appear basal in phylogenetic reconstructions. These taxa share unspecialized exogenous spermatia and are found exclusively on aquatic hosts. Coreomyces, (an unusual genus found only on aquatic water-boatmen [Heteroptera, Corixidae] and characterized by unique perithecial development and production of antheridial cells on the primary axis below the perithecium) appears to represent an intermediate stage between these basal taxa and the more advanced members of Laboulbeniaceae. The latter are typified by the presence of more specialized endogenous antheridia and occurrence largely on terrestrial insects.  No firm conclusions can yet be drawn from these datasets however, since many critical genera remain to be sequenced. Nevertheless, the answers to many intriguing questions regarding the evolution of these enigmatic fungi finally appear to be within grasp. It should now be possible to formulate and test higher-level phylogenetic hypotheses regarding Laboulbeniales; to investigate morphological plasticity and relate this to host, position, and sex-of-host specificities; to test morphology-based species concepts within the order- linking these to observed patterns of geographical distribution; and to examine the patterns of coevolution occurring between Laboulbeniales and their arthropod hosts.

SPECIFICITY
As a direct consequence of their obligate relationship with their hosts Laboulbeniales fungi exhibit an often high degree of host specificity. This was recognized early in the study of these organisms and in varying
degrees is characteristic of most obligate parasites. Examination of published host-parasite lists (Frank, 1982; Hulden, 1983; Weir, 1996) mainly from temperate regions clearly shows that levels of host specificity displayed by Laboulbeniales are generally high when compared to most other groups of parasites that exploit arthropods. A relatively small proportion of the parasite species have been reported from more than
one host but host association data are too fragmentary for any firm conclusions to be reached. In the most intensively studied mycobiota for these fungi, that of Poland (Majewski, 1994), the host range for any given parasite appears, with very few exceptions, to be restricted taxonomically, and generally encompasses only species that belong to the same genus or group of closely related genera. At odds with these findings is the realisation that some species of Laboulbeniales, for example Laboulbenia vulgaris, have apparently broad geographical distributions, encompassing both tropical and cool temperate areas (Hammond, 1995), something almost unknown in species of the arthropod groups which include most of their hosts. The occurrence in nature of morphologically similar but genetically and physiologically distinct species of Laboulbeniales cannot, at this point, be discounted.

An even more intriguing aspect of Laboulbeniales biology are the numerous reports of so-called 'position specificity'- the often precise occurrence of thalli on very restricted areas of the body of the host. This phenomenon was first observed by Peyritsch (1875) who noted that Stigmatomyces baeri usually grew on the upper surface of the female fly and on the lower surface of the male. Position phenomena of this type are quite frequently encountered and are readily explained by assuming that ascospore transmission from one host individual to another is optimized during copulation. Transmission during mating does not, however, provide an hypothesis to explain many other examples of position specificity found in the Laboulbeniales as, in many instances, both sexes of host are equally heavily infested, and in the same position on the integument. In the most extreme example, found in the genus Chitonomyces on the African whirligig beetle Orectogyrusspecularis (Gyrinidae), 16 parasite species have been described (Thaxter, 1926). Whether these are valid species or represent different physiological growth-forms of the same species remains yet to be determined.

A third type of specificity phenomenon called 'sex-of-host specificity' was described by Benjamin and Shanor (1952) in their work on the parasites of Bembidion picipes. Here 6 parasite species were distinguished on a
single host, 2 of these were found only on male beetles, a third species was apparently restricted to females. The restricted nature of this specificity phenomenon has more recently been questioned (Scheloske, 1976).

Laboratory-based experiments on the host specificity of a single species of Laboulbenia (DeKesel, 1996) indicated that this fungus was potentially plurivorous on a range of Carabidae but was restricted to a
single host in nature as a result of reinforced ecological isolation. Further detailed experimental and genetical studies are undoubtedly required in order to clarify some of the issues regarding species-concepts
and specificity raised here.

REFERENCES

[from Weir, A. The Laboulbeniales: an enigmatic group of arthropod-associated fungi. In: Sechbach, J. Enigmatic Microorganisms and Life in Extreme Environments. Kluwer Academic Publishers, Dordrecht, The Netherlands.]

ssu rDNA extractions(* = partial sequence obtained)
Acallomyces sp. 
Autoicomyces falcatus
Autoicomyces reflexus*
Botryandromyces ornatus*
Cantharomyces sp.
Ceratomyces mirabilis*
Ceratomyces sp. indet.*
Chitonomyces melanurus
Cochliomyces trinitatis*
Coreomyces spp. (4 species) * (one partial sequence)
Corethromyces bicolor*
Corethromyces sp. nov. *
Cucujomyces bilobatus
Diaphoromyces kuschelii
Dimeromyces anisolabis
Dimorphomyces sp.
Dioicomyces sp.*
Distolomyces forficulae
Gloeandromyces sp.
Herpomyces sp.
Hesperomyces coccinelloides*
Hesperomyces virescens*
Hydraeomyces halipli
Hydrophilomyces sp.*
Ilytheomyces sp
Kyphomyces sp.
Laboulbenia cristata*
Laboulbenia flagellata
Laboulbenia notiophili
Laboulbenia pedicellata
Laboulbenia philonthi*
Laboulbenia vulgaris
Monoicomyces invisibilis
Monoicomyces sp.
Rhachomyces philonthinus*
Rhachomyces canariensis
Rhadinomyces pallidus*
Rhynchophoromyces minor*
Rickia passalina*
Sphaleromyces lathrobii*
Stigmatomyces* (11 species sequenced)
Stigmatomyces borealis*
Stigmatomyces crassicollis
Stigmatomyces discocerinae*
Stigmatomyces entomophilus
Stigmatomyces ephydrae*
Stigmatomyces hydrelliae*
Stigmatomyces limnophorae*
Stigmatomyces limosinae*
Stigmatomyces ochtherae
Stigmatomyces papuanus
Stigmatomyces paralimnae*
Stigmatomyces parydrae
Stigmatomyces protrudens*
Stigmatomyces purpureus*
Stigmatomyces rugosus*
Stigmatomyces scaptomyzae*
Teratomyces mirabilis
Tettigomyces sp.
Zeugandromyces sp.
Zodiomyces vorticellarius*

Contact Meredith Blackwell or Alex Weir for information on availability of research materials.
Laboulbeniales Home Page / Phylogenetic Studies of Laboulbeniales / Methods / Literature / Mycology at LSU

Last Modified: 24 June 2005
Meredith Blackwell
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