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Laboulbenia Slackensis and L. Littoralis Sp Mycologia, 106(3), 2014, pp. 407–414. DOI: 10.3852/13-348 # 2014 by The Mycological Society of America, Lawrence, KS 66044-8897 Laboulbenia slackensis and L. littoralis sp. nov. (Ascomycota, Laboulbeniales), two sibling species as a result of ecological speciation Andre´ De Kesel1 the phylogenetic relatedness of taxa within a host National Botanic Garden of Belgium, Domein van range, specificity has been attributed generally to the Bouchout, BE-1860 Meise, Belgium need for certain substances from the host (Scheloske Danny Haelewaters 1969, Tavares 1979). Studies directed at understand- Department of Organismic and Evolutionary Biology, ing the mechanisms governing host specificity and Harvard University, 22 Divinity Avenue, Cambridge, explaining observed host ranges have been limited in Massachusetts 02138 part because these fungi can be manipulated only by growing infected insect colonies and artificially introducing a foreign host. An alternative way to Abstract: Laboulbenia littoralis is described from the investigate host specificity is to examine unrelated halobiont Cafius xantholoma (Coleoptera, Staphylini- insects living in the same habitat. Laboulbeniales dae); it previously was misidentified and not properly infecting co-habiting and stenotopic hosts, which are documented. Morphologically the new species be- characterized by having a very strict habitat choice, longs to a group of carabidicolous taxa similar to are interesting in terms of host specificity and Laboulbenia pedicellata and especially Laboulbenia ecological speciation. The latter, according to the slackensis. It is generally accepted that the specificity modern evolutionary synthesis, is the result of of Laboulbeniales is based on their need for the micro-evolutionary process of divergent natural substances from the host. In this relatively strict selection between populations exploiting different context, shifts between unrelated hosts are difficult to resources or environments, ultimately leading to explain. We present morphological and ecological reproductive isolation (e.g. Mayr 1942, Dobzhansky evidence supporting the hypothesis that these fungi 1951, Schluter 2000). are capable of shifting between unrelated hosts as Host and parasite phylogenies often align as a long as they share the same habitat. Adaptation to a result of codivergence (shared history) (Legendre particular environment, combined with a reduced et al. 2002, Downie and Gullan 2005, Futuyma 2005, dependence from specific nutrients of the host, Page 1994) but explaining how morphologically explains the proposed interfamilial host shift. similar Laboulbeniales can occur on phylogenetically Key words: Cafius, ecological specificity, host unrelated hosts is challenging. Field data indicate that shift, parasitic fungi, plurivory, reproductive isolation, plurivorous Laboulbeniales, such as Laboulbenia taxonomy ecitonis G. Blum, can be found only on unrelated hosts occupying the same ecological niche, including INTRODUCTION Staphylinidae, Histeridae, mites (Acari, Mesostigmata, Uropodidae) and ants (Hymenoptera, Formicidae) Laboulbeniales are obligate ectoparasites associated (Benjamin 1971). Plurivory is still unexplained and with arthropods. The order consists of 140 genera many factors are thought to be involved, including (Rossi and Santamarı´a 2012) and about 2050 species, accidental transmission (Scheloske 1969) and adap- 80% of them reported from Coleoptera (Weir and tation to common nutrients available from the Blackwell 2005). Among these, the Carabidae cohabiting hosts (Scheloske 1969, Benjamin 1971). (ground beetles) and Staphylinidae (rove beetles) Rossi (2011) and Arndt et al. (2003) suggest that host are the most common hosts, accounting for 17 and 47 shifts of Laboulbenia species have occurred between genera of Laboulbeniales respectively (Frank 1982, Cicindelinae and other Carabidae living in the same Tavares 1985, Rossi and Santamarı´a 2008). With more habitat, resulting in a number of morphologically than 600 species (Kirk et al. 2008, Rossi 2011) the similar taxa. Benjamin (1971) suggested in this genus Laboulbenia Mont. & C.P. Robin is the largest context that ‘‘successful colonization of a new host within the Laboulbeniales. is probably a rare event, but it is possible, even likely, Most Laboulbeniales have a high degree of host that fortuitous parasite transfer has played a role in specificity (Benjamin 1971, Tavares 1985). Based on the evolution of new species groups and even genera.’’ Mutations also are thought to allow host Submitted 18 Oct 2013; accepted for publication 18 Dec 2013. shifts, yielding cryptic species with different nutri- 1 Corresponding author. E-mail: [email protected] tional requirements (Rossi 2011). The transmission 407 408 MYCOLOGIA experiments from Ce´pe`de and Picard (1907) showed 1971), and slides were sealed with transparent fingernail that L. vulgaris Peyr. and L. pedicellata Thaxt. (as L. polish. Both insects and microscope slides are deposited at gracilipes Ce´pe`de & F. Picard) were not able to the National Herbarium of Belgium (BR). French and interchange hosts, even though the hosts belong to Italian host specimens were studied at the American Museum of Natural History (New York); respective micro- the same genus (Bembidion Latreille 1802). The major scope slides are deposited at the Farlow Herbarium, effect of rearing conditions in transmission experi- Harvard University (FH). Drawings and measurements were ments with Laboulbeniales has been shown in made with an Olympus BX51 light microscope with drawing experiments with L. slackensis Ce´pe`de & F. Picard, tube, digital camera and AnalySIS 5 imaging software (Soft which under natural conditions is a host-specific Imaging System GmbH). Host taxonomy and classification parasite, apparently restricted to the salt mash- follows Vorst (2010), unless otherwise cited. inhabiting Pogonus chalceus (Marsham, 1802) (De Biometrics.—Differences in thallus dimensions and shapes Kesel 1993, 1996). Nonetheless, data from transmis- were tested following De Kesel & Van den Neucker (2005). sion experiments show that it can infect several other We measured 15 variables and four ratios from at least 30 Carabidae; it was demonstrated that the development mature thalli of each species. These parameters were used of thalli on these hosts was influenced by the rearing (abbreviations and explanations are given between paren- conditions rather than by the host species (De Kesel theses): total thallus length (TL, from foot to perithecial 1996). apex); length of the receptacle (RL, from foot to insertion To date we know, from both field observations and cell); perithecium length (PL, without cell VI); perithecium laboratory experiments, that the habitat (imposed or width (PW); height of cell I (cell I); height of cell II (cell II); chosen by the host) seems to determine the success of height of cell III (cell III); height of cell IV (cell IV); height of the paraphysopodium (par); width of the insertion cell ectoparasites. This observation is an important (IC) and length of the appendages (app, intact whenever element in considering the ecological specificity of possible). The length of these septa was measured: septum Laboulbeniales (Scheloske 1969, Majewski 1994b, De I–II, septum II–VI; septum II–III; septum of cell III with Kesel 1996). It helps to understand the difference and cells IV and V. To better understand shapes and propor- meaning of a usual host and an occasional host, tions, these ratios also were calculated: PL/PW; cell I/cell II; including why in certain habitats a parasite can be cell IV/par and II–VI/II–III. Differences were tested with found on an atypical host. Altogether the habitat Student’s t test (Sokal and Rohlf 1981) with Statistica 10.0. preference of the host as an important driving force Host species was used as a grouping variable. The behind specialization and speciation of Laboulbe- significance value was P , 0.05. Thalli included in the niales also is recognized. With this in mind we analysis came from all parts of host integument, regardless searched for L. slackensis in its natural habitat of host species or sex. (coastal environments and saltmarshes), aiming to find it on a number of Carabidae. Instead we found RESULTS infected populations of the staphylinid beetle Cafius Statistical analysis.—Significant differences between xantholoma bearing thalli of the newly described Laboulbenia littoralis and L. slackensis were observed Laboulbenia littoralis, morphologically similar to L. for parameters, PL, PW, cell I, cell II, cell III, cell IV, slackensis. par, IC, app, I–II, II–VI, II–III, III– (IV+V); and ratios, The present paper deals with a number of PL/PW, cell I/cell II, cell IV/par, II–VI/II–III morphologically similar Laboulbenia species occur- (TABLE I). Tested differences were not significant ring on unrelated hosts from these coastal habitats. for two remaining parameters, TL and RL. Our results provide new evidence for habitat-related interfamilial host shifts in the genus Laboulbenia. TAXONOMY MATERIALS AND METHODS Laboulbenia littoralis De Kesel & Haelew., sp. nov. FIG.1 Morphology.—Insects were obtained from seaweed and plant debris from above the high water mark along east MycoBank MB801461 coast beaches in Belgium and the Netherlands. At each site Illustrations: Balazuc (1974 Fig. 18, ut L. cafii), De 40–80 L debris were carefully transferred to a bag and Kesel (1997 Pl. 20 and 1998 Pl. 1.5 ut L. cafii). transported to the laboratory. The samples were placed in
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