Three New Species of Laboulbenia from Roland Thaxter's Backlog Of
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Studies of the Laboulbeniomycetes: Diversity, Evolution, and Patterns of Speciation
Studies of the Laboulbeniomycetes: Diversity, Evolution, and Patterns of Speciation The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:40049989 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA ! STUDIES OF THE LABOULBENIOMYCETES: DIVERSITY, EVOLUTION, AND PATTERNS OF SPECIATION A dissertation presented by DANNY HAELEWATERS to THE DEPARTMENT OF ORGANISMIC AND EVOLUTIONARY BIOLOGY in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the subject of Biology HARVARD UNIVERSITY Cambridge, Massachusetts April 2018 ! ! © 2018 – Danny Haelewaters All rights reserved. ! ! Dissertation Advisor: Professor Donald H. Pfister Danny Haelewaters STUDIES OF THE LABOULBENIOMYCETES: DIVERSITY, EVOLUTION, AND PATTERNS OF SPECIATION ABSTRACT CHAPTER 1: Laboulbeniales is one of the most morphologically and ecologically distinct orders of Ascomycota. These microscopic fungi are characterized by an ectoparasitic lifestyle on arthropods, determinate growth, lack of asexual state, high species richness and intractability to culture. DNA extraction and PCR amplification have proven difficult for multiple reasons. DNA isolation techniques and commercially available kits are tested enabling efficient and rapid genetic analysis of Laboulbeniales fungi. Success rates for the different techniques on different taxa are presented and discussed in the light of difficulties with micromanipulation, preservation techniques and negative results. CHAPTER 2: The class Laboulbeniomycetes comprises biotrophic parasites associated with arthropods and fungi. -
New and Interesting <I>Laboulbeniales</I> From
ISSN (print) 0093-4666 © 2014. Mycotaxon, Ltd. ISSN (online) 2154-8889 MYCOTAXON http://dx.doi.org/10.5248/129.439 Volume 129(2), pp. 439–454 October–December 2014 New and interesting Laboulbeniales from southern and southeastern Asia D. Haelewaters1* & S. Yaakop2 1Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University 22 Divinity Avenue, Cambridge, Massachusetts 02138, U.S.A. 2Faculty of Science & Technology, School of Environmental and Natural Resource Sciences, Universiti Kebangsaan Malaysia, Bangi 43600, Malaysia * Correspondence to: [email protected] Abstract — Two new species of Laboulbenia from the Philippines are described and illustrated: Laboulbenia erotylidarum on an erotylid beetle (Coleoptera, Erotylidae) and Laboulbenia poplitea on Craspedophorus sp. (Coleoptera, Carabidae). In addition, we present ten new records of Laboulbeniales from several countries in southern and southeastern Asia on coleopteran hosts. These are Blasticomyces lispini from Borneo (Indonesia), Cantharomyces orientalis from the Philippines, Dimeromyces rugosus on Leiochrodes sp. from Sumatra (Indonesia), Laboulbenia anoplogenii on Clivina sp. from India, L. cafii on Remus corallicola from Singapore, L. satanas from the Philippines, L. timurensis on Clivina inopaca from Papua New Guinea, Monoicomyces stenusae on Silusa sp. from the Philippines, Ormomyces clivinae on Clivina sp. from India, and Peyritschiella princeps on Philonthus tardus from Lombok (Indonesia). Key words — Ascomycota, insect-associated fungi, morphology, museum collection study, Roland Thaxter, taxonomy Introduction One group of microscopic insect-associated parasitic fungi, the order Laboulbeniales (Ascomycota, Pezizomycotina, Laboulbeniomycetes), is perhaps the most intriguing and yet least studied of all entomogenous fungi. Laboulbeniales are obligate parasites on invertebrate hosts, which include insects (mainly beetles and flies), millipedes, and mites. -
Laboulbeniomycetes, Eni... Historyâ
Laboulbeniomycetes, Enigmatic Fungi With a Turbulent Taxonomic History☆ Danny Haelewaters, Purdue University, West Lafayette, IN, United States; Ghent University, Ghent, Belgium; Universidad Autónoma ̌ de Chiriquí, David, Panama; and University of South Bohemia, Ceské Budejovice,̌ Czech Republic Michał Gorczak, University of Warsaw, Warszawa, Poland Patricia Kaishian, Purdue University, West Lafayette, IN, United States and State University of New York, Syracuse, NY, United States André De Kesel, Meise Botanic Garden, Meise, Belgium Meredith Blackwell, Louisiana State University, Baton Rouge, LA, United States and University of South Carolina, Columbia, SC, United States r 2021 Elsevier Inc. All rights reserved. From Roland Thaxter to the Present: Synergy Among Mycologists, Entomologists, Parasitologists Laboulbeniales were discovered in the middle of the 19th century, rather late in mycological history (Anonymous, 1849; Rouget, 1850; Robin, 1852, 1853; Mayr, 1853). After their discovery and eventually their recognition as fungi, occasional reports increased species numbers and broadened host ranges and geographical distributions; however, it was not until the fundamental work of Thaxter (1896, 1908, 1924, 1926, 1931), who made numerous collections but also acquired infected insects from correspondents, that the Laboulbeniales became better known among mycologists and entomologists. Thaxter set the stage for progress by describing a remarkable number of taxa: 103 genera and 1260 species. Fewer than 25 species of Pyxidiophora in the Pyxidiophorales are known. Many have been collected rarely, often described from single collections and never encountered again. They probably are more common and diverse than known collections indicate, but their rapid development in hidden habitats and difficulty of cultivation make species of Pyxidiophora easily overlooked and, thus, underreported (Blackwell and Malloch, 1989a,b; Malloch and Blackwell, 1993; Jacobs et al., 2005; Gams and Arnold, 2007). -
<I>Camerunensis</I> Sp. Nov. Parasitic O
MYCOTAXON ISSN (print) 0093-4666 (online) 2154-8889 © 2016. Mycotaxon, Ltd. July–September 2016—Volume 131, pp. 613–619 http://dx.doi.org/10.5248/131.613 Long-hidden in Thaxter’s treasure trove: Laboulbenia camerunensis sp. nov. parasitic on African Curculionidae Tristan W. Wang1, Danny Haelewaters2* & Donald H. Pfister2 1 Harvard College, 365 Kirkland Mailing Center, Cambridge, Massachusetts 02138, U.S.A. 2 Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, 22 Divinity Avenue, Cambridge, Massachusetts 02138, U.S.A. * Correspondence to: [email protected] Abstract—A new species, Laboulbenia camerunensis, parasitic on Curculio sp. from Cameroon, is described from a historical slide prepared by Roland Thaxter. It is the seventh species to be described from the family Curculionidae worldwide and the first from the African continent. The species is recognized by the characteristic outer appendage. The latter consists of two superimposed hyaline cells, separated by a black constricted septum, the suprabasal cell giving rise to two branches, the inner of which is simple and hyaline, and the outer tinged with brown. A second blackish constricted septum is found at the base of this outermost branch. Description, illustrations, and comparison to other species are given. Key words—Laboulbeniales, Laboulbeniomycetes, insect-associated fungi, taxonomy, weevils Introduction The order Laboulbeniales (Fungi, Ascomycota, Laboulbeniomycetes) consists of microscopic ectoparasites that develop on the exoskeleton of certain invertebrates. The hosts are primarily beetles but also include millipedes, mites, and a variety of insects (flies, ants, cockroaches, and others). Unlike other multicellular fungi, Laboulbeniales exhibit determinate growth, meaning that the fungal body (thallus) develops from a two-celled ascospore through a restricted and regulated number of mitotic divisions to produce an individual with a set number of distinctively arranged cells (Tavares 1985, Santamaría 1998). -
And Bat Fly-Associated Fungal Ectoparasites
Fungal Ecology 39 (2019) 371e379 Contents lists available at ScienceDirect Fungal Ecology journal homepage: www.elsevier.com/locate/funeco Climatic effects on the distribution of ant- and bat fly-associated fungal ectoparasites (Ascomycota, Laboulbeniales) * Tamara Szentivanyi a, b, , Danny Haelewaters c, d, e, Zoltan Radai f, Edvard Mizsei g, h, Walter P. Pfliegler i, Ferenc Bathori f, g, Andras Tartally f, Philippe Christe a, 1, Olivier Glaizot a, b, 1 a Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland b Museum of Zoology, Lausanne, Switzerland c Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA d Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, Cambridge, MA, USA e Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic f Department of Evolutionary Zoology and Human Biology, University of Debrecen, Debrecen, Hungary g Department of Ecology, University of Debrecen, Debrecen, Hungary h Department of Tisza Research, Hungarian Academy of Sciences, Centre for Ecological Research, Danube Research Institute, Debrecen, Hungary i Department of Molecular Biotechnology and Microbiology, University of Debrecen, Debrecen, Hungary article info abstract Article history: Laboulbeniales (Ascomycota: Laboulbeniomycetes) are obligate ectoparasitic fungi of arthropods with a Received 28 May 2018 worldwide distribution. Their effects on host physiology and behaviour as well as their ecology have Received in revised form recently gained wider attention. One aspect that is virtually unknown regarding Laboulbeniales and 11 March 2019 arthropod-associated fungi in general, is how abiotic factors shape the distribution of these parasites. We Accepted 13 March 2019 used ant- and bat fly-associated Laboulbeniales to study whether climatic elements play a role in the distribution of fungal species. -
Laboulbeniomycetes: Intimate Fungal Associates of Arthropods
Annual Review of Entomology Laboulbeniomycetes: Intimate Fungal Associates of Arthropods Danny Haelewaters,1,2,3 Meredith Blackwell,4,5 and Donald H. Pfister6 1Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana 47907, USA; email: [email protected] 2Department of Zoology, University of South Bohemia, 37005 Ceskéˇ Budejovice, Czech Republic 3Department of Biology, Research Group Mycology, Ghent University, 9000 Ghent, Belgium 4Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803, USA; email: [email protected] 5Department of Biological Sciences, University of South Carolina, Columbia, South Carolina 29208, USA 6Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, Cambridge, Massachusetts 02138, USA; email: [email protected] Annu. Rev. Entomol. 2021. 66:257–76 Keywords First published as a Review in Advance on biotrophs, fungal life history, Herpomycetales, insect dispersal, August 31, 2020 Laboulbeniales, Pyxidiophorales The Annual Review of Entomology is online at ento.annualreviews.org Abstract Access provided by Harvard University on 01/11/21. For personal use only. https://doi.org/10.1146/annurev-ento-013020- Arthropod–fungus interactions involving the Laboulbeniomycetes have Annu. Rev. Entomol. 2021.66:257-276. Downloaded from www.annualreviews.org 013553 been pondered for several hundred years. Early studies of Laboulbe- Copyright © 2021 by Annual Reviews. niomycetes faced several uncertainties. Were they parasitic worms, red al- All rights reserved gal relatives, or fungi? If they were fungi, to which group did they belong? What was the nature of their interactions with their arthropod hosts? The historical misperceptions resulted from the extraordinary morphological features of these oddly constructed ectoparasitic fungi. -
New Scientific Discoveries: Plants and Fungi
Received: 26 April 2020 | Revised: 4 June 2020 | Accepted: 5 June 2020 DOI: 10.1002/ppp3.10148 REVIEW New scientific discoveries: Plants and fungi Martin Cheek1 | Eimear Nic Lughadha2 | Paul Kirk3 | Heather Lindon3 | Julia Carretero3 | Brian Looney4 | Brian Douglas1 | Danny Haelewaters5,6,7 | Ester Gaya8 | Theo Llewellyn8,9 | A. Martyn Ainsworth1 | Yusufjon Gafforov10 | Kevin Hyde11 | Pedro Crous12 | Mark Hughes13 | Barnaby E. Walker2 | Rafaela Campostrini Forzza14 | Khoon Meng Wong15 | Tuula Niskanen1 1Identification and Naming, Royal Botanic Gardens, Kew, UK 2Conservation Science, Royal Botanic Gardens, Kew, UK 3Biodiversity Informatics and Spatial Analysis, Royal Botanic Gardens, Kew, UK 4Vilgalys Mycology Laboratory, Department of Biology, Duke University, Durham, NC, USA 5Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, USA 6Herbario UCH, Universidad Autónoma de Chiriquí, David, Panama 7Department of Biology, Research Group Mycology, Ghent University, Gent, Belgium 8Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, UK 9Department of Life Sciences, Imperial College London, London, UK 10Laboratory of Mycology, Institute of Botany, Academy of Sciences of the Republic of Uzbekistan, Tashkent, Uzbekistan 11Center of Excellence in Fungal Research, Mae Fah Luang University, Thailand 12Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands 13Royal Botanic Garden Edinburgh, Edinburgh, United Kingdom 14Jardim Botânico do Rio de Janeiro, Rio de Janeiro, Brasil 15Singapore Botanic Gardens, National Parks Board, Singapore, Singapore Correspondence Martin Cheek, Identification and Naming Societal Impact Statement Department, Royal Botanic Gardens, Kew, Research and publication of the planet's remaining plant and fungal species as yet Richmond TW9 3AE, UK. Email: [email protected] unknown to science is essential if we are to address the United Nations Sustainable Development Goal (SDG) 15 “Life on Land” which includes the protection of ter- restrial ecosystems and halting of biodiversity loss. -
New and Interesting <I>Laboulbeniales</I> From
ISSN (print) 0093-4666 © 2014. Mycotaxon, Ltd. ISSN (online) 2154-8889 MYCOTAXON http://dx.doi.org/10.5248/129.439 Volume 129(2), pp. 439–454 October–December 2014 New and interesting Laboulbeniales from southern and southeastern Asia D. Haelewaters1* & S. Yaakop2 1Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University 22 Divinity Avenue, Cambridge, Massachusetts 02138, U.S.A. 2Faculty of Science & Technology, School of Environmental and Natural Resource Sciences, Universiti Kebangsaan Malaysia, Bangi 43600, Malaysia * Correspondence to: [email protected] Abstract — Two new species of Laboulbenia from the Philippines are described and illustrated: Laboulbenia erotylidarum on an erotylid beetle (Coleoptera, Erotylidae) and Laboulbenia poplitea on Craspedophorus sp. (Coleoptera, Carabidae). In addition, we present ten new records of Laboulbeniales from several countries in southern and southeastern Asia on coleopteran hosts. These are Blasticomyces lispini from Borneo (Indonesia), Cantharomyces orientalis from the Philippines, Dimeromyces rugosus on Leiochrodes sp. from Sumatra (Indonesia), Laboulbenia anoplogenii on Clivina sp. from India, L. cafii on Remus corallicola from Singapore, L. satanas from the Philippines, L. timurensis on Clivina inopaca from Papua New Guinea, Monoicomyces stenusae on Silusa sp. from the Philippines, Ormomyces clivinae on Clivina sp. from India, and Peyritschiella princeps on Philonthus tardus from Lombok (Indonesia). Key words — Ascomycota, insect-associated fungi, morphology, museum collection study, Roland Thaxter, taxonomy Introduction One group of microscopic insect-associated parasitic fungi, the order Laboulbeniales (Ascomycota, Pezizomycotina, Laboulbeniomycetes), is perhaps the most intriguing and yet least studied of all entomogenous fungi. Laboulbeniales are obligate parasites on invertebrate hosts, which include insects (mainly beetles and flies), millipedes, and mites. -
Checklist of Thallus-Forming Laboulbeniomycetes from Belgium and the Netherlands, Including Hesperomyces Halyziae and Laboulbenia Quarantenae Spp
A peer-reviewed open-access journal MycoKeys 71: 23–86Checklist (2020) of Laboulbeniomycetes from Belgium and the Netherlands 23 doi: 10.3897/mycokeys.71.53421 RESEARCH ARTICLE MycoKeys http://mycokeys.pensoft.net Launched to accelerate biodiversity research Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including Hesperomyces halyziae and Laboulbenia quarantenae spp. nov. Danny Haelewaters1,2,3, André De Kesel4 1 Purdue University, West Lafayette, Indiana, United States of America 2 University of South Bohemia, České Budějovice, Czech Republic 3 Ghent University, Ghent, Belgium 4 Meise Botanic Garden, Meise, Belgium Corresponding author: Danny Haelewaters ([email protected]) Academic editor: Cecile Gueidan | Received 19 May 2020 | Accepted 7 July 2020 | Published 30 July 2020 Citation: Haelewaters D, De Kesel A (2020) Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including Hesperomyces halyziae and Laboulbenia quarantenae spp. nov.. MycoKeys 71: 23–86. https://doi.org/10.3897/mycokeys.71.53421 Abstract In this paper we present an updated checklist of thallus-forming Laboulbeniomycetes (Ascomycota, Pezi- zomycotina), that is, the orders Herpomycetales and Laboulbeniales, from Belgium and the Netherlands. Two species are newly described based on morphology, molecular data (ITS, LSU ribosomal DNA) and ecology (host association). These areHesperomyces halyziae on Halyzia sedecimguttata (Coleoptera, Coc- cinellidae) from both countries and Laboulbenia quarantenae -
New Species and New Records of Laboulbeniales (Ascomycota) from Thailand
Mycosphere 9(6): 1151–1172 (2018) www.mycosphere.org ISSN 2077 7019 Article Doi 10.5943/mycosphere/9/6/6 New species and new records of Laboulbeniales (Ascomycota) from Thailand Rossi W and Bernardi M Sect. Environmental Sciences, Dept. MeSVA, University of L’Aquila, 67100 Coppito (AQ), Italy Rossi W, Bernardi M 2018 – New species and new records of Laboulbeniales (Ascomycota) from Thailand. Mycosphere 9(6), 1151–1172, Doi 10.5943/mycosphere/9/6/6 Abstract Eight new species of Laboulbeniales (Ascomycota) are described. These are Corethromyces fuscoramosus, parasitic on Medon sp. (Coleoptera, Staphylinidae); Eucantharomyces ferreroi, parasitic on Pogonoglossus sp. (Coleoptera, Carabidae); Euphoriomyces rugosus, parasitic on Agathidium sp. (Coleoptera, Leiodidae); Kyphomyces siamensis, parasitic on Holotrochus sp. (Staphylinidae); Rickia cifoneae, parasitic on Melisia spp. (Acarina, Canestriniidae); Stigmatomyces coronatus, parasitic on Ochthera sp. (Diptera, Ephydridae); Teratomyces cylindrocarpus, parasitic on Diochus sp. (Staphylinidae); Zeugandromyces assingii, parasitic on Neosclerus areolatus (Staphylinidae). Twenty-nine species are reported for the first time from Thailand, 5 of which are new for the whole Asian continent and 8 are recorded for the first time after description. A new synonymy is established: Stigmatomyces subcircinalis Thaxt. 1931 = S. tortilis Thaxt. 1918. Key words – 8 new species – Ectoparasitic fungi – Indochina – Mites – Laboulbeniomycetes – Taxonomy Introduction The first records of Laboulbeniales from Thailand are more than one hundred years old. These are two species of Laboulbenia (L. orectochili Thaxt. and L. proliferans Thaxt.) reported by Roland Thaxter in the second part of his huge monograph, in 1908. A third species was added only after 72 years, i.e. Arthrorhynchus eucampsipodae Thaxt. (Blackwell 1980). -
NHBSS 032 1H Sugiyama Lab
48 K. SUGIYAMA AND D. PHANICHAPOL Genus Dimeromyces Thaxter: D. cherrhonesites Balazuc, D. oscinosomalis Thaxter. Genus Enathromyces Thaxter: E. indicus Thaxter. Genus Laboulbenia Peyritsch: L. anoplogenii Thaxter, L. catascopi Thaxter, L. celestia/is Thaxter, L. idiostoma Thaxter, L. kunckelii (Giard) Thaxter, L. morionis Thaxter, L. pheropsophi Thaxter, L. proliferans Thaxter, and L. tachys Thaxter. Genus Rickia Thaxter: R. eumorphi Thaxter. Genus Rhynchophoromyces Thaxter : R. denticulatus Thaxter and R. rostratus Thaxter. Genus Zodiomyces Thaxter : Z. subseriatus Thaxter. The present paper includes descriptions of all species of the Laboulbeniomycetes collected in Thailand, their host insects and distribution. DESCRIPTIONS OF SPECIES 1. Autoicomyces falcifer (Thaxter) Thaxter, Mem. Amer. Acad. Arts Sci. 13:435 (1908) et 16: 357 (1931). SUGIYAMA & SHAZAWA. Trans. myco/. Soc. Japan 18: 220 (1977). (Fig. 2, D). Ceratomyces falcifer Thaxter, Proc. Amer. Acad. Arts Sci. 41 : 318 (1905). Autoicomyces japonicus Thaxter, Mem. Amer. Acad. Arts Sci. 16 : 359 (1931 ). SuGIYAMA, Ginkgoana 2 : 18 (1973). Total length to the tip of perithecium exclusive of the apical projection, 205 fl. m long. 80 tJ.m thick. Thallus hyaline, uniformly yellowish, partly darkened, consis ting of a receptacle and a perithecium. Receptacle cylindrical, hyaline, consisting of the basal and dis tal portions, 95 tJ.m long, 70 tJ.m thick; the basal portion gradually tapering towards the basal end, forming the stalk portion of the thallus, forming an obconical foot at the basal end, comprising 3 one-cell layers, 62 tJ.m long, 30 fl.m thick; the distal portion darker than the basal portion, free from the perithecium except for the basal part, tapering towards the distal and, 112 tJ.m long, 27 tJ.m thick. -
MYCOTAXON ISSN (Print) 0093-4666 (Online) 2154-8889 © 2016
MYCOTAXON ISSN (print) 0093-4666 (online) 2154-8889 © 2016. Mycotaxon, Ltd. July–September 2016—Volume 131, pp. 613–619 http://dx.doi.org/10.5248/131.613 Long-hidden in Thaxter’s treasure trove: Laboulbenia camerunensis sp. nov. parasitic on African Curculionidae Tristan W. Wang1, Danny Haelewaters2* & Donald H. Pfister2 1 Harvard College, 365 Kirkland Mailing Center, Cambridge, Massachusetts 02138, U.S.A. 2 Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, 22 Divinity Avenue, Cambridge, Massachusetts 02138, U.S.A. * Correspondence to: [email protected] Abstract—A new species, Laboulbenia camerunensis, parasitic on Curculio sp. from Cameroon, is described from a historical slide prepared by Roland Thaxter. It is the seventh species to be described from the family Curculionidae worldwide and the first from the African continent. The species is recognized by the characteristic outer appendage. The latter consists of two superimposed hyaline cells, separated by a black constricted septum, the suprabasal cell giving rise to two branches, the inner of which is simple and hyaline, and the outer tinged with brown. A second blackish constricted septum is found at the base of this outermost branch. Description, illustrations, and comparison to other species are given. Key words—Laboulbeniales, Laboulbeniomycetes, insect-associated fungi, taxonomy, weevils Introduction The order Laboulbeniales (Fungi, Ascomycota, Laboulbeniomycetes) consists of microscopic ectoparasites that develop on the exoskeleton of certain invertebrates. The hosts are primarily beetles but also include millipedes, mites, and a variety of insects (flies, ants, cockroaches, and others). Unlike other multicellular fungi, Laboulbeniales exhibit determinate growth, meaning that the fungal body (thallus) develops from a two-celled ascospore through a restricted and regulated number of mitotic divisions to produce an individual with a set number of distinctively arranged cells (Tavares 1985, Santamaría 1998).