doi: 10.15407/ukrbotj73.02.178 D.V. LEONTYEV Kharkiv State Zooveterinary Academy 1, Akademichna Str., Kharkiv, 62134, Ukraine [email protected] THE EVOLUTION OF SPOROPHORE IN RETICULARIACEAE (MYXOMYCETES) Leontyev D.V. The evolution of sporophore in Reticulariaceae (Myxomycetes). Ukr. Bot. J., 2016, 73(2): 178—184. Kharkiv State Zooveterinary Academy 1, Akademichna Str., Kharkiv, 62134, Ukraine [email protected] Abstract. Recent molecular studies have clarified the phylogenetic relations within the family Reticulariaceae (Myxomycetes, Myxogastrea), allowing to reconstruct the ways of the morphological evolution within the family. We conclude, that the general tendency of the sporophore evolution in Reticulariaceae was the transformation of the stalked forms to the sessile ones, followed by the development of the metameric sporophores, called pseudoaethalia and aethalia, from the separate sporocarps. The common ancestor of the family was similar to Alwisia lloydiae having stalked sporocarps and tubular capillitium. At least four evolutionary lineages originated form this ancestor: 1) Alwisia → Tubifera, 2) Alwisia → Rigidotubula (and probably Siphoptychium), 3) Alwisia → (Lycogala) → Thecotubifera, 4) Alwisia → Lycogala → Reticularia. In each of these branches, the processes like a loss of stalks, transition from spherical to elongated sporothecae, transformation of solitary sporocarps to grouped ones, a loss of capillitium and formation of pseudocapillitium, have occurred independently. Therefore, the type of the fruiting body, and presence of capillitium or pseudocapillitium, cannot be considered as sufficient criteria for separating myxomycete genera. Key words: 18S rDNA, aethalium, capillitium, convergence, paralellism, phylogeny, pseudoaethalium, pseudocapilliti- tum, spore ornamentation, sporocarp, sporotheca. Myxogastrea, or Myxomycetes, are the group of ameboid epidendrum (L.) Fr., Tubifera ferruginosa (Batsch) J.F. eukaryotes, able to produce macroscopic fruiting bodies Gmel., and T. dictyoderma Nann.-Bremek. & of complicate structure. Within the group, five orders Loer. in their traditional understanding appeared and about twelve families are traditionally recognized, to be polyphyletic. A revision of these taxa, based among which the family Reticulariaceae is characterized on morphological and molecular data, allowed to by the absence of true capillitium and pseudoaethaliate describe 9 new species: Alwisia lloydiae Leontyev, or aethaliate structure of the fruiting bodies (Nannenga- S.L. Stephenson et Schnittler, A. morula G. Moreno, Bremekamp, 1991; Neubert et al., 1993; Lado, Pando, Leontyev, D.W. Mitch., S.L. Stephenson, C. Rojas & 1997; Ing, 1999; Poulain et al., 2011). Schnittler, A. repens Leontyev, Schnittler, G. Moreno, The traditional understanding of the taxonomical S.L. Stephenson, D.W. Mitchell & C. Rojas, structure and discriminative features of Reticulariaceae Tubifera applanata Leontyev & Fefelov, T. corymbosa was reconsidered in our recent study, based on the Leontyev, Schnittler, S.L. Stephenson & L.M. Walker, 18S rDNA phylogeny (Leontyev et al., 2014a; 2014b; T. dudkae (Leontyev & G. Moreno) Leontyev, 2015). The family, with a few exceptions, appeared Moreno & Schnittler, T. magna Leontyev, Schnittler, to be a monophyletic taxon, subdivided to at least S.L. Stephenson & T. Kryvomaz, T. montana Leontyev, six clusters, which corresponds to the genera Alwisia Schnittler & S.L. Stephenson, T. pseudomicrosperma Berk. & Broome, Lycogala Adans., Reticularia Leontyev, Schnittler & S.L. Stephenson, and two Bull., Tubifera G.F. Gmel., Rigidotubula ad int. and subspecies: T. ferruginosa subsp. ferruginosa Leontyev, Thecotubifera ad int., among which Alwisia was re- Schnittler & S.L. Stephenson and T. ferruginosa subsp. erected (Leontyev et al., 2014a; 2014b), and two last acutissima Leontyev, Schnittler & S.L. Stephenson names are to be published as new to science. One more (Leontyev et al., 2014a; 2014b; 2015). Two more species genus, the recently re-erected Siphoptychium Rostaf., (Rigidotubula reticulata ad int., R. violacea ad int.) was united with Reticulariaceae based on morphological and one new combination (Thecotubifera dictyoderma data (Leontyev, 2015). ad int., comb. nov. pro Tubifera dictyoderma Nann.- The genera Reticularia and Tubifera, species Bremek. & Loer.) are prepared for the publication. Alwisia bombarda Berk. & Broome, Lycogala The species of Reticularia which have warty spores © D.V. LEONTYEV, 2016 with olive, golden-yellow or brown pigmentation 178 ISSN 0372-4123. Ukr. Bot. J., 2016, 73(2) Fig. 1. Phylogeny of the Reticulariaceae based on 18S rDNA 5’-domain sequences. The tree was constructed by Bayesian Inference. ML bootstrap replicates above 50 and Bayesian posterior probabilities above 0.5 are shown for each branch. A hyphen indicates a conflicting topology. The scale bar indicates the fraction of substitutions per site. Asterisk: the genotype displayed by the type specimen of the respective taxon. ISSN 0372-4123. Укр. ботан. журн., 2016, 73(2) 179 Tubifera Reticularia Siphoptychium Rigidotubula violacea, Reticularia intermedia casparyi R. reticulata Secondary formation of Tubifera microsperma, capillitium T. pseudomicrosperma Reticularia lycoperdon Reduction Formation of columella Branched pseudocapillitium of spherical sporothecae Cartilaginous peridium ? Tubifera dimorphotheca Tubifera applanata Reticularia Tubifera ferruginosa splendens, T.montana, T.magna R. jurana Hypothallic stalk Reduction of spherical Formation sporothecae of aethalium Thecotubifera dictyoderma Formation of pseudocapillitium Tubifera corymbosa Tubifera dudkae Formation of cortex Formation of cylindrical ? sporothecae ? Ancestral form Reticularia lobata Ancestral form Spongy hypothallus Reduction of capillitium Pseudoaethalium formation Pseudoaethalium formation Alwisia Siphoptychium? Secondary formation Alwisia repens of capillitium Lycogala epidendrum Stalk reduction Grouping of sporocarps Siphoptychium? Alwisia morula Lycogala conicum, L. exiguum Reduction of capillitium Reduction of hypothallus Confluence Reduction of stalks of stalk Lycogala Alwisia bombarda Alwisia lloydiae Lycogala flavofuscum Last common ancestor Fig. 2. Evolution of the sporophore in Reticulariaceae. The genealogy of taxa corresponds to the current understanding of the phylogeny of the group (see Fig. 1). Bars indicate the most important evolutionary changes. Dotted arrows show the alternative evolutionary scenarios. Gray filling unites the members of the same genus. 180 ISSN 0372-4123. Ukr. Bot. J., 2016, 73(2) (R. liceoides, R. olivacea, R. aurea, R. rubiginosa, The next plesiomorphic character of Alwisia is the R. simulans) on the basis of obtained data were excluded presence of a well-developed capillitium, resembling from the family Reticulariaceae. The first two species that of another bright-spored myxomycetes, were removed to Cribrariaceae, with the simultaneous Dianemataceae and Trichiaeceae. This similarity re-erection of the genus Licaethalium Rostaf. (Leontyev supports a hypothesis that the presence of capillitium et al., 2015). is the basal characteristic for the Reticularaceae and for The current understanding of the phylogeny of the Lucisporodia in general. Reticulariaceae, based on these data, is shown in Fig. 1. Among species of Alwisia, two are characterized The results obtained have allowed to look at the by well developed, free stalks, and another two morphological diversity of Reticulariaceae from a new (A. bombarda, A. lloydiae) – by the presence of point. In contrast to the traditional understanding, the capillitium (A. morula, A. lloydiae). There is only one family appeared to include species with stalked and known species, which unites both plesiomorphies lost sessile sporocarps (Alwisia lloydiae, A. repens, A. morula), by most of Reticulariaceae, the A. lloydiae, which we pseudoaethalia with the entire cortex (Thecotubifera consider as the closest to the last common ancestor dictyoderma) and pseudoaethalia, composed of spherical of the family. It is noteworthy that this species occurs sporothecae (Tubifera dudkae). The true capillitium was in the Australian continent and in Tasmania, the well found to be rather common structure within the family, known refuges of a relict biota. being developed in Alwisia, Lycogala and Siphoptychium, From the basal form, related with A. lloydiae, at while the threads, described in sporocarps of Tubifera least three evolutionary lineages have originated. First (Nannenga-Bremekamp, 1991; Neubert et al., 1993), of them is represented by the vector A. lloydiae → appeared to be fungal hyphae, feeding with the spores, A. morula → A. repens, in which the sporothecae lose but not a capillitium (Leontyev et al., 2015). the capillitium (A. morula) and their stalks become New knowledge about the phylogeny of the procumbent (A. repens). We suppose that this lineage group, together with a deeper understanding of its has continued in the genera Tubifera, Rigidotubula, morphological variability, gives us a chance to understand and probably Siphoptychium. Simultaneously to the how the structure of these organisms was changed in the loss of capillitium and stalks, the spore dissemination process of evolution. In a response to this possibility, type changed from the active way, with the help of we composed a concept which describes regularities of capillitium, to the passive one, using rain drops and/or the evolutionary changes of the sporophore structure in insects. Reticulariaceae (Fig.