Evolution and reproduction modes in the Roccella galapagoensis aggregate (Roccellaceae, Arthoniales)

Abstract

The “species pair” concept obscures both intra‐ and interspecific relationships and should be abandoned, evolutionarily and taxonomically. Based on our molecular phylogenetic work on the genus Roccella we are able to show for the first time that sexually and vegetatively dispersed entities in an anticipated “species pair” (Roccella galapagoensis/R. lirellina) actually form several distinct monophyletic genotypes, here interpreted as species in which sexual reproduction has been repeatedly evolved. The species accepted here are based on a phylogenetic hypothesis supported by data from the ITS rDNA region and an unidentified locus possibly related to calmodulin. Altogether 89 sequences from both loci were newly produced and used in phylogenetic analyses. The Roccella galapagoensis aggregate was resolved as monophyletic. The sister group includes Roccella decipiens (sexual) and R. gracilis (asexual). Based on the present data it is equally parsimonious to suggest a sorediate or a fertile ancestor to the Roccella galapagoensis aggregate. The ancestor must have arrived in the Galapagos Islands through long distance dispersal and have included the ability to reproduce both sexually with ascospores and asexually with soredia. Taxonomy, nomenclature and phylogeny are provided for five American Roccella species in the Roccella galapagoensis aggregate with geographical focus on the Galapagos Islands. One species is obligatory sexual, one is obligatory asexual and three species are facultative sexual/asexual. Roccella albida Tehler is newly described. Roccella canariensis is united with R. tinctoria.

The phylogeny of Arthoniales (Pezizomycotina) inferred from nucLSU and RPB2 sequences

“…2m), as already shown in numerous previous studies based on both morphological and molecular data Myllys 1999;Tehler 1983Tehler , 1990Tehler and Irestedt 2007). Roccella is the first large and critical genus of the Arthoniales for which all species are now sequenced (Tehler and Irestedt 2007;Tehler et al 2009aTehler et al ,b, 2010. Only three species of Dirina are included in our phylogenetic tree, but a more detailed phylogenetic study of this genus is currently undertaken (Tehler et al, in prep.…”

“…This unusual high level of homoplasy might indicate that the Arthoniales is a very old group with taxa having evolved in parallel for very long times including sub-groups that have experienced adaptive radiation with subsequent convergent evolution. As discussed by Tehler et al (2009a) the precursors to the genus Roccella may actually have evolved and established a distribution already at the opening of the Atlantic Ocean in the Mesozoic. Despite the fact that this implies a very slow evolutionary rate and that conservative evolution prevailed for species over long period of times, it is obvious that adaptive radiation also must have played an important role in the evolution of other species in Roccella, as shown by the rapid evolution of the Roccella galapagoensis complex.…”

“…These two counterparts were traditionally treated as separate species. As shown by a detailed study of the genus Roccella (Tehler et al 2009a, and references therein), the "species pair" concept should be abandoned, both evolutionarily and taxonomically, because it obscures intra-and interspecific relationships. This standpoint is evidently supported by our results on Schismatomma albocinctum (incl.…”

“…Endemism is common in the family Roccellaceae, in which many monotypic genera were described with an often much reduced distribution area, and particularly in the genera Roccella and Roccellina. E.g., the genus Roccella contains not less than 13 endemic species, more than half of the currently recognised 24 species (Tehler et al 2009a(Tehler et al ,b, 2010. The diversity of life-habits and the high degree of endemism render the phylogenetic study of the Arthoniales exciting in many aspects (evolution, phylogeography, taxonomy, etc.…”

“…It was shown that the fruticose growth habit has evolved or been lost multiple times in the Roccellaceae and several times even within genera. More recently, the origin, evolution and taxonomy of the genus Roccella were studied in detail using several loci (Tehler et al 2009a(Tehler et al ,b, 2010. The authors concluded that the "species pair" concept should be abandoned in these genera.…”