Evidence for Multiple Evolutionary Origins in the Moss Flora of Macaronesia
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BRIEF COMMUNICATION doi:10.1111/j.1558-5646.2009.00787.x AND IF ENGLER WAS NOT COMPLETELY WRONG? EVIDENCE FOR MULTIPLE EVOLUTIONARY ORIGINS IN THE MOSS FLORA OF MACARONESIA Delphine A. Aigoin,1,2,3 Nicolas Devos,1,4 Sanna Huttunen,5,6 Michael S. Ignatov,7,8 Juana M. Gonzalez-Mancebo,9,10 and Alain Vanderpoorten1,11 1Institute of Botany, University of Liege,` 27 Blvd du Rectorat, B22, Sart Tilman, 4000 Liege,` Belgium 2E-mail: [email protected] 3Institute of Evolutionary Sciences, University of Montpellier II, Place Eugene` Bataillon, 34095 Montpellier Cedex 5, France 4E-mail: [email protected] 5Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland 6E-mail: shuttu@utu.fi 7Main Botanical Garden of Russian Academy of Sciences, Botanicheskaya 4, 127276 Moscow, Russia 8E-mail: [email protected] 9Department of Botany, University of La Laguna, 38271 La Laguna, Tenerife, Canary Islands, Spain 10E-mail: [email protected] 11E-mail: [email protected] Received March 27, 2009 Accepted June 23, 2009 The Macaronesian endemic flora has traditionally been interpreted as a relict of a subtropical element that spanned across Europe in the Tertiary. This hypothesis is revisited in the moss subfamily Helicodontioideae based on molecular divergence estimates derived from two independent calibration techniques either employing fossil evidence or using an Monte Carlo Markov Chain (MCMC) to sample absolute rates of nucleotide substitution from a prior distribution encompassing a wide range of rates docu- mented across land plants. Both analyses suggest that the monotypic Madeiran endemic genus Hedenasiastrum diverged of other Helicodontioideae about 40 million years, that is, well before Macaronesian archipelagos actually emerged, in agreement with the relict hypothesis. Hedenasiastrum is characterized by a plesiomorphic morphology, which is suggestive of a complete morpho- logical stasis over 40 million years. Macaronesian endemic Rhynchostegiella species, whose polyphyletic origin involves multiple colonization events, evolved much more recently, and yet accumulated many more morphological novelties than H. percurrens. The Macaronesian moss flora thus appears as a complex mix of ancient relicts and more recently dispersed, fast-evolving taxa. KEY WORDS: Bryophytes, fossils, macronesian endemism, molecular dating, morphological evolution. Macaronesia is a string of North Atlantic volcanic islands (the demism (see Juan et al. 2000 for review). Engler (1879), fol- Azores, Madeira, Canaries, and Cape Verde) that emerged 0.4– lowed by many biogeographers (see Vanderpoorten et al. 2007 20 million years ago and are characterized by high rates of en- for review), proposed that Macaronesian endemics are the relics C 2009 The Author(s). Journal compilation C 2009 The Society for the Study of Evolution. 3248 Evolution 63-12: 3248–3257 BRIEF COMMUNICATION of biota that were widespread across Europe during the Tertiary phological stasis since the Tertiary period among Macaronesian and decimated on the continent during the glaciations. In con- endemics. trast with the expectations of the refugium concept, however, several lines of evidence from analyses of moss species dis- tributions (Vanderpoorten et al. 2007) and molecular evolution Material and Methods rates in angiosperms (Carine 2005) have recently questioned En- TAXONOMIC AND MORPHOLOGICAL CHARACTER gler’s hypothesis. In mosses, the hypothesis of extinction of a SAMPLING Tertiary flora in all but Macaronesian areas is solely supported The 17 genera of Helicodontioideae as circumscribed by Aigoin by extremely limited fossil evidence in the genus Echinodium et al. (2009) were sampled (Table 1). Each genus was represented (Frahm 2004). This interpretation is, however, weakened by the by one to three species, with a special emphasis on Rhynchoste- polyphyletic origin of the genus (Stech et al. 2008), thereby giella, for which all eight species were sampled. Three other raising doubts about the actual sister relationship between fos- species, namely R. papuensis, R. leptoneura,andR. muriculata, sil and extant Macaronesian Echinodium species. By contrast, clearly do not belong to the genus, and the appropriate taxonomic the nested phylogenetic position of the Azorean endemic liver- changes will be presented elsewhere. Aerobryidium filamentosum, wort Leptoscyphus azoricus within a Neotropical clade (Devos a species of the sister family Meteroriaceae, as well as representa- and Vanderpoorten 2009); the close biogeographic affinities of tive taxa of each of the three subfamilies of Brachytheciaceae was several Macaronesian groups with the North and South Ameri- sampled as outgroups (Table 1). Forty-three morphological char- can continents (see Vanderpoorten et al. [2007] for review); and acters that are variable across the Helicodontioideae, including the polyphyletic origin among Macaronesian populations of the 34 gametophytic and nine sporophytic ones, were scored for each moss Grimmia montana, which are genetically identical or most of the sampled taxa (Appendices S1 and S2) (see Huttunen and closely related to those of different continents (Vanderpoorten Ignatov [2004] for a thorough account on character significance et al. 2008) all point to recurrent migrations between the latter and description). and the Macaronesian archipelagos, potentially followed by in situ MOLECULAR PROTOCOLS AND PHYLOGENETIC speciation. ANALYSES The continental extinction and recent speciation hypothe- Four chloroplast regions (trnL-trnF, atpB-rbcL, psbT-psbH, and ses make different predictions regarding the rates of speciation psbA-trnH) were selected for exhibiting the appropriate level of and morphological evolution. In fact, as opposed to neoendemics, variation at the genus level in the Brachytheciaceae (Huttunen and which originated from local speciation processes and often under- Ignatov 2004). DNA extraction, PCR and sequencing protocols, went spectacular adaptive radiations involving a sudden burst of sequence editing, alignment, indel scoring, and selection of mod- morphological diversification (see Gillepsie and Roderick [2002] els for DNA substitutions and indel evolution follow Aigoin et al. for review), paleoendemics, which survived continental extinc- (2009). Phylogenetic reconstruction was conducted with MrBayes tions on the islands, have most often retained a highly conserved 3.1.2. Four independent Monte Carlo Markov Chains (MCMCs) morphology for millions, or tens of million years, to such an extent of 2,000,000 iterations each were run and trees and model param- that extant taxa appear conspecific with fossil species (Sunding eters were sampled every 10,000 generations. The convergence 1979). of the MCMCs was verified visually from the likelihood values, In this article, we revisit hypotheses on the origin of Mac- and trees of the “burn-in” were discarded. aronesian endemism in the mosses from the Brachytheciaceae, A significant departure of alternative topologies involving a subfamily Helicodontioideae. This group includes several Mac- monophyletic origin of the three Macaronesian endemic Rhyn- aronesian endemics, namely the monotypic Madeiran Hedenasi- chostegiella species, namely R. bourgeana, R. macilenta,andR. astrum percurrens,andthreeRhynchostegiella species: Rhyn- trichophylla, was tested by constrained analyses. The MCMC chostegiella bourgeana and R. trichophylla, which are restricted analysis described above was rerun under the constraint that only to the Canary Islands, and R. macilenta, whose distributions trees fitting with a monophyletic origin of the Macaronesian en- span Madeira and the Canaries. In addition, and unlike most demic Rhynchostegiella species were sampled. We then deter- bryophytes, a fairly well-documented fossil record is available mined whether the constraint induced a significant loss of like- (Miller 1984). We produced a molecular phylogeny of the Heli- lihood by means of the Bayes factors, as assessed by twice the codontioideae to test the hypothesis of a radiation within Rhyn- difference in the log marginal likelihood between the two runs. chostegiella and date the origin of its Macaronesian endemic lin- eages, contrasting the results derived from a fossil calibration and MOLECULAR DATING an analysis employing absolute rates of molecular evolution. We Times of divergence were calculated to determine the origin then used the phylogeny to test the hypothesis of a long mor- of the most recent common ancestor (hereafter, MRCA) of H. EVOLUTION DECEMBER 2009 3249 BRIEF COMMUNICATION Table 1. Taxon sampling, voucher information (for sequences produced for the present study), and GenBank accession numbers. Species trnL/trnF atpB/rbcL psbT/psbH psbA/trnH Voucher specimen for sequences 3250 Aerobryidium filamentosum (Hook.) M. Fleisch. AF397789 – AF417347 – Aerolindigia capillacea (Hornsch.) M. Menzel FJ262414 FJ262441 FJ262474 FJ262499 Ecuador, Toapanta & Caranqui 1437 (MO) Brachytheciastrum collinum (Schleich. ex Mull.¨ Hal.) AY184776 AY663296 AY184757 – EVOLUTION Ignatov and Huttunen Brachythecium salebrosum (Hoffm. ex F. Weber and AF397857 AY663309 AF417448 AY312896 D. Mohr) Schimp. Bryhnia novae-angliae (Sull. and Lesq.) Grout AF161122 AJ288397 AF417405 – DECEMBER 2009 Bryoandersonia illecebra (Hedw.) H. Rob. AF397819 – AF417365 FJ262501 USA, Bowers 22214 (MA) Cirriphyllum crassinervium (Taylor) Loeske and M. Fleisch. FJ262415 FJ262443 FJ262476 FJ262502 France, Vanderpoorten 413 (LG) Cirriphyllum koponenii (Ignatov) Ignatov and Huttunen