Origins and Diversity of a Cosmopolitan Fern Genus on an Island Archipelago
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Research Article SPECIAL ISSUE: Island Plant Biology—Celebrating Carlquist’s Legacy Origins and diversity of a cosmopolitan fern genus on an island archipelago Paul G. Wolf1,2*, Carol A. Rowe1, Joshua P. Der3, Martin P. Schilling1, Clayton J. Visger4 and John A. Thomson5 1 Department of Biology, Utah State University, Logan, UT 84322, USA 2 Ecology Center, Utah State University, Logan, UT 84322, USA 3 Department of Biological Science, California State University, Fullerton, CA 92834, USA 4 Department of Biology, University of Florida, Gainesville, FL 32611, USA 5 National Herbarium of NSW, Royal Botanic Gardens and Domain Trust, Mrs Macquaries Road, Sydney, NSW 2000, Australia Received: 29 July 2015; Accepted: 9 October 2015; Published: 20 October 2015 Associate Editor: Chelsea D. Specht Citation: Wolf PG, Rowe CA, Der JP, Schilling MP, Visger CJ, Thomson JA. 2015. Origins and diversity of a cosmopolitan fern genus on an island archipelago. AoB PLANTS 7: plv118; doi:10.1093/aobpla/plv118 Abstract. Isolated oceanic islands are characterized by patterns of biological diversity different from that on nearby continental mainlands. Isolation can provide the opportunity for evolutionary divergence, but also set the stage for hybridization between related taxa arriving from different sources. Ferns disperse by haploid spores, which are pro- duced in large numbers and can travel long distances in air currents, enabling these plants to become established on most oceanic islands. Here, we examine the origins and patterns of diversity of the cosmopolitan fern genus Pteridium (Dennstaedtiaceae; bracken) on the Galapagos Islands. We use nucleotide sequences from two plastid genes, and two nuclear gene markers, to examine phylogeography of Pteridium on the Galapagos Islands. We incorp- orate data from a previous study to provide a worldwide context. We also sampled new specimens from South and Central America. We used flow cytometry to estimate genome size of some accessions. We found that both plastid and nuclear haplotypes fall into two distinct clades, consistent with a two-diploid-species taxonomy of P. aquilinum and P. esculentum. As predicted, the allotetraploid P. caudatum possesses nuclear haplotypes from both diploid spe- cies. Samples from the Galapagos include P. esculentum subsp. arachnoideum, P. caudatum and possible hybrids between them. Multiple Pteridium taxa were also observed growing together at some sites. We find evidence for mul- tiple origins of Pteridium on the Galapagos Islands and multiple origins of tetraploid P. caudatum throughout its range in Central and South America. We also posit that P. caudatum may include recent diploid hybrids, backcrosses to P. esculentum, as well as allotetraploid plants. The Galapagos Islands are positioned close to the equator where they can receive dispersing propagules from both hemispheres. This may partly explain the high levels of diversity found for this cosmopolitan fern on these islands. Keywords: Biogeography; bracken; ferns; Galapagos; hybridization; islands; nuclear genes; phylogeny; Pteridium. * Corresponding author’s e-mail address: [email protected] Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properlycited. AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 1 Wolf et al. — Origins of Galapagos Pteridium Introduction morphological characters, including those that are used for taxonomic treatments. Furthermore, regional and Oceanic islands provide an ideal biological setting for local treatments often do not incorporate the context of evolutionary change and thus for the study of evolution- variation that is seen at the global scale. A few authors ary processes. On islands that are distantly isolated from have examined Pteridium in a worldwide context. For continents, there can be an increased opportunity for example, Ching (1940) considered the genus to comprise organisms to diverge genetically from those in the ori- 6 species, whereas a year later, Tryon (1941) treated ginal source populations. Furthermore, remote islands Pteridium as a single species with 2 subspecies and 12 can act as a sink for individuals of the same species varieties. Page (1976) reviewed information on geo- (or closely related species) arriving from more than one graphic variation and concluded that there is probably original source, thereby setting the stage for hybridiza- more than one species, but he made no formal taxonomic tion, increased genetic diversity, or both. Angiosperms changes. More recently, in a series of articles (Thomson and gymnosperms colonize islands most often via 2000, 2012; Thomson et al. 2008), Thomson has recog- seeds, which contain diploid embryos. This is contrasted nized two main diploid species: P. aquilinum (correspond- in ferns (monilophytes) and lycophytes, which are dis- ing to Tryon’s subspecies aquilinum) from Europe, North persed by haploid spores. In many cases, spore-bearing America, Asia and Africa and P. esculentum (correspond- plants require two spores, and subsequently two gameto- ing approximately to Tryon’s subspecies caudatum). phytes, for successful establishment (Soltis and Soltis Pteridium esculentum is treated by some authors as two 1987; Soltis et al. 1988). Moreover, spore-dispersed plants species: P. esculentum in Australia and New Zealand and appear to have high levels of gene flow relative to seed P. arachnoideum in South America (see, for example, plants (Soltis and Soltis 1987), presumably because Schwartsburd et al. 2014), whereas others treat esculen- spores are smaller and more easily transported in the tum and arachnoideum as subspecies of P. esculentum air than most seeds. An increased dispersal potential (Thomson 2012; Zhou et al.2014), a system we follow can result in colonization of new areas from multiple here. Regardless of rank assignment, evidence for two spore sources, and may involve an increased opportunity main clades of Pteridium includes analyses of plastid DNA for hybridization relative to seed plants. Here, we explore variation (Der et al. 2009; Zhou et al.2014). Further, several this possibility as we assess the origins and diversity of the hybrids and allotetraploids have been examined (Thomson cosmopolitan fern genus Pteridium on the Galapagos and Alonso-Amelot 2002; Zhou et al. 2014). Der et al.(2009) Islands. noted that development of nuclear genomic markers The Galapagos Islands are a group of 14 main islands would be critical for establishing the origins of hybrid taxa and 100 rocks or islets, 1000 km west of mainland and for other systematic studies of Pteridium. Ecuador (Snell et al. 1996). The islands vary in age ranging South America is home to two main Pteridium taxa: dip- from 0.7 to 4.2 million years since emergence above loid P. esculentum subsp. arachnoideum and allotetraploid sea level (White et al. 1993). However, additional evi- P. caudatum, the latter a hybrid between P. esculentum dence points to a much older archipelago existing at from South America and P. aquilinum from North America the same spot prior to the current emergence (Christie (Thomson and Alonso-Amelot 2002). Tetraploidy was et al.1992). Rassmann (1997) cited this idea to explain inferred on the basis of Feulgen cytometry (Tan and why estimates of some lineage ages are more than Thomson 1990) and spore size and guard cell length 5 million years old. The relative isolation of the islands (Thomson and Alonso-Amelot 2002). The hybrid origin of from the nearest mainland coasts (Ecuador and Costa P. caudatum is further supported by the additive pattern Rica) has resulted in a high level of endemism. There of DNA markers from P. aquilinum and P. esculentum are estimated to be 236 endemic plant species on the (Thomson 2000; Thomson and Alonso-Amelot 2002). Add- islands (Tye and Francisco-Ortega 2011). Origins of the itional characters that can be used to distinguish Galapagos flora are now thought to be quite diverse P. caudatum from P. esculentum subsp. arachnoideum in and include northern and southern Andes and other South America include the presence of gnarled trichomes parts of South America, as well as Central America and between veins abaxially (Thomson and Martin 1996) the Caribbean (Tye and Francisco-Ortega 2011). The and free laminar lobes on P. esculentum. An additional wide range of elevations and rainfall patterns results in taxon was recently described from north eastern Brazil a diversity of ecological habitats (Itow 2003). (Schwartsburd et al.2014). Pteridium is a worldwide genus that has been treated Most chromosome counts of Pteridium show 2n ¼ 104 from as few as one species to .20. There are several (Page 1976; Sheffield et al. 1989; Thomson 2000; Tindale taxonomic challenges in the genus, one of which is the and Roy 2002; Bainard et al. 2011), with other comple- high level of variability and phenotypic plasticity for ments, such as triploidy (Sheffield et al. 1993), assumed 2 AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 Wolf et al. — Origins of Galapagos Pteridium to be rare. One count of 2n ¼ 52 from Spain (Lo¨ve and (2) To determine how many Pteridium taxa are on the Kjellqvist 1972) has not been corroborated despite Galapagos Islands. resamplingfromthesamearea(Sheffield et al. 1989). (3) To examine whether different Pteridium taxa occupy Jarrett et al. (1968) reported the first observation of cyto- different islands, or elevations on the Galapagos logical variation in the genus, with a count of 2n ¼ 208 Islands. (tetraploid) for one sporophyte of Pteridium from the Gal- (4) To examine the possible mainland origins of Galapa- apagos Islands. This report has been the motivation for gos Pteridium. previous as well as the current focus on Pteridium from these islands. Klekowski (1973) used gametophytes grown from spores collected from the islands to examine Methods the ability to self-fertilize and cross with Pteridium from We sampled 17 Pteridium from three of the Galapagos other sources.