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Species Diversity Versus Phylogenetic Diversity: a Practical Study in the Taxonomically Difficult Genus Dactylorhiza (Orchidaceae)

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Species Diversity Versus Phylogenetic Diversity: a Practical Study in the Taxonomically Difficult Genus Dactylorhiza (Orchidaceae) BIOLOGICAL CONSERVATION 129 (2006) 4– 13 available at www.sciencedirect.com journal homepage: www.elsevier.com/locate/biocon Species diversity versus phylogenetic diversity: A practical study in the taxonomically difficult genus Dactylorhiza (Orchidaceae) Yohan Pillona,b,1, Michael F. Faya, Alexey B. Shipunova, Mark W. Chasea,* aJodrell Laboratory, Royal Botanic Gardens, Kew, Kew Road, Richmond, Surrey TW9 3DS, UK bLaboratoire de Biologie et Physiologie Ve´ge´tales Applique´es (LBPVA), Universite´ de la Nouvelle-Cale´donie, BP 4477, 98847 Noume´a, New Caledonia ARTICLE INFO ABSTRACT Article history: Setting conservation priorities in taxonomically complex groups such as the orchid genus Received 28 December 2004 Dactylorhiza is a difficult task. As an alternative to taxonomic diversity, we used here a Received in revised form molecular phylogenetic analysis and the results of a genetic investigation using plastid 17 May 2005 microsatellites with an extensive geographic sampling to assess in a more objective way Accepted 3 June 2005 the patterns of diversity within this genus. Although western Europe is thought to be the Available online 18 November 2005 main diversity centre for the genus due to the large number of species found there, we found higher phylogenetic and genetic diversity as well as higher endemicity in the Cauca- Keywords: sus and the Mediterranean Basin, two biodiversity hotspots. Species number seems to be Biodiversity hotspots correlated with taxonomic effort, tentatively estimated here by the number of herbaria, Dactylorhiza and is thus biased and not an appropriate measure of diversity. Our results show that phy- Orchids logenetic analyses and genetic data obtained with molecular tools can offer an alternative Phylogenetic diversity measure of biodiversity that is not sensitive to taxonomic inflation. Conservation of allote- Taxonomy traploid taxa is also discussed, and it is recommended that sites in which polyploids are formed should be conserved rather than any specific allotetraploid taxon. Ó 2005 Elsevier Ltd. All rights reserved. 1. Introduction been shown to be monophyletic if the former monotypic genus Coeloglossum Hartman is included in synonymy (Prid- Members of the genus Dactylorhiza Necker ex Nevski (Orchid- geon et al., 1997; Cribb and Chase, 2001). aceae), the spotted and marsh orchids, are terrestrial orchids from the Northern Hemisphere. They occupy a wide range of 1.1. Distribution and diversity open habitats from dune slacks to alpine meadows, including swamps and peat bogs. The subtribe to which they belong, The distribution of Dactylorhiza, including D. viridis Bateman, Orchidinae, is most diverse in Eurasia, encompassing the Pridgeon and Chase formerly Coeloglossum viride Hartman, majority of European orchids. According to Averyanov covers most of Europe, most of temperate Asia, North Africa, (1990), there are 75 species of Dactylorhiza worldwide and 58 Japan, the Aleutian Islands and northern parts of North in Europe, North Africa and the Near East (hereafter termed America (Fig. 1). Averyanov (1990) distinguished three centres Europe and adjacent areas; Delforge, 2001). Dactylorhiza has of diversity: western Europe (including the British Isles, Ger- * Corresponding author: Tel.: +44 2083325364; fax: +44 2083325310. E-mail address: [email protected] (M.W. Chase) 1 Present address: Laboratoire de Botanique, Centre IRD de Noume´a, BP A5, 98848 Noume´a, New Caledonia.. 0006-3207/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2005.06.036 BIOLOGICAL CONSERVATION 129 (2006) 4– 13 5 Fig. 1 – World distribution of the genus Dactylorhiza (shaded areas), including the former genus Coeloglossum, modified from Pridgeon et al. (2001) and Luer (1975). of three broad groups: D. incarnata s.l., D. maculata s.l. and allotetraploids that are hybrids between the first two groups (Hedre´n, 2001). The D. maculata group is itself composed of diploid and tetraploid species, delimitation of which is of- ten difficult. 1.3. Threats and conservation status As with many other terrestrial orchids, populations of Dacty- lorhiza have decreased due to habitat loss. Many wetlands in Europe have been drained, and changing agricultural prac- tices have led to the degradation of their habitats through Fig. 2 – Species diversity of Dactylorhiza across Eurasia, use of fertilizers, early haymaking, etc. More recently, the de- reproduced from Averyanov (1990). Darker areas are said to crease in agricultural pressure has had a counterintuitive ef- contain the greatest number of Dactylorhiza species. fect: abandonment of grassland leads to forest expansion and fewer suitable habitats. However, a few species such as D. fuchsii and D. praetermissa have shown some ability to colo- many and southern Scandinavia), the Carpathian Balkan area nize human disturbed environments, but generally tran- and Asia Minor (Fig. 2). This is in broad agreement with data siently. Another threat to Dactylorhiza is the collection of given in Delforge (2001), according to whom the greatest spe- their tubers to make salep, used as food and medicine. This cies richness is found in northwestern Europe. For instance, is a particularly important threat in the Himalayas (Srivastava nine species are endemic to the British Isles according to Del- and Mainera, 1994), where D. hatagirea or ‘‘panch aunle’’ is forgeÕs classification (2001). Dactylorhiza viridis, the species judged critically endangered (Biodiversity Conservation Prior- with the largest range, is the only one to become widespread itisation Project, 1998) due to over-collection. Thus, several in the New World (Luer, 1975). Dactylorhiza is thus unusual species of Dactylorhiza are declining, and some are already among European orchid genera, most of which show greatest protected at a national scale, e.g., in Belgium, Luxembourg, diversity around the Mediterranean Basin. Nepal, and the UK. Setting conservation priorities in taxonomically complex 1.2. Taxonomic issues in the genus groups is an essential but especially difficult task because these species tend to be over-represented in red lists (Pilgrim Dactylorhiza is universally recognized as a taxonomically et al., 2004). Hybridization has often made decision-making challenging genus (Bourne´rias et al., 1998; Pedersen, 1998; difficult in conservation (Rieseberg and Gerber, 1995; Wayne Delforge, 2001; Hedre´n, 2001), as demonstrated by the differ- and Gittleman, 1995), and neglecting taxonomy can have ences in the number of species recognized by different disastrous effects on the conservation of a particular group, authors (reviewed by Pedersen, 1998), from 12 to 75 world- e.g., the tuatara (Daugherty et al., 1990). In the case of Dacty- wide and from 6 to 58 in Europe. There can even be impor- lorhiza such problems have already been encountered; D. lap- tant differences between treatments by the same author. ponica, formerly classed as a threatened species in Britain, Delforge (1995) for example, added nine species between proved to be indistinguishable from D. traunsteineri (a more his monographs of 1995 and 2001. This taxonomic complex- frequent species) after morphological and molecular investi- ity can largely be explained by the frequency of hybridiza- gations (Bateman, 2001; Pillon et al., in press; Bateman, sub- tion, and nearly all hybrid combinations are possible mitted). Thus, caution should be applied before setting taxon (Averyanov, 1990). Most Dactylorhiza species belong to the priorities, and molecular systematics can aid in this task D. incarnata/maculata polyploid complex, which is composed (Soltis and Gitzendanner, 1999). 6 BIOLOGICAL CONSERVATION 129 (2006) 4– 13 1.4. Alternative measures of biodiversity entry order with tree bisection reconnection (TBR) swapping and no tree limit per replicate. Clade support was assessed The aim of conservation biology is to preserve biodiversity: with 1000 bootstrap replicates. DELTRAN optimization was ‘‘the variety of life in all its manifestation’’ (Gaston and Spicer, used for branch length measures because of known problems 1998). Species richness is by far the most commonly used with ACCTRAN in PAUP*4.01b10. No particular short or long measure of biodiversity, but many others also exist (Purvis branches that could result in substantial under- or over- and Hector, 2000). Some approaches have proposed giving dif- weighting of a lineage were observed. All DNA sequences ferent weight to species because some species are more dis- have been submitted to GenBank and have Accession Nos. tinctive and genetically isolated than others, e.g., one DQ022863 to DQ022926 (DQ022863 to DQ022894 for ITS and species of apomictic Taraxacum may not deserve the same DQ022895 to DQ022926 for the rpl16 intron). attention as the single species of Welwitschia (Vane-Wright Using the distributions given in Delforge (2001), we listed et al., 1991). Because Dactylorhiza species are unequally dis- for each country or region the species occurring there and tant from each other, some being barely distinguishable mapped them on the tree. Phylogenetic diversity was mea- genetically and others relatively isolated, we thought that sured for each region as the sum of branch lengths (i.e., num- evolutionary history or phylogenetic diversity could be a bet- ber of nucleotide substitutions) between the first node within ter measure of the diversity of a region (Faith, 1992; Mace Dactylorhiza and the tips of the tree whenever the correspond- et al., 2003) than purely taxonomic diversity. A hierarchical
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