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Phylogeography and Conservation Genetics of Endangered European Margaritiferidae (Bivalvia: Unionoidea)

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Phylogeography and Conservation Genetics of Endangered European Margaritiferidae (Bivalvia: Unionoidea) Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2003? 2003 78? Original Article A. MACHORDOM ET AL. MARGARITIFERIDAE CONSERVATION GENETICS Biological Journal of the Linnean Society, 2003, 78, 235–252. With 3 figures Phylogeography and conservation genetics of endangered European Margaritiferidae (Bivalvia: Unionoidea) ANNIE MACHORDOM*, RAFAEL ARAUJO, DIRK ERPENBECK† and MARÍA-ÁNGELES RAMOS Museo Nacional de Ciencias Naturales, José Gutiérrez Abascal 2, 28006 Madrid, Spain. Received 26 April 2002; accepted for publication 29 October 2002 Margaritifera margaritifera and M. auricularia are among the most endangered freshwater mussels in the world, and the only species of the genus found in Europe. Our genetic study explores allozymic variability (27 loci) and dif- ferentiation at the mitochondrial sequence level (partial COI and 16S rRNA gene sequences). The Spanish M. auric- ularia population showed genetic parameters of variation that were of the same order as those of other freshwater molluscs (though at the lower end of the range), probably permitting its potential recovery. The difference between this species and M. margaritifera was clearly established (ten diagnostic allozymic loci, Nei = 0.462, and mean nucle- otide divergence around 9.4%). The M. margaritifera populations analysed showed a certain degree of population genetic structure (according to allozyme data) that was not, however, related to a geographical cline. Nevertheless, two mitochondrial lineages (albeit very closely related) were identified: a northern lineage extending from Ireland to the Kola Peninsula including the western Atlantic coast, and a second cluster distributed from Ireland to the Iberian Peninsula. The phylogenetic relationships between these two species and other related taxa were established. The putative M. m. durrovensis could be considered an ‘ecophenotype’. Palaeobiogeographical scenarios are presented and indicate unexpected ‘recent’ gene flow between M. margaritifera populations that were theoretically isolated in the early Tertiary. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society 2003, 78, 235– 252. ADDITIONAL KEYWORDS: 16S rRNA – allozymes – COI – freshwater mussels – genetic variation – Margaritifera – mtDNA. INTRODUCTION to endangered populations or species could provide limits for the units to manage, preserving the total The concept of ‘Conservation Genetics’ was developed diversity of the taxon. Thus, certain cryptic species or ‘to contribute to the preservation of the natural diver- local adaptations might come to light, and the subse- sity of species with a view to preserve the evolutionary quent conservation programme would be designed to potential of species by exploring the relationships maintain the variability of the species, essential for between today’s advances in genetics and their poten- their evolution and survival. tial contribution to the quality of wildlife (animal and Though the last decades have seen renewed conser- plant) conservation’ (Schonewald-Cox et al., 1983). vation interests and improved molecular tools, there is Moritz (1994) also indicated that a prerequisite for still a bias towards studies on emblematic vertebrates managing biodiversity is the identification of popula- despite the fact that most biodiversity is provided by tions with independent evolutionary histories. The dif- invertebrate species. ferent genetic or molecular tools that may be applied Freshwater mussels (Unionoidea) are among the most endangered invertebrates in the world. Their decline is the result of ever increasing human activity regarding freshwater habitats, such as the regulation *Corresponding author. E-mail: [email protected] †Current and impoundment of rivers (Vaughn & Taylor, 1999). address: Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, PO Box 94766, 1090 GT Amsterdam, Such is the extent of their loss, that of the 344 union- the Netherlands. oid species in the United States, 35 are extinct, 57 are © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 78, 235–252 235 236 A. MACHORDOM ET AL. endangered, five are threatened and 61 are candidates 1910) is strongly linked to salmonids (Ziuganov et al., (Bogan, 1998). In Europe, the remarkable decline suf- 1994), while the European M. auricularia is thought to fered by freshwater mussel populations has recently be associated with the acipenserids (Altaba, 1990; attracted the attention and concern of national and Araujo & Ramos, 2000b). This relationship with international conservation organizations (Kileen, anadromous fishes can be interpreted as an ancestral Seddon & Holmes, 1998). However, to date, few inves- feature for their transition from the sea to the fresh- tigations have focused on Unionoidea, and the real sit- water habitat aimed at ensuring larval survival. uation is poorly understood and especially alarming Moreover, the unionids in general present a morpho- for the Margaritiferidae family. logical plasticity that sometimes impedes clear taxo- Margaritiferidae species are presumed to be among nomic classification. Thus, effective management the most primitive freshwater mussels (i.e. close to could be hampered by this lack of information, which ancestors from the sea that colonized fresh waters and is practically non-existent at the population level gave rise to all other unionaceans; Davis & Fuller, (King et al., 1999). 1981; Campbell, 2000). With nearly ten species spread Given these premises, the molecular study of avail- throughout the northern hemisphere, Margaritifer- able living European species of Margaritiferidae was idae are among the most threatened Unionoidea and considered to be of major interest for understanding include relatively ‘unknown’ species such as Marga- both the evolution of this mollusc group and its con- ritifera auricularia (Spengler, 1793) in the NW Palae- servation problems. With these objectives in mind, a arctic, and Margaritanopsis laosensis (Lea, 1863) combined approach (allozymic electrophoresis and inhabiting only one known Asian locality. Marga- mitochondrial DNA sequencing) was applied for the ritifera auricularia has recently been the subject of first time to the European species of this group. thorough investigation (Araujo & Ramos, 1998, 2000a, The decline of these bivalves prevented us from 2001; Araujo, Bragado & Ramos, 2000) since the dealing with large numbers of specimens from some ‘rediscovery’ of a population of some 2000 specimens in populations, which were sometimes below the recom- Spain and the collection of live specimens in 1991 from mended figures for population structure analyses. Moroccan rivers (Araujo & Ramos, 2000b). In Europe, Nevertheless, this is currently an insurmountable populations of the widespread Margaritifera marga- problem that should not dissuade us from obtaining as ritifera (Linnaeus, 1758) were reduced by 90% over the much data as possible on these endangered species. course of the last century. This has generated much Thus, the main aims of this paper were: (i) to investi- controversy with respect to the ‘ecophenotype’ (i.e. a gate the evolutionary relationships of the European morphological local adaptation) Margaritifera marga- M. margaritifera populations by testing for genetic dif- ritifera durrovensis (Phillips, 1928) (Chesney, Oliver & ferentiation or structure and (ii) to investigate genetic Davis, 1993), an Irish hard water population inhabit- variability and phylogenetic relationships of the ing a single river, the Nore, and listed as a protected Spanish M. auricularia. subspecies by the International Union for Conserva- tion of Nature (IUCN). MATERIAL AND METHODS The life history of the margaritiferids has been used as a ‘book example’ in biogeographical studies (e.g. the TAXA AND SPECIMENS 1922 classic by Wegener Die Entstehung der Kontinente The samples used were portions of mussel foot. To und Ozeane). Margaritifera margaritifera is considered ensure the survival of most of the organisms analysed, the oldest species of the group, emerging before the when possible, a small piece of foot (<1 cm3) was dis- Atlantic splitting of American from European popula- sected in situ and maintained in liquid nitrogen or tions (i.e. before the early Tertiary) (Bauer, 1997). Nev- absolute ethanol before being transported to the lab- ertheless, numerous conflicting hypotheses have been oratory. The specimens were then returned alive to put forward to explain the origins of this group their original habitat (Fig. 1). Otherwise, specimens (Walker, 1910; Smith, 1976; Taylor, 1988). This contro- were transported to the laboratory alive. versy prompted our attempt to find an explanation for Table 1 shows the 133 specimens included in the both the origin and the previous wide distribution of allozyme study [36 M. auricularia, 87 M. margaritifera, the margaritiferids through a comparison of their and an outgroup of ten Potomida littoralis (Lamarck, genetic diversity. The larvae (glochidia) of all union- 1801)]. As these species are severely endangered, oids are parasitic on the gills and/or fins of suitable some populations were underrepresented. Neverthe- fish hosts. This specificity between glochidia and less, the number of loci analysed (27) could, at least fishes may provide a clue to understanding their dis- partly, make up for the scarce number of specimens tribution (Taylor & Uyeno, 1965; Bauer, 1997). The studied (Nei, 1978). evolution
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