Genetic Structure of Fragmented Populations of a Threatened Endemic Percid of the Rhoˆne River: Zingel Asper

Heredity (2004) 92, 329–334 & 2004 Nature Publishing Group All rights reserved 0018-067X/04 $25.00 www.nature.com/hdy Genetic structure of fragmented populations of a threatened endemic percid of the Rhoˆne river: Zingel asper J Laroche1,2 and JD Durand1,3 1Laboratoire d’Ecologie des Hydrosyste`mes Fluviaux, UMR CNRS 5023, Universite´ Claude Bernard, 43 bd du 11 Novembre 1918, 69622 Villeurbanne cedex, France; 2Laboratoire Ressources Halieutiques – Poissons Marins, Institut Universitaire Europeén de la Mer, Place Nicolas Copernic, 29280, Plouzane´, France; 3IRD/Laboratoire Geńome, Populations, Interactions, UMR CNRS 5000, Universite´ Montpellier II, Station Me´diterraneénne de l’Environnement Littoral 1, quai de la Daurade F-34200 Se`te, France Zingel asper is an endemic percid of the Rhoˆne basin equilibrium between mutation and drift. Thus, this population considered to be critically endangered. This species was shows an apparently better evolutionary potential for long- continuously distributed throughout the Rhoˆne in 1900, but term survival. Since 1930, a marked fragmentation of the today only occupies 17% of its initial area. In the present whole Rhoˆne system has appeared, related to the develop- study, five microsatellite loci were used to assess the level of ment of dams, and we assume that the significant genetic genetic variability within and among populations localized in differentiation detected between the populations could different sub-basins. Contrasting results were obtained for mainly reflect the impact of this fragmentation. The high the three main populations from the Rhoˆne. A reduced allelic turnover of the Z. asper populations, and the major role of diversity was observed for the two populations displaying the dispersal in population persistence (highlighted in a recent lowest patch sizes (length of the river system occupied); of population dynamics study), indeed suggest that the differ- these, a recent genetic bottleneck was detected for the entiation observed could mainly have arisen from habitat population showing a particularly low density. However, the fragmentation in recent history. third population was characterized by a relatively large Heredity (2004) 92, 329–334, advance online publication, 25 spatial extent, high local fish concentrations and an allelic February 2004; doi:10.1038/sj.hdy.6800424 diversity that was twice as high and associated with an Keywords: percid; genetic structure; microsatellites; Zingel Introduction have maintained a high level of genetic diversity (Withler et al, 2000). The same trend was observed for remnant During the last century in Europe, most river systems populations of bull trout in a tributary to lake Pend have shown extensive channel fragmentation, induced Oreille (Idaho), which displayed a high level of allelic by dams and flow regulation. This leads to the diversity and heterozygosity; in this environmental disappearance of habitats and to the reduction of the context, the expected genetic erosion could lag behind possibility of dispersal, and it thus limits the possibilities the demographic data for several generations (Spruell for numerous species to realize their biological cycle. et al, 1999). The time lag could be substantial particularly These alterations to the physical habitat could threaten for relatively long-lived species such as bull trout. In the many plant and animal populations through a possible same river system, another investigation was conducted erosion of their genetic variability by bottlenecks, genetic on the impact of a dam on bull trout (Neraas and Spruell, drift or inbreeding. 2001) which showed: (1) a demographic decline of the However, studies of temporal variability in genetic populations in upstream tributaries following the con- diversity over the last 50 years in Atlantic salmon struction of the dam, and (2) a reduction in the gene flow populations stress that the observed reduced level of through the prevention of migratory fish returning to variability was probably not an effect of human- their natal estuaries to spawn. Thus, the river fragmenta- mediated changes in population size, but instead could tion could lead in the future to the erosion of the genetic be associated with a founder effect during the recoloni- diversity in populations above the dam. zation of Northern Europe after the last glaciation More generally, population genetic theory predicts (Nielsen et al, 1997, 1999). Furthermore, despite succes- that, unless the reduction in effective population size has sive demographic bottlenecks and high exploitation, been very severe, no major changes in genetic variability some populations of sockeye salmon in British Columbia should be detectable (Frankel and Soule´, 1981). As expected, therefore, experimentally bottlenecked populations of mosquitofish reared in mesocosms showed a Correspondence: J Laroche, Current address: Laboratoire Ressources Halieutiques – Poissons Marins, Institut Universitaire Europeén de la significant erosion of their genetic diversity only with Mer, Place Nicolas Copernic, 29280, Plouzane´, France. very reduced effective sizes (Spencer et al, 2000). In a E-mail: [email protected] river system, the fragmentation of habitats cannot reduce Genetic structure of a threatened percid J Laroche and JD Durand 330 significantly the overall genetic diversity in populations maintain all populations of this species, and key of ubiquitous fish species, particularly if their effective populations need to be identified for priority action sizes remain large in the main channel of the river (Ferguson et al, 1995). (Laroche et al, 1999), thus counterbalancing the possible The aim of this investigation was to explore the genetic effects of genetic drift. On the other hand, fish species variability of Z. asper populations over different spatial displaying strong habitat requirements and small popu- scales in the Rhoˆne basin, using selectively neutral lation sizes in first-order rivers, such as Cottus gobio markers (microsatellites). Our main objectives were: (Hanfling and Brandl, 1998), may be suitable models in which to study the impact of fragmentation on genetic diversity. 1. to analyse the genetic diversity within populations Numerous studies in conservation genetics have and consequently to highlight possible genetic erosion focused on ways to preserve the genetic diversity of of the most endangered populations; endangered species (Avise, 1994; Vrijenhoek, 1998) and 2. to investigate genetic differentiation between the maintain local genetic resources. As natural areas different river watersheds, which could be the result remaining become smaller and increasingly fragmented, of a long-term geological history creating founder it is a matter of urgency to understand the evolutionary effects and/or of a more recent evolutionary history dynamics of small populations, in order to preserve them linked to habitat fragmentation (bottlenecks, genetic (Lande, 1988). drift, etc.); The genus Zingel is a percid whose distribution is 3. to set up the first basis of a conservation strategy. restricted to rivers zoogeographically connected with the Danube. Zingel asper, an endemic fish in the Rhoˆne basin, Material and methods is the result of a connection with the Danube system in the Pliocene (Changeux and Pont, 1995). In 1900, Z. asper The Rhoˆne river is the 42nd largest river in the world was distributed continuously throughout the Rhoˆne and (mean annual discharge) and some sectors are heavily main tributaries but today only occupies 17% of this area; perturbed by anthropogenic pressure from 19 hydro- this species is sensitive to overall habitat degradation electric plants (the first of which was erected in 1925), and particularly to the silting up of the bottoms five nuclear plants and from industrial pollution (Bra- (Changeux and Pont, 1995). The fishing pressure on vard et al, 1992). Over the whole Rhoˆne basin, the Z. asper remains very low and this species has not been remnant populations of Z. asper are mainly localized in artificially managed in the Rhoˆne basin. This species is three river watersheds (Labonne, 2002). The different considered to be critically endangered, but is only sampling stations were Droˆme (D1), Beaume (from B1 to marginally protected by a localized Biotope Protection B3), and Durance (DU1, DU2) (Figure 1). A similar Order (Keith, 2000). It will clearly be impossible to fishing effort (from 5 to 7 days, between 1997 and 1999) Beaume B1 (37 p)5 p) B2 (2 Saône Chass B3 (29 p) ezac Ardèche LYON e (15 p) Drôm Durance Rhône Buech Durance ) DU1 (34 p) DU2 (24 p 100 Km Figure 1 Approximate sample sites of Z. asper from the Rhoˆne basin. Numbers between brackets correspond to the number of sampled fish. Heredity Genetic structure of a threatened percid J Laroche and JD Durand 331 was conducted at each watershed; the very low Results density of fish in some rivers sometimes allowed us to catch only a small number of individuals. Allelic diversity, heterozygosity and linkage disequilibrium Fish were caught by scoop nets; a limited fragment The allelic diversity and the observed and expected of caudal fin was sectioned and placed in a tube heterozygosities were estimated for sampled locations with ethanol (90%), then the fish was reintroduced into (Table 1). The mean allelic richness was rather similar for the river. the Droˆme (6) and the Beaume (E8.4) and was DNA was extracted from the fins using the DNAeasy significantly higher for the Durance (E16); this trend Tissue kit (QIAGEN). The final elution

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