2. BROWN TROUT POPULATION GENETIC STRUCTURE

2.1 TAXONOMIC CONFUSION MUST NOT IMPEDE CONSERVATION
2.2 DIVERSITY OF BROWN TROUT IN THE MEDITERRANEAN-ADRIATIC REGION
2.3 DIVERSITY OF BROWN TROUT IN THE BLACK, CASPIAN AND ARAL SEA BASINS
2.4 DIVERSITY OF BROWN TROUT IN THE ATLANTIC REGION
2.5 GENETICALLY DISTINCT SYMPATRIC POPULATIONS
2.6 TEMPORAL HETEROGENEITY

The genetic diversity of the brown trout is distributed at several hierarchical levels. A schematic illustration of this hierarchy is shown in Figure 2.1. It should be stressed that at present, the existence of an hierarchical population genetic structure has been confirmed, but the number and properties of the "levels" within the hierarchy, the number and properties of groupings within different levels, as well as the amount of interaction between groupings and "lineages" largely remains unresolved.

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Fig. 2.1 Very schematic illustration of the hierarchical genetic substructuring within the brown trout species. It is presently clear that a hierarchical structure exists and that it probably looks something like this, but it is unclear (1) how many levels there are, (2) how many groupings within levels there are and (3) the degree of interaction between grouping within and between levels.

 

At a large geographical scale, a number of highly divergent evolutionary lineages have been proposed for the southern and eastern range of the species based on analyses of mitochondrial and nuclear DNA (e.g., Bernatchez et al 1992; Giuffra et al. 1994, 1996; Bernatchez and Osinov 1995; Garcia-Marin and Pla 1996; Largiader and Scholl 1996; Antunes et al. 1999). In the northern range, that has been strongly affected by Pleistocene glaciations, one evolutionary "lineage", often referred to as the "Atlantic race", appears to be predominant (Bernatchez et al. 1992). However, several studies indicate that even here the situation is more complex, as postglacial recolonizations from more than one glacial refuge may have taken place, although it is currently unclear how many recolonization "lineages" can be identified (Ferguson & Fleming 1983; Hamilton et al. 1989; Hynes et al. 1996; García-Marín et al. 1999). The current pattern regarding the distribution of five major evolutionary lineages over the Eurasian range was proposed by Bernatchez (1995) on the basis of mitochondrial DNA analyses, and is illustrated in Figure 2.

At a more local scale, medium to strong genetic differentiation has been observed between brown trout populations in many European countries representing different basins, drainages, river systems and spawning sites (e.g., Ryman et al. 1979; Ryman 1983; Crozier & Ferguson 1986; Ferguson & Taggart 1991; Apostolidis et al. 1997; Hansen & Mensberg 1998; Estoup et al. 1998). This differentiation is due partly to the strong homing instinct of brown trout, resulting in limited gene flow among populations. Gene flow among populations may also be restricted due to impassable geographic barriers that promote genetic differentiation. In addition, different "evolutionary lineages" can be found in a mosaic pattern of distribution at a very fine geographic scale presumably due to complex colonisation histories.

In general, little or no correlation has been observed between genetic and geographical distances between landlocked populations. However, this is not necessarily the case for sea-run brown trout where populations may be connected by gene flow (Moran et al. 1995; Hansen & Mensberg 1998; Bouza et al. 1999). It must be stressed that very little is still known about the genetic population structure of "sea trout" and of the relationship between anadromous and resident populations, though most published data suggest that coexisting resident and anadromous trout interbreed and are part of the same population (Campbell 1977; Jonsson 1985; Hindar et al. 1991a; Cross et al. 1992).

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2.1 TAXONOMIC CONFUSION MUST NOT IMPEDE CONSERVATION

There is considerable confusion regarding the taxonomy of the brown trout (cf. Elliott 1994; Kottelat 1997). This confusion stems from an ongoing discussion on how to classify the various morphologically and/or genetically distinct groupings that have been identified. Some suggest that these groupings should receive species status, and up to 57 species names for various forms of brown trout have been proposed since the beginning of the modern nomenclature system in the middle of the 18th century. Some of these classifications have been based on minor morphological and/or life history forms, probably reflecting mainly environmental and phenotypic plasticity (Bernatchez et al. 1992). In brown trout, morphology or life history appears not to be sufficient for delineation of taxonomic units with evolutionary significance and can be misleading. For example, existing data indicate that populations classified as subspecies in terms of life history forms, i.e., S. t. trutta (anadromous form), S. t. lacustris (lake dwelling form), and S. t. fario (stream resident form), do not necessarily represent monophyletic groups (Ryman 1983; Hindar et al. 1991a; Cross et al. 1992).

phylogeographic lineages
Figure 2. Geographical distribution of the five major evolutionary lineages of brown trout as proposed by Bernatchez (1995). Please note that the figure is an updated version of the corresponding figure in Bernatchez (1995) and it contains unpublished data. The figure is provided with kind permission of Dr. Bernatchez (Dept. of Biology, University of Laval, Sainte-Foy, Quebec, Canada and will appear in one of his forthcoming publications. It must not be copied or reproduced.

Clearly, classification of population genetic groupings should be based on genetic information. However, even with data indicating a genetically distinct unit, it is unclear what this unit should be called; a species, a subspecies, or a genetically distinct population within a species. In the sections describing the genetic diversity in the three major European regions (2.2-2.4) the classification used is that preferred by the various TROUTCONCERT research members of that particular region. Thus, the use of, for instance, "Salmo marmoratus" does not imply that all of the authors of this report prefer that designation before "Salmo trutta marmoratus".

In the section on the current threat status of the brown trout (4.1) we use the nomenclature of the publications cited. The apparent taxonomic discrepancies between countries reflect the fact that there is considerable taxonomic disagreement (e.g., what species concept should be applied) in contemporary literature (Berg 1948; Lelek 1987; Kottelat 1997). As an illustration of these opposing views, Lelek (1987) considers brown trout a single species and also lists a few subspecies names, whereas the most recent checklist by Kottelat (1997) that also takes genetic data into account, proposes more than 20 different species and indicates that this listing is probably incomplete.

The unclear taxonomy described above is not unique to the brown trout; similar discussions exist concerning other species as well (e.g., cutthroat trout; Allendorf & Leary 1988; whitefish; Bernatchez 1995). It is important to stress, however, that the taxonomic discussions do not affect measures necessary for conservation and management. Effective conservation of the brown trout must be based on the genetic differences between populations regardless of whether we call these populations species, subspecies or local populations.

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2.2 DIVERSITY OF BROWN TROUT IN THE MEDITERRANEAN-ADRIATIC REGION

The Mediterranean-Adriatic Province is the region in Europe where the Salmo trutta-complex exhibits the highest phenotypic diversity (Behnke 1968). Several morphs of brown trout with variable taxonomic status depending on the authors, have been recognized in this area, most of them in the Balkanic regions and Turkey (S. trutta macrostigma, S. trutta dentex, S trutta peristericus, S. marmoratus, S. carpio, S. obtusirostris, etc.). Lists of these putative species or subspecies can be found in Behnke (1965, 1968), Banarescu et al. (1971), Economidis & Banarescu (1991), Kottelat (1997) and Dorofeeva (1998).

Studies based on variation of nuclear and mitochondrial DNA have confirmed high genetic diversity among brown trout populations in the Mediterranean-Adriatic region. However, only two different entities have presently been clearly distinguished based on genetic data: S. marmoratus and the Mediterranean populations of S. trutta. Most of the earlier taxonomic classifications that were based on phenotypic variation and which resulted in complex biogeographic structuring of, for instance, the populations of the Balkan Peninsula, have not been confirmed by the data generated using recent molecular techniques (Karakousis & Triantaphyllidis 1990, Apostolidis et al. 1997).

S. marmoratus: The marble trout shows strong morphological and ecological characteristics which easily distinguishes it from other Mediterranean brown trout populations (Sommani 1961; Behnke 1968). The marble trout also exhibits substantial genetic divergence from other identified Mediterranean populations as well as from the "lineages" of the Danubian and Atlantic regions (Bernatchez et al 1992, Giuffra et al. 1994, 1996). Genetic distance estimates based on allozyme variation and nucleotide divergence of mtDNA suggest that S. marmoratus differentiated from the other "lineages" 1-3 million years ago. The distribution of the marble trout is restricted to basins of the upper Adriatic sea, and there are no indications of pronounced population substructuring within that "lineage".

In some tributaries of the Pô river, the marble trout is found in zones of narrow overlap (i.e., parapatry) with native populations of S. trutta (Giuffra et al. 1996). Some authors suggest that this situation prevailed before the introduction of exotic S. trutta which resulted in hybridization between the two forms. If the marble trout really did coexist with the native S. trutta, this would support the contention that it is a "true species" (Sommani 1961; Behnke 1968), but no clear documentation of this situation is available. Presently, this taxon is threatened by industrial and agricultural pollution, and it is very difficult to find populations which are not heavily introgressed by Atlantic stocks. The risk of extinction and complete introgression is high. Owing to its restricted distribution and the probability that only a few small uncontaminated populations exist, a conservation program is urgently needed for this unique morph.

Mediterranean S. trutta: Among the remaining populations of Salmo trutta distributed around the Mediterranean area no apparent large scale population genetic structure can be detected using mtDNA and protein electrophoresis. These populations harbour two substantially differentiated mtDNA haplotypes (Bernatchez et al. 1992; Bernatchez 1995). The occurrence of these two differentiated haplotypes suggests that a minimum of two distinct groups existed in the past. The two mtDNA lineages are now scattered across the region in a rather unpredictable pattern and can be found within the same population (Giuffra et al 1994). However, nuclear markers indicate a highly complex population structuring. In a small geographic area populations exhibiting fixed differences at one or more loci were found, in some cases these genetic dissimilarities were associated with ecological and phenotypic differences (Krieg & Guyomard 1985; Apostolidis et al. 1996a; Giuffra et al. 1996).

A particularly interesting morph is the one endemic to the Garda Lake in the Pô basin: S. carpio. It has been identified as a true species because it exhibits very specific ecological and reproductive traits (exclusively lake dwelling, two reproductive periods per year, and deep-water spawning) which differentiate it from a sympatric form of brown trout, identified as a population of S. trutta lacustris (Behnke 1972). Recent molecular studies (Giuffra et al 1994) suggest that S. carpio originates from a rather recent hybridization event between S. trutta and S. marmoratus, followed by intensive genetic drift. However, its species status remains unclear since the sympatric populations of S. trutta lacustris form is now extinct. S. carpio does not show any evidence of genetic introgression with introduced Atlantic stocks, but is threatened by pollution and overfishing. The risk of extinction is very high. Although its species status is not established and its origin could be quite recent, this form presents pronounced genetic and phenotypic distinctiveness within the microgeographic context of the Pô valley, and thus deserves urgent conservation actions.

The taxonomic status of many populations in the Balkan countries and Turkey remains to be confirmed using genetic techniques. For instance, it is presently unclear whether some of the morphs identified in those areas (i.e., S. trutta macrostigma, S. obstusirostris) are really genetically distinct. The degree of introgression of alleles from Atlantic populations currently used in enhancement programs in the Balkan countries and Turkey is also unknown for most of the populations.

The Mediterranean region is probably the region where additional macrogeographic studies of genetic and phenotypic variability patterns are most urgently needed. It is also important to clarify the current status of the original diversification of brown trout in this region. Ongoing stocking activities with releases of large quantities of exotic brown trout is thought to constitute a severe threat to the local populations, but data is largely lacking.

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2.3 DIVERSITY OF BROWN TROUT IN THE BLACK, CASPIAN AND ARAL SEA BASINS

Compared to other parts of the native range of brown trout, very few populations in the eastern range (which represents over 50% of the total) have been genetically studied (Bernatchez et al. 1992, Bernatchez & Osinov 1995, Riffel et al. 1995, Largiadèr & Scholl 1995, Osinov & Bernatchez 1996). The area within the eastern range from which samples have been analysed encompasses the Black, Caspian and Aral Sea basins. The scarcity of available genetic data from these three basins is well illustrated by the fact that the most conclusive results summarised here are based only on ten populations from within the limits of the former Soviet Union (Bernatchez & Osinov 1995, Osinov & Bernatchez 1996). Within this region, two of the five major phylogeographic groupings, as defined by mitochondrial DNA genotypes, the "Danubian" grouping and the "Atlantic" grouping were detected (Bernatchez et al. 1992, Bernatchez & Osinov 1995, Osinov & Bernatchez 1996). Most populations studied possessed exclusively "Danubian" haplotypes, whereas Atlantic haplotypes were only found in a few individuals from the headwaters of the Danubian drainages (Bernatchez et al. 1992) and in one population from a tributary of the Upper Volga (Caspian Sea basin; Osinov & Bernatchez 1996). In both cases, it was not possible to infer whether these occurrences of the Atlantic haplotypes have resulted from natural colonisations or of artificial introductions. The same applies for the two occurrences of "Danubian" haplotypes that so far have been detected outside of the Black, Caspian and Aral Sea basins in two populations from Mediterranean drainages, i.e., in a Greek population (Apostolidis et al. 1997), and in a population in former Yugoslavia (Bernatchez et al. 1992).

Congruence between mitochondrial and allozyme variation was observed when comparing populations of the "Atlantic" and "Danubian" groupings (Bernatchez & Osinov 1995, Osinov & Bernatchez 1996). In these studies, two allozyme loci LDH-C1* (=LDH-5) and MEP-1* were found to be the most discriminatory nuclear markers with respect to the two phylogeographic groupings. The geographic variation at these two loci also suggests that secondary contact (natural and artificial) between the "Atlantic" and "Danubian" groupings has been common in the headwaters of the Danubian and northern Caspian drainages (Bernatchez & Osinov 1995, Riffel et al. 1995, Largiadèr & Scholl 1995, Osinov & Bernatchez 1996). The allozyme data further indicate that these contacts were in some cases followed by introgressive hybridisation. However, the level of mixing between the two groupings appears to be very limited, when considering the total range of the Danubian grouping. Further studies, using both nuclear and mitochondrial markers, are urgently needed for a better assessment of the natural or artificial origin of presumed "Atlantic" genes in these particular areas. Such studies are a prerequisite for a sustainable management of the natural genetic resources of brown trout of several European countries (e.g. Austria, Germany, and Switzerland).

The genetic differentiation at the nuclear level between "Danubian" trout and the major groupings occurring in the Mediterranean-Adriatic region has not yet been clearly demonstrated. This is due to a lack of studies that assess genetic differentiation at nuclear loci between Mediterranean populations and populations from the "Danubian" grouping using the same techniques. As is the case for allozymes, for example, electrophoretic techniques and studied loci differ considerably between laboratories, and hence comparisons between results of different studies can be misleading. In this context, it is noteworthy that one study from Turkey found fixed differences at three allozyme loci between two populations of the Black and Mediterranean Sea basins, respectively (Togan et al. 1995). However, so far no mtDNA data has been published for these two populations and it would be too speculative to assume that these differences are representative for the nuclear differentiation between brown trout of the "Danubian" and "Mediterranean" groupings.

On the basis of morphological and ecological variation, populations of the Black, Caspian and Aral Sea have been classified into distinct taxa (Berg 1948), i.e. populations from the Black Sea basin are recognised as S. t. labrax, those from the Caspian Sea basin as S. t. caspius, and those from the Aral Sea basin as S. t. oxianus. In addition, distinct ecophenotypic forms from Lake Sevan (Caspian Sea basin) are recognised as a separate species (S. ischchan). In the studies of Bernatchez & Osinov (1995) and Osinov & Bernatchez (1996), the combined results of allozyme and mitochondrial markers provided weak support for this taxonomic distinction (cf. Fig.2 of Bernatchez & Osinov 1995). For example, it could be clearly demonstrated that S. ischchan represents a morphologically and ecologically unique trout form that evolved recently and belongs to the same evolutionary lineage as all other trout from the Caspian, Black and Aral Sea basins. This trout form is therefore not a species derived from a primitive ancestor of all brown trout populations as has been hypothesised by Behnke (1986).

In the context of conservation and management, the most relevant finding of the aforementioned studies is the high level of population genetic differentiation that was found within the "Danubian" grouping. All populations from the Black, Caspian and Aral Sea possessed private alleles or mtDNA genotypes and were genetically distinct. Therefore, as was stated by the authors, they represent unique gene pools that warrant individual recognition for conservation and management (Bernatchez & Osinov 1995, Osinov & Bernatchez 1996). Finally, if taking into account that the findings are based on a very small number of populations of the "Danubian lineage" relative to its enormous geographic range, it appears likely that a substantial part of the existing genetic variability within this major evolutionary lineage still remains undetected. Thus, additional genetic studies for a firmer assessment of genetic population structure of brown trout within the eastern basins are urgently needed.

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2.4 DIVERSITY OF BROWN TROUT IN THE ATLANTIC REGION

The Atlantic phylogeographic group, as defined by mitochondrial DNA genotypes (Bernatchez et al. 1992), is found throughout the Atlantic river systems from Iceland and Norway in the north to Iberia and the Atlas mountains of Morocco and also in Baltic and White Sea drainages. However, significant differences in nuclear and mitochondrial DNA markers distinguish Atlantic Iberian populations from the more northern Atlantic populations (Moran et al. 1995; Antunes et al. 1999; Bouza et al. 1999; García-Marín et al. 1999; Weiss et al. 2000). The northern part of the Atlantic region was ice covered during the last glaciation and thus many populations have existed only since postglacial times, i.e. during the past 10,000 to 18,000 years. During the last glaciation the main distribution of the Atlantic lineage would have been in France, Iberia and North Africa. However, in addition to the brown trout populations being present in these unglaciated parts of the Atlantic region, one or more glacial refugia probably existed at the margins of the ice sheets. The ice cover was not continuous for the glacial period but there were major advances and retreats of glaciers during this time and associated with these were changes in sea level. These could have allowed periods of allopatry followed by secondary contact.

Although the extent of overall genetic differentiation resulting from a few thousand years of separation would be small, rapid evolution of ecological and other life history specializations could have occured (Behnke 1972). The natal homing behaviour of brown trout means that differences in life history characteristics such as time and place of spawning, even though these may only involve a few genes, can produce reproductive isolation. Genetic differentiation is reinforced and extended by natural selection when the populations come into secondary contact. Current brown trout populations in Northwestern Europe have thus arisen by postglacial colonization from one or more "Atlantic" glacial refugia. It is also possible that colonization occurred from the Southeastern part of the range through late glacial river exchange between the Volga and the Baltic rivers. Thus, in parts of the range there has possibly been some secondary contact and introgression with the Danubian lineage (Osinov & Bernatchez 1996).

On the basis of discontinuities in LDH-C1*(=LDH-5*)100 and *90 allele frequencies, Ferguson and Fleming (1983) proposed that Britain and Ireland had been colonised in the postglacial period by two "races" of brown trout. The first colonist was referred to as the "ancestral race" as it is characterised by the LDH-C1*100 allele that, on the basis of comparison with other salmonid species, is the ancestral allele at this locus. The second race was called the "modern race" and was characterised by the more recent LDH-C1*90 allele that is unique to brown trout. This dual colonization hypothesis was extended by Hamilton et al. (1989) to the rest of NW Europe on the basis of additional analyses. The phylogeny of mtDNA haplotypes and the pattern of haplotype distribution suggested that the post-glacial colonization of NW Europe was more complex than the dual colonization previously proposed (Hynes et al. 1996).

On the basis of genetic variation at LDH-C1* and CK-A1*, García-Marín et al. (1999) proposed that northwestern Europe was colonised by three lineages characterised as follows:

Lineage I: LDH-C1* 90 CK-A1*100;

Lineage II: LDH-C1* 100 CK-A1*115;

Lineage III: LDH-C1* 100 CK-A1*100.

García-Marín et al. (1999) proposed that colonization occurred from (i) a northern and eastern radiation from a refuge centred near the English Channel, (ii) a northern expansion from a refuge in Atlantic drainages of Iberia and southern France, and (iii) a north-western migration from an eastern Mediterranean-Caspian refuge. They suggest that most current populations in the formerly glaciated area are introgressed combinations of these lineages. In a recent study, however, this hypothesis is re-evaluated, and it's suggested that gene flow from refugia in central (e.g., France and Germany) and eastern continental Europe alone can explain the current geographic distribution of mtDNA haplotypes and putative diagnostic allozyme alleles throughout previously glaciated regions of northern Europe (Weiss et al. 2000).

Irrespective of the number and exact pattern of postglacial colonization it is clear that more than one postglacial colonization took place. Current genetic diversity in northwestern Europe is thus the result of independent postglacial colonization by genetically distinct brown trout "lineages" together with genetic differentiation that has occurred in isolation during postglacial times. In practice, however, it is difficult with currently available phylogeographic information to differentiate between these two aspects. Introgression between "forms" has probably occurred (Osinov & Bernatchez 1996; Garcia-Marin et al. 1999a) and possibly also sympatric/micro-allopatric speciation.

Many populations of brown trout are unique in one or more aspects. Often populations are genetically unique as shown by protein or DNA studies. This is particularly so in the unglaciated southwestern part of the Atlantic range where populations have persisted for much longer than in the northwestern part. Specific alleles often occur in only one or a few populations with up to 66% of the total genetic variation in northwestern Europe being distributed among populations (Ferguson 1989).

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2.5 GENETICALLY DISTINCT SYMPATRIC POPULATIONS

An interesting and important phenomenon that has been observed is the existence of reproductively isolated and genetically differentiated populations that occur sympatrically on a small geographic scale. The occurrence of such sympatric populations was first reported in Lake Bunnersjöarna in Sweden (Allendorf et al. 1976, Ryman et al. 1979). Following a routine genetic investigation, it was discovered that this very small mountain lake was actually inhabited by two co-existing, genetically distinct, brown trout populations. The reproductive isolation appeared complete due to the apparent fixation for different alleles at a locus coding for lactate dehydrogenase. Further, because of this alternate fixation it could be easily determined which population each fish belonged to, and it could thus be shown that the populations were characterized by significantly different growth rates (Ryman et al. 1979).

Subsequently, a similar situation of sympatry has been reported to occur in Lough Melvin in Ireland (Ferguson & Mason 1981; Ferguson & Taggart 1991). The brown trout of Lough Melvin have been subjected to very detailed studies. L. Melvin is a lake of some 21 km2 situated in northwestern Ireland. Three types of brown trout, known locally as gillaroo, sonaghen and ferox, have been described from the lake. They are distinct morphologically (Cawdery & Ferguson 1988) and have different feeding preferences (Ferguson 1986). Allozyme studies (Ferguson & Mason 1981; Ferguson & Taggart 1991) showed major differences in the occurrence and frequency of alleles indicating a high degree of reproductive isolation between the three types. Examination of mitochondrial DNA restriction fragment length polymorphisms (McVeigh et al. 1995; Hynes et al. 1996), multi-locus DNA fingerprints (Prodöhl et al. 1992), single-locus minisatellite variation and microsatellite variation (A. Duguid & P. Prodöhl, pers. comm.) further confirm the genetic discreetness of the three types. This reproductive integrity of the Melvin trout types is maintained by geographical separation of the spawning sites through natal homing (Ferguson & Taggart 1991). The gillaroo spawn in the only outflowing river of the lake, whereas sonaghen spawn in the inflowing rivers. The ferox spawn in the lower deeper section of one of the inflowing rivers, which is also used further upstream by sonaghen. Another example of genetically and morphologically distinct sympatric populations in Ireland involves brown trout known locally as dollaghan and salmon trout in the L. Neagh system (Crozier & Ferguson 1986).

In a number of lakes in Britain and Ireland, as well as "normal" brown trout, long-lived piscivorous trout, often referred to as ferox, are found and these in some cases can exceed 10kg in mass. In at least two lakes in Britain and Ireland ferox appear to be reproductively isolated from sympatric trout. In a lake in the Hardangervidda area of Norway trout with a variant allele, which result in a fine-spotted pattern, coexist with other brown trout (Skaala & Jorstad 1987). This spotting pattern is controlled by a single locus with two codominant alleles (Skaala & Jorstad 1987). A morph with a marmorated coloration exists alongside trout of "normal" coloration in the River Otra in Norway (Skaala & Solberg 1997).

Finally, it should be stressed that it is still unclear to what extent sympatric populations represents a common phenomenon in the brown trout. The presence of different morphotypes within a single lake does not in itself provide enough evidence of multiple populations until this has been confirmed by genetic data. Further, for statistical reasons, it may be difficult to detect the existence of multiple populations when they are not distinguished by fixed (or very large) allele frequency differences, or when different morphotypes (potentially representing different populations) are absent which could serve as a natural starting point for making allele frequency comparisons. For example, Jorde & Ryman (1996) describe a situation where it took several years of sampling (i.e. several hundreds of fish) until it became evident that two of their lakes actually harboured multiple genetically distinct and co-existing populations. Since most population genetic surveys are typically based on relatively limited sample sizes (say, 50-100 individuals per population), the existence of sympatric brown trout populations on a small geographic scale may be more common than is presently recognized.

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2.6 TEMPORAL HETEROGENEITY

A large amount of data has been generated on the frequency and geographical distribution of different alleles at genetic marker loci in natural brown trout populations in Europe. However, information regarding the temporal dynamics of those marker alleles is still relatively sparse despite the fact that such information is essential for conservation and sustainable management. Typically, population genetic investigations include sampling at one particular occasion only, i.e., they lack temporal replication. This situation is by no means unique to brown trout, but reflects a general phenomenon.

Several workers have compared gene frequencies from natural populations of several species sampled at 2-3 occasions (e.g., Krimbas & Tsakas 1971; Begon et al. 1980; Ryman 1983; Burns & Zink 1990; Waples & Teel 1990; Hedgecock et al. 1992; Ruzzante et al. 1997), and a few such studies have also been conducted on brown trout (Ryman & Ståhl 1980; Hansen & Loeschcke 1996). For most species, however, few studies exist that systematically follow genetic changes within a population over extended periods of time (e.g., DeSalle et al. 1987; Turner et al. 1999). This fairly limited knowledge of the extent of temporal variation of genetic markers influences the interpretation of observed spatial patterns; it is largely unclear if they are stable over time (Ryman 1983; Burns & Zink 1990).

In a couple of recent studies the genetic composition of populations over several years has been reported for a few natural brown trout populations in Sweden (Jorde & Ryman 1995, 1996; Laikre et al. 1998). In those studies material was collected over more than ten years, and the main results may be summarized as follows: 1. The existence of genetic change over time has been established. 2. These changes may be relatively large even between consecutive cohorts. 3. The demography of species with overlapping generations (which applies to the brown trout) affects the genetic dynamics of the population - evaluation of genetic data based on discrete generation theory may therefore obscure the interpretations. 4. The amount of allele frequency change is larger in populations with over-lapping generations as compared to populations with discrete generations. 5. Cohorts (age classes) born approximately 1 generation apart are genetically more similar than cohorts born fewer or more years apart. 6. Temporal genetic data combined with demographic data may be used to estimate the genetically effective population size (Ne; section 1.3). 7. Estimates of Ne indicate that the effective size of populations in lakes of similar size may vary considerably and may be relatively small. The female effective size in one population was estimated to approximately half that of the total effective size (Jorde & Ryman 1996; Laikre et al. 1998; Palm et al., in prep).

Some other recent studies on Atlantic salmon (Salmo salar) compared microsatellite markers from old scale samples with contemporary data from the same populations. Nielsen et al. (1997, 1999a,b) studied Atlantic salmon populations from Denmark over a period from 1913 to the present and found that the genetic structure of populations was remarkably stable over time. A qualitatively similar result was obtained by Tessier & Bernatchez (1999) in a study of landlocked salmon covering a time-span of app. 30 years.

The limited data that do exist on temporal genetic variability for salmonid populations indicate that observed patterns of spatial differentiation are releatively stable over time (Ryman 1997a). For instance, in the study mentioned above on natural brown trout populations in Sweden the spatial component of genetic diversity (i.e. between lakes) was estimated to 4.5% whereas the temporal component (i.e. between years within lakes) was estimated to 0.5% (Jorde & Ryman 1996; Ryman 1997a). Therefore, there is no reason to "panic" and automatically conclude that the information on spatial genetic population structure of brown trout (or other salmonids) generated over the years is "useless". However, it is obvious that extended studies of temporal genetic variability in brown trout populations (as well as populations of other species) are needed to increase the understanding of the genetic dynamics of natural populations. A better understanding for these processes is necessary for adequate management and conservation measures. It is extremely difficult to monitor and evaluate the effects of various activities on the biodiversity at the gene level if the magnitude of the "normal" variation in genetic composition over time is unknown. Studies needed include not only empirical observations, but also theoretical developments. For instance, research focus on genetic models for age-structured populations with overlapping generations is needed to permit interpretation of empirical data, and to better understand the impact on natural populations of various activities (Ryman 1997b).

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3. Threats to brown trout populations