Fine-scale population structure in Atlantic salmon from Maine's Penobscot River drainage

We report a survey of microsatellite DNAvariation in Atlantic salmon from theunimpounded lower reaches of Maine's PenobscotRiver. Our analysis indicates that Atlanticsalmon in the Penobscot River are distinct fromother populations that have little or nohistory of human-mediated repopulation,including two of its tributaries, Cove Brookand Kenduskeag Stream, another Maine river, theDucktrap, and Canada's Miramichi and Ganderrivers. Significant heterogeneity was detectedin allele frequency among all threesubpopulations sampled in the Penobscotdrainage. The high resolution of the 12-locussuite was quantified using maximum likelihoodassignment tests, which correctly identifiedthe source of 90.4–96.1% of individuals fromwithin the Penobscot drainage. Currentpopulations are clearly isolated from eachother, however we are unable to determine fromthe present data whether the populations inCove Brook and Kenduskeag Stream are recentlydiverged from populations stocked into thePenobscot River over the last century, or areaboriginal in origin. The degree of populationstructure identified in the Penobscot drainageis noteworthy in light of its lengthy historyof systematic restocking, the geographicproximity of the subpopulations, and the extentof the differentiation. Similar populationstructure on this extremely limited geographicscale could exist among Atlantic salmon runselsewhere in Maine and throughout the species'range and should be taken into account forfuture management decisions.     

Short-term genetic changes: evaluating effective population size estimates in a comprehensively described brown trout (Salmo trutta) population

The effective population size (N(e)) is notoriously difficult to accurately estimate in wild populations as it is influenced by a number of parameters that are difficult to delineate in natural systems. The different methods that are used to estimate N(e) are affected variously by different processes at the population level, such as the life-history characteristics of the organism, gene flow, and population substructure, as well as by the frequency patterns of genetic markers used and the sampling design. Here, we compare N(e) estimates obtained by different genetic methods and from demographic data and elucidate how the estimates are affected by various factors in an exhaustively sampled and comprehensively described natural brown trout (Salmo trutta) system. In general, the methods yielded rather congruent estimates, and we ascribe that to the adequate genotyping and exhaustive sampling. Effects of violating the assumptions of the different methods were nevertheless apparent. In accordance with theoretical studies, skewed allele frequencies would underestimate temporal allele frequency changes and thereby upwardly bias N(e) if not accounted for. Overlapping generations and iteroparity would also upwardly bias N(e) when applied to temporal samples taken over short time spans. Gene flow from a genetically not very dissimilar source population decreases temporal allele frequency changes and thereby acts to increase estimates of N(e). Our study reiterates the importance of adequate sampling, quantification of life-history parameters and gene flow, and incorporating these data into the N(e) estimation.     

Spatial and temporal variation of genetic diversity and estimation of effective population sizes in Atlantic salmon (Salmo salar, L.) populations from Asturias (Northern Spain) using microsatellites

Rivers in Asturias (northern Spain) constitute the southern limit of the distribution of Atlantic salmon (Salmo salar L.) in Europe, a biological resource facing one of the more serious challenges for conservation today. In this work, eight microsatellite loci have been used to analyse samples collected in 1993 and 1999 from four Asturian rivers (Esva, Narcea, Sella, and Cares), obtaining information about the temporal and the spatial genetic variation in these populations and, in addition, estimations of their effective population sizes. The temporal analysis revealed a general decrease in all the estimated genetic variability parameters when samples from 1993 (mean A ₍₁₉₉₃₎ = 6.47, mean H _O(1993) = 0.472, mean H _E(1993) = 0.530) were compared with those obtained in 1999 (mean A ₍₁₉₉₉₎ = 6.16, mean H _O(1999) = 0.460, mean H _E(1999) = 0.490). This reduction was particularly notable for the case of the Esva river. Our results pointed to a pattern of spatial genetic differentiation inside the Asturian region (F _{ST (1993)} = 0.016 P < 0.01; F _{ST (1999)} = 0.023 P < 0.01). Using the standard Temporal Method we found estimates of N _e^{^} _(Esva) = 75.1 (33.2–267.2); N _e^{^} _(Cares) = 96.6 (40.0–507.5), N _e^{^} _(Sella) = 106.5 (39.1–9396.4) and N _e^{^} _(Narcea) = 113.9 (42.0–3693.3). The use of likelihood-based methods for the N _e^{^} estimations improved the results (smaller CIs) for the Esva and Cares rivers (N _e^{^} _(Esva) = 63.9 (32.3–165.3); N _e^{^} _(Cares) = 76.4 (38.8–202.0) using a Maximum likelihood approach) and suggested the presence of larger populations for the Sella and Narcea rivers (N _e^{^}≈200). These results showed that the Asturian Atlantic salmon populations (in particular Esva and Cares river populations) could be close to the conservation genetic borderline for avoiding inbreeding depression although we discuss some implications of the analysis of temporal genetic change in populations with overlapping generations.     

Census vs. effective population size in chinook salmon: large- and small-scale environmental perturbation effects

Population viability has often been assessed by census of reproducing adults. Recently this method has been called into question and estimation of the effective population size (Ne) proposed as a complementary method to determine population health. We examined genetic diversity in five populations of chinook salmon (Oncorhynchus tshawytscha) from the upper Fraser River watershed (British Columbia, Canada) at 11 microsatellite loci over 20 years using DNA extracted from archived scale samples. We tested for changes in genetic diversity, calculated the ratio of the number of alleles to the range in allele size to give the statistic M, calculated Ne from the temporal change in allele frequency, used the maximum likelihood method to calculate effective population size (NeM), calculated the harmonic mean of population size, and compared these statistics to annual census estimates. Over the last two decades population size has increased in all five populations of chinook examined; however, Ne calculated for each population was low (81-691) and decreasing over the time interval measured. Values of NeM were low, but substantially higher than Ne calculated using the temporal method. The calculated values for M were generally low (M < 0.70), indicating recent population reductions for all five populations. Large-scale historic barriers to migration and development activities do not appear to account for the low values of Ne; however, available spawning area is positively correlated with Ne. Both Ne and M estimates indicate that these populations are potentially susceptible to inbreeding effects and may lack the ability to respond adaptively to stochastic events. Our findings question the practice of relying exclusively on census estimates for interpreting population health and show the importance of determining genetic diversity within populations.     

Being abundant is not enough: a decrease in effective population size over eight generations in a Norwegian population of the seaweed, Fucus serratus

The brown alga Fucus serratus is a key foundation species on rocky intertidal shores of northern Europe. We sampled the same population off the coast of southern Norway in 2000 and 2008, and using 26 microsatellite loci, we estimated the changes in genetic diversity and effective population size (Ne). The unexpectedly low Ne (73-386) and Ne/N ratio (10-3-10-4), in combination with a significant decrease (14%) in allelic richness over the 8-year period, suggests an increased local extinction risk. If small Ne proves to be a common feature of F. serratus, then being abundant may not be enough for the species to weather future environmental changes.     

Genetic diversity and effective size of the Atlantic salmon Salmo salar L. inhabiting the River Eo (Spain) following a stock collapse

Historic angling records suggest the occurrence of a drastic decline in the River Eo (Spain) Atlantic salmon population size during the past two decades, as a result of overexploitation and habitat deterioration. In recent years, the population has been apparently recovering, and the present study is aimed to report information on the level of genetic diversity and the effective size of the current population as these may have immediate consequences for its conservation. Eighty-six salmon from two temporal groups (1998–1999 and 2004–2006), representing three generations, were genotyped using a panel of eight microsatellites. Inspite of the recent decline in census numbers and the detection of the signs of a population bottleneck, the population exhibits a high level of genetic diversity, similar to that from other populations, and almost unchanged during the period of study [average allelic richness ( A ) = 14·0 and 13·9, and average heterozygosity ( H _e) = 0·843 and 0·851 in 1998–1999 and 2004–2006, respectively]. The effective population size ( N _e) estimated by two different temporal methods showed a consistent value around 80 salmon, whereas the estimates from the linkage disequilibrium (LD) method provided a value around 165 individuals for either sample. The recent growing number of salmon, as indicated by fisheries records, the relatively large estimates of the ratio N _e/ N (with range 0·23–0·44 for the temporal estimates and 0·31–0·59 for the LD estimates) and the high levels of diversity found suggest that the population has not been greatly affected by the historical census declines and can be expected to recover in the future.     

Genetic effective size of a wild primate population: influence of current and historical demography

A comprehensive assessment of the determinants of effective population size (N(e)) requires estimates of variance in lifetime reproductive success and past changes in census numbers. For natural populations, such information can be best obtained by combining longitudinal data on individual life histories and genetic marker-based inferences of demographic history. Independent estimates of the variance effective size (N(ev), obtained from life-history data) and the inbreeding effective size (N((eI), obtained from genetic data) provide a means of disentangling the effects of current and historical demography. The purpose of this study was to assess the demographic determinants of N(e) in one of the most intensively studied natural populations of a vertebrate species: the population of savannah baboons (Papio cynocephalus) in the Amboseli Basin, southern Kenya. We tested the hypotheses that N(eV) < N < N(eI) (where N = population census number) due to a recent demographic bottleneck. N(eV) was estimated using a stochastic demographic model based on detailed life-history data spanning a 28-year period. Using empirical estimates of age-specific rates of survival and fertility for both sexes, individual-based simulations were used to estimate the variance in lifetime reproductive success. The resultant values translated into an N(eV)/N estimate of 0.329 (SD = 0.116, 95% CI = 0.172-0.537). Historical N(eI), was estimated from 14-locus microsatellite genotypes using a coalescent-based simulation model. Estimates of N(eI) were 2.2 to 7.2 times higher than the contemporary census number of the Amboseli baboon population. In addition to the effects of immigration, the disparity between historical N(eI) and contemporary N is likely attributable to the time lag between the recent drop in census numbers and the rate of increase in the average probability of allelic identity-by-descent. Thus, observed levels of genetic diversity may primarily reflect the population's prebottleneck history rather than its current demography.     

Genetic and phenotypic changes in an Atlantic salmon population supplemented with non-local individuals: a longitudinal study over 21 years

While introductions and supplementations using non-native and potentially domesticated individuals may have dramatic evolutionary effects on wild populations, few studies documented the evolution of genetic diversity and life-history traits in supplemented populations. Here, we investigated year-to-year changes from 1989 to 2009 in genetic admixture at 15 microsatellite loci and in phenotypic traits in an Atlantic salmon (Salmo salar) population stocked during the first decade of this period with two genetically and phenotypically distinct source populations. We detected a pattern of temporally increasing introgressive hybridization between the stocked population and both source populations. The proportion of fish returning to the river after a single winter at sea (versus several ones) was higher in fish assigned to the main source population than in local individuals. Moreover, during the first decade of the study, both single-sea-winter and multi-sea-winter (MSW) fish assigned to the main source population were smaller than local fish. During the second decade of the study, MSW fish defined as hybrids were lighter and smaller than fish from parental populations, suggesting outbreeding depression. Overall, this study suggests that supplementation with non-local individuals may alter not only the genetic diversity of wild populations but also life-history traits of adaptive significance.     

Mitochondrial DNA variation, effective female population size and population history of the endangered Chinese sturgeon, Acipenser sinensis

The anadromous Chinese sturgeon (Acipenser sinensis), mainly endemic to the Yangtze River in China, is an endangered fish species. The natural population has declined since the Gezhouba Dam blocked its migratory route to the spawning grounds in 1981. In the near future, the completion of the Three Gorges Dam, the world's largest hydroelectric project, may further impact this species by altering the water flow of the Yangtze River. Little is currently known about the population genetic structure of the Chinese sturgeon. In this study, DNA sequence data were determined from the control region (D-loop) of the mitochondrial genome of adult sturgeons (n = 106) that were collected between 1995–2000. The molecular data were used to investigate genetic variation, effective female population size and population history of the Chinese sturgeon in the Yangtze River. Our results indicate that the reduction in abundance did not change genetic variation of the Chinese sturgeon, and that the population underwent an expansion in the past. AMOVA analysis indicated that 98.7% of the genetic variability occurred within each year's spawning populations, the year of collection had little influence on the diversity of annual temporary samples. The relative large effective female population size (N _ef) indicates that good potential exists for the recovery of this species in the future. Strikingly, the ratio of N _ef to the census female population size (N _f) is unusually high (0.77–0.93). This may be the result of a current bottleneck in the population of the Chinese sturgeon that is likely caused by human intervention. This revised version was published online in July 2006 with corrections to the Cover Date.     

Life history changes in Atlantic salmon from the River Dee,Wales

The change in life history of Atlantic salmon (Salmo salar L.) on the River Dee over the last 60 years is described. Over the last 60 years, salmon have shown a change in run timing, the majority currently entering the river between August and October compared with prior to June. This has coincided with a change in the sea age composition, which was dominated by multi-sea winter salmon prior to the 1980s after which the proportion of 1sea-winter fish increased until they now dominate the mature population. Growth rates of salmon in fresh water remained relatively stable until the mid-1980s and then increased. By the end of the 1990s juvenile salmon were, by the end of their first and second year, respectively, ∼60 and ∼19%, on average, larger than they were between the late 1930s and mid-1980s. This has been reflected in a change in the age composition of smolts where the mean smolt age has declined from ∼2 years prior to the 1980s to ∼1.6 years in the late 1990s. There was no observed trend in post-smolt (marine) growth for salmon. Size at return for 1SW salmon appeared stable while there is some evidence of an increase in mean length of 2SW salmon at the end of the 1990s. A steady state life history model was developed which suggests an increase in the instantaneous rate of mortality by 2.9% from 1.495 year⁻¹ in 1937/1938 to 1.538 year⁻¹ in 1967/1969 and by 21.6% to 1.870 year⁻¹ in 1997/1999. This is considered to explain the shift in mean age at maturity from 5.2 to 4.8 to 3.9 years for the three periods examined. There is close agreement between the observed mean age at maturity and that predicted by the model suggesting optimal lifetime reproductive success. Guest editors: S. Dufour, E. Prévost, E. Rochard & P. Williot Fish and diadromy in Europe (ecology, management, conservation)     

Spatial and temporal genetic differentiation and effective population size of brown trout (<Emphasis Type="Italic">Salmo trutta</Emphasis>, L.) in small Danish rivers

The spatial and temporal genetic structure of brown trout populations from three small tributaries of Lake Hald, Denmark, was studied using analysis of variation at eight microsatellite loci. From two of the populations temporal samples were available, separated by up to 13 years (3.7 generations). Significant genetic differentiation was observed among all samples, however, hierarchical analysis of molecular variance (AMOVA) showed that differentiation among populations accounted for a non-significant amount of the genetic differentiation, whereas differentiation among temporal samples within populations was highly significant (0.0244, P<0.001). Estimates of effective population size (N _e) using a maximum-likelihood based implementation of the temporal method, yielded small values (N _e ranging from 33 to 79). When a model was applied that allows for migration among populations, N _e estimates were even lower (24–54), and migration rates were suggested to be high (0.13–0.36). All samples displayed a clear signal of a recent bottleneck, probably stemming from a period of unfavourable conditions due to organic pollution in the 1970–1980’s. By comparison to other estimates of N _e in brown trout, Lake Hald trout represent a system of small populations linked by extensive gene flow, whereas other populations in larger rivers exhibit much higher N _e values and experience lower levels of immigration. We suggest that management considerations for systems like Lake Hald brown trout should focus both on a regional scale and at the level of individual populations, as the future persistence of populations depends both on maintaining individual populations and ensuring sufficient migration links among these populations.     

Effective size,census size,and genetic monitoring of the endangered razorback sucker, <Emphasis Type="Italic">Xyrauchen texanus</Emphasis>

For the past several decades the Lake Mohave population of the federally endangered razorback sucker, Xyrauchen texanus, has had no natural recruitment because of intensive predation on larvae by non-native fishes. In response to impending extirpation, a repatriation program was implemented where larval razorbacks are collected from the wild following natural spawning, reared in protective custody, and then repatriated at a much larger size. In this study, we estimated annual (N _bf) and generational female effective size (N _ef) of the spawning stock by characterizing temporal genetic changes in mtDNA among larval cohorts, and then compared these estimates to the estimated number of reproductively capable (adult) females in Lake Mohave (N _f). Razorback suckers have life history and mortality schedules that could yield values of N _ef/N _f as low as 10⁻⁵ due to match–mismatch recruitment (or the “Hedgecock effect”) that increases variance in reproductive success. Average N _bf was estimated to be 160, N _ef was 706, and the ratio N _ef/N _f was 0.29 and 0.38 for arithmetic and harmonic mean N _f, respectively. Our findings indicate that (i) larval sampling in Lake Mohave sufficiently encompasses temporal and spatial variation within annual larval cohorts as to be representative of the spawning stock, (ii) roughly 3–16% (about 8% on average) of adult females contribute genetically to larval cohorts each year, and (iii) repatriated fishes appear to be contributing genetically to larval cohorts. Simultaneous genetic and demographic monitoring offers insights that neither approach can provide alone into effects of population decline and management practices in this species.     

Diel activity pattern of juvenile Atlantic salmon (Salmo salar) in early and late winter

Radiotelemetry was used to investigate the diel activity pattern of juvenile Atlantic salmon (Salmo salar) in early and late winter. Fish were active throughout the diel cycle. However, there was significantly less daytime than nighttime movement and movement declined significantly with increasing fork length. Maximizing winter growth rate, through an overall increase in foraging activity, may reduce the risk of starvation in smaller fish. The results of the present study provide evidence that the activity patterns of juvenile salmonids are quite complex and support the suggestion that individual variation in activity patterns are, at least, partially driven by body size.     

Impact of precocious male parr on the effective size of a wild population of Atlantic salmon

1. There is growing evidence that sexually mature but morphologically juvenile males of Atlantic salmon (precocious or mature male parr) actively participate in reproduction and, therefore, in the genetic composition of the populations of this species. The impact of mature male parr on the effective population size (N_e) of such populations has been previously studied under experimental settings, but no studies have been performed directly on natural populations. 2. Continuous monitoring and sampling of all sea returns is possible in the Lérez River (northwest of Spain). From demographic data on variances of reproductive success and genetic data from six microsatellite marker loci we carried out parentage assignment and assessed the impact of male parr on demographic and genetic estimates of N_e in two consecutive years. 3. Our results reveal that: (i) approximately 60% of the total sire paternity is attributable to mature parr; (ii) mature parr decrease the variance of reproductive success of males by a threefold factor and increase the effective population size of males by a 10‐fold factor; (iii) however, they do not substantially affect the variance of reproductive success and the effective size of females; (iv) mature parr increase two‐to threefold the overall effective size of the population but the ratio N_e/N, where N is the population size including or not mature parr in each case, is not affected.     

Temporal changes in allele frequencies and low effective population size in greater prairie-chickens

The number of greater prairie-chickens in Wisconsin has decreased by 91% since 1932. The current population of approximately 1500 birds exists primarily in four isolated management areas. In previous studies of the Wisconsin populations we documented low levels of genetic variation at microsatellite loci and the mitochondrial DNA control region. Here we investigate changes in genetic structure between the four management areas in Wisconsin over the last 50 years. We estimated the harmonic mean effective population size (Ne) over the last 50 years by comparing allele frequencies from the early 1950s with those from contemporary samples. Using a pseudo-likelihood approach that accounted for migration, estimates of Ne (15-32 prairie-chickens within each management area) were 10 times lower than census numbers from booming-ground counts. These low estimates of Ne are consistent with increased habitat fragmentation and an increase in genetic isolation between management areas over the last 50 years. The reduction of gene flow between areas has reduced Ne, increased genetic drift and, consequently, reduced genetic variation. These results have immediate consequences for the conservation of the prairie-chicken, and highlight the importance of how mating systems and limited dispersal may exacerbate the loss of genetic variation in fragmented populations.     

Genetic variation, genetic structure and effective population size in the tropical holoparasitic endophyteBdallophyton bambusarum (Rafflesiaceae)

The genetic population structure inBdallophyton bambusarum, an endoparasite, was studied in ten subpopulations from a subdeciduous tropical forest in Veracruz Mexico. The sample was analyzed using seven polymorphic loci in cellulose acetate electrophoresis. Isozyme data indicated that the subpopulations ofB. bambusarum contained high genetic variability (H_ep = 0.452 ± 0.045, S.E.). Our analysis suggests that almost each inflorescence ofB. bambusarum is an individual. The subpopulations studied were genetically similar (average Nei's genetic identity 0.941 ± 0.051 and F _st values 0.097 ± 0.026), suggesting that genetic differentiation among subpopulations was small. Direct estimates of effective population size was derived from observations of three fluorescent dyes, and from the genetic neighborhood area derived from these data. The neighborhood area, multiplied by the total density of individuals, gave an N_e = 124.84 plants, and when corrected to consider the proportion of males and females gave an N_e = 118.59 individuals. An indirect estimate of Nm was obtained from the F _st values (mean Nm=2.037), giving an indirect estimate of the effective population size N_b = 12.8 individuals. Both values are relatively high when compared to other plant studies. The gene flow and/or effective populations size of the studied subpopulations ofB. bambusarum are believed to be large enough to prevent differentiation among subpopulations due to genetic drift.     

Effect of natural selection on the duplicated lysyl oxidase gene in Atlantic salmon

We examined the polymorphism of the lysyl oxidase (LOX) locus, involved in the initiation of muscle collagen cross-linking, in three populations of Atlantic salmon with different life histories and growth rates and compared it with a closely related species (rainbow trout). Up to four alleles were observed per individual, probably as a consequence of the tetraploid origin of the salmonid genome. We found high polymorphism in the LOX locus (16 alleles expressed in total and several low frequency private alleles) in two natural Atlantic salmon populations and extremely reduced diversity in a farmed population (3 alleles) with low density of collagen crosslinks. We also assessed the relative role of selection in maintaining LOX genetic variability in Atlantic salmon. Results from several neutrality tests suggest that selection is playing a role in shaping diversity at the LOX locus. Positive selection was inferred by three different likelihood phylogeny-based methods and one selected site, identified by all three different methods (PAML, FEL and REL) was located within the “copper-talon” characteristic of LOX proteins. We suggest that the retention of four alleles in the salmon LOX locus could be related to its multiple functions.     

Demineralization of the vertebral skeleton in Atlantic salmon Salmo salar L. during spawning migration

In Atlantic salmon, Salmo salar, the mineral rate of vertebrae in a given fish varies according to the position of the vertebra along the rachidian axis. Indeed, the mean rate goes from 49% in the anterior vertebrae and raises to 51% in post-truncal vertebrae. Although no significant difference in the mineral rate was noticed between males and females either in the lower river basin or after spawning, the mineral rate of vertebral bone decreased significantly (1–2%) during spawning migration. Vertebrae, like scales, are an important reservoir of calcium from which fasting salmon draws the minerals and organic materials necessary for the substantial remodeling of cranial bones in males and for sexual maturation. We hypothesize that mineral decrease in vertebrae may be the result of a halastasic demineralization of the vertebral tissues.