Spatiotemporal relationship between adult census size and genetic population size across a wide population size gradient

Adult census population size (N) and effective number of breeders (N_b) are highly relevant for designing effective conservation strategies. Both parameters are often challenging to quantify, however, making it of interest to determine whether one parameter can be generalized from the other. Yet, the spatiotemporal relationship between N and N_b has not been well characterized empirically in many taxa. We analysed this relationship for 5–7 consecutive years in twelve brook trout populations varying greatly in N (49‐10032) and N_b (3‐567) and identified major environmental variables affecting the two parameters. N or habitat size alone explained 47–57% of the variance in N_b, and N_b was strongly correlated with effective population size. The ratio N_b/N ranged from 0.01 to 0.45 and increased at small N or following an annual decrease in N, suggesting density‐dependent constraints on N_b. We found no evidence for a consistent, directional difference between variability in N_b and/or N_b/N among small and large populations; however, small populations had more varying temporal variability in N_b/N ratios than large populations. Finally, N_b and N_b/N were 2.5‐ and 2.3‐fold more variable among populations than temporally within populations. Our results demonstrate a clear linkage between demographic and evolutionary parameters, suggesting that N_b could be used to approximate N (or vice versa) in natural populations. Nevertheless, using one variable to infer the other to monitor trends within populations is less recommended, perhaps even less so in small populations given their less predictable N_b vs. N dynamics.     

Temporal genetic stability and high effective population size despite fisheries-induced life-history trait evolution in the North Sea sole

Heavy fishing and other anthropogenic influences can have profound impact on a species' resilience to harvesting. Besides the decrease in the census and effective population size, strong declines in mature adults and recruiting individuals may lead to almost irreversible genetic changes in life-history traits. Here, we investigated the evolution of genetic diversity and effective population size in the heavily exploited sole (Solea solea), through the analysis of historical DNA from a collection of 1379 sole otoliths dating back from 1957. Despite documented shifts in life-history traits, neutral genetic diversity inferred from 11 microsatellite markers showed a remarkable stability over a period of 50 years of heavy fishing. Using simulations and corrections for fisheries induced demographic variation, both single-sample estimates and temporal estimates of effective population size (N(e) ) were always higher than 1000, suggesting that despite the severe census size decrease over a 50-year period of harvesting, genetic drift is probably not strong enough to significantly decrease the neutral diversity of this species in the North Sea. However, the inferred ratio of effective population size to the census size (N(e) /N(c) ) appears very small (10(-5) ), suggesting that overall only a low proportion of adults contribute to the next generation. The high N(e) level together with the low N(e) /N(c) ratio is probably caused by a combination of an equalized reproductive output of younger cohorts, a decrease in generation time and a large variance in reproductive success typical for marine species. Because strong evolutionary changes in age and size at first maturation have been observed for sole, changes in adaptive genetic variation should be further monitored to detect the evolutionary consequences of human-induced selection.     

Population genetic structure and effective population size of ayu (Plecoglossus altivelis), an amphidromous fish

The temporal and spatial population genetic structure of ayu Plecoglossus altivelis (Salmoniformes: Plecoglossidae), an amphidromous fish, was examined using analysis of variation at six microsatellite DNA loci. Intracohort genetic diversities, as measured by the number of alleles and heterozygosity, were similar among six cohorts (2001–2006) within a population (Nezugaseki River), with the mean number of alleles per cohort ranging from 11·0 to 12·5 and the expected heterozygosity ranging from 0·74 to 0·77. Intrapopulational genetic diversities were also similar across the three studied populations along the 50 km coast, with the mean number of alleles and the expected heterozygosity ranging from 11·33 to 11·67 and from 0·75 to 0·76, respectively. The authors observed only one significant difference in pair-wise population differentiation ( F _ST-value) between the cohorts within a population and among three populations. Estimates of the effective population size ( N _e) based on maximum-likelihood method yielded small values (ranging from 94·8 to 135·5), whereas census population size ranged from c. 4800 to 24 000. As a result, the ratio of annual effective population sizes to census population size ( N _e/ N ) ranged from 0·004 to 0·023. These estimates of N _e/ N agree more closely with estimates for marine fishes than that of the larger estimates for freshwater fishes. The present study suggests that ayu which is highly fecund and shows low survival during the early life stages is also characterized by having low value of N _e/ N , similar to marine species with a pelagic life cycle.     

Large variations in the ratio of effective breeding and census population sizes between two species of pond-breeding anurans

The viability of wild populations is frequently assessed by monitoring adult census sizes ( N _c). This approach is particularly useful for pond-breeding amphibians, because assemblages during the breeding season are relatively easy to detect and count. However, it is the genetic effective population size ( N _e) or surrogates such as effective breeding population size ( N _b) that are of primary importance for long-term viability. Although N _c estimates of one anuran amphibian ( Bufo bufo ) in Britain were much larger than those of another ( Rana temporaria ) at the same sites, the ratios of N _b to N _c were much smaller in B. bufo than in R. temporaria. These differences were sufficiently great as to reverse the effective size order at one site, such that N _b for R. temporaria was larger than that for B. bufo. Differences in adult sex ratios at breeding sites probably contributed to lower N _b values in B. bufo populations compared with those of R. temporaria . The relationship of N _b to N _c can therefore vary dramatically even between similar species, to the extent that just monitoring N _c can give misleading impressions of relative effective breeding sizes and thus of population viability. It will be increasingly important to estimate N _e or N _b in wildlife populations for assessment of conservation priorities.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 365–372.     

Effects of population characteristics and structure on estimates of effective population size in a house sparrow metapopulation

Effective population size (N_e) is a key parameter to understand evolutionary processes and the viability of endangered populations as it determines the rate of genetic drift and inbreeding. Low N_e can lead to inbreeding depression and reduced population adaptability. In this study, we estimated contemporary N_e using genetic estimators (LDNE, ONeSAMP, MLNE and CoNe) as well as a demographic estimator in a natural insular house sparrow metapopulation. We investigated whether population characteristics (population size, sex ratio, immigration rate, variance in population size and population growth rate) explained variation within and among populations in the ratio of effective to census population size (N_e/N_c). In general, N_e/N_c ratios increased with immigration rates. Genetic N_e was much larger than demographic N_e, probably due to a greater effect of immigration on genetic than demographic processes in local populations. Moreover, although estimates of genetic N_e seemed to track N_c quite well, the genetic N_e‐estimates were often larger than N_c within populations. Estimates of genetic N_e for the metapopulation were however within the expected range (<N_c). Our results suggest that in fragmented populations, even low levels of gene flow may have important consequences for the interpretation of genetic estimates of N_e. Consequently, further studies are needed to understand how N_e estimated in local populations or the total metapopulation relates to actual rates of genetic drift and inbreeding.     

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.     

Variance effective population size is affected by census size in sub-structured populations

Measurement of allele frequency shifts between temporally spaced samples has long been used for assessment of effective population size (N_e), and this ‘temporal method’ provides estimates of N_e referred to as variance effective size (N_eV). We show that N_eV of a local population that belongs to a sub-structured population (a metapopulation) is determined not only by genetic drift and migration rate (m), but also by the census size (N_c). The realized N_eV of a local population can either increase or decrease with increasing m, depending on the relationship between N_e and N_c in isolation. This is shown by explicit mathematical expressions for the factors affecting N_eV derived for an island model of migration. We verify analytical results using high-resolution computer simulations, and show that the phenomenon is not restricted to the island model migration pattern. The effect of N_c on the realized N_eV of a local subpopulation is most pronounced at high migration rates. We show that N_c only affects local N_eV, whereas N_eV for the metapopulation as a whole, inbreeding (N_eI), and linkage disequilibrium (N_eLD) effective size are all independent of N_c. Our results provide a possible explanation to the large variation of N_e/N_c ratios reported in the literature, where N_e is frequently estimated by N_eV. They are also important for the interpretation of empirical N_e estimates in genetic management where local N_eV is often used as a substitute for inbreeding effective size, and we suggest an increased focus on metapopulation N_eV as a proxy for N_eI.     

Temporal genetic variation of mitochondrial DNA and the female effective population size of red drum (Sciaenops ocellatus) in the northern Gulf of Mexico

We studied genetic drift of mitochondrial DNA (mtDNA) haplotype frequencies in a natural population of red drum (Sciaenops ocellatus) from the northern Gulf of Mexico (Gulf). The amount of genetic drift observed across temporally adjacent year classes (1986–89) was used to estimate variance effective (female) population size (N_ef). N_ef was estimated to be 14 308 and the ratio of female effective size to adult female census size was approximately 0.004, which is among the lowest value reported for vertebrate animals. Low effective size relative to census size among red drum in the northern Gulf may result from yearly fluctuations in the number of breeding females, high variance in female reproductive success, or both. Despite low genetic effective size relative to census size, the genetic effective population size of red drum in the northern Gulf appears sufficiently large to preclude potentially deleterious effects of inbreeding.     

Small effective population sizes in two planktonic freshwater copepod species (Eudiaptomus) with apparently large census sizes

In small planktonic organisms, large census sizes (N(c)) suggest large effective population sizes (N(e)), but reliable estimates are rare. Here, we present N(e)/N(c) ratios for two freshwater copepod species (Eudiaptomus sp.) using temporal samples of multilocus microsatellite genotypes and a pseudo-likelihood approach. N(e)/N(c) ratios were very small in both Eudiaptomus species (10(-7)-10(-8)). Although we hypothesized that the species producing resting eggs (E. graciloides) had a larger N(e) than the other (E. gracilis), estimates were not statistically different (E. graciloides: N(e) = 672.7, CI: 276-1949; E. gracilis: N(e) = 1027.4, CI: 449-2495), suggesting that the propagule bank of E. graciloides had no detectable influence on N(e).     

History vs. current demography: explaining the genetic population structure of the common frog (Rana temporaria)

The amount of genetic variability at neutral marker loci is expected to decrease, and the degree of genetic differentiation among populations to increase, as a negative function of effective population size. We assessed the patterns of genetic variability and differentiation at seven microsatellite loci in the common frog (Rana temporaria) in a hierarchical sampling scheme involving three regions (208-885 km apart), three subregions within regions and nine populations (5-20 km apart) within subregions, and related the variability and differentiation estimates to variation in local population size estimates. Genetic variability within local populations decreased significantly with increasing latitude, as well as with decreasing population size and regional site occupancy (proportion of censured localities occupied). The positive relationship between population size and genetic variability estimates was evident also when the effect of latitude (cf. colonization history) was accounted for. Significant genetic differentiation was found at all hierarchical levels, and the degree of population differentiation tended to increase with increasing latitude. Isolation by distance was evident especially at the regional sampling level, and its strength increased significantly towards the north in concordance with decreasing census and marker-based neighbourhood size estimates. These results are in line with the conjecture that the influence of current demographic factors can override the influence of historical factors on species population genetic structure. Further, the observed reductions in genetic variability and increased degree of population differentiation towards the north are in line with theoretical and empirical treatments suggesting that effective population sizes decline towards the periphery of a species' range.     

Effective/census population size ratio estimation: a compendium and appraisal

With an ecological-evolutionary perspective increasingly applied toward the conservation and management of endangered or exploited species, the genetic estimation of effective population size (N_e) has proliferated. Based on a comprehensive analysis of empirical literature from the past two decades, we asked: (i) how often do studies link N_e to the adult census population size (N)? (ii) To what extent is N_e correctly linked to N? (iii) How readily is uncertainty accounted for in both N_e and N when quantifying N_e/N ratios? and (iv) how frequently and to what degree might errors in the estimation of N_e or N affect inferences of N_e/N ratios? We found that only 20% of available N_e estimates (508 of 2617; 233 studies) explicitly attempted to link N_e and N; of these, only 31% (160 of 508) correctly linked N_e and N. Moreover, only 7% (41 of 508) of N_e/N ratios (correctly linked or not) reported confidence intervals for both N_e and N; for those cases where confidence intervals were reported for N_e only, 31% of N_e/N ratios overlapped with 1, of which more than half also reached below N_e/N = 0.01. Uncertainty in N_e/N ratios thus sometimes spanned at least two orders of magnitude. We conclude that the estimation of N_e/N ratios in natural populations could be significantly improved, discuss several options for doing so, and briefly outline some future research directions.     

A comparison of single‐sample effective size estimators using empirical toad (Bufo calamita) population data: genetic compensation and population size‐genetic diversity correlations

The accuracy and precision of four single‐sample estimators of effective population size, N_e (heterozygote excess, linkage disequilibrium, Bayesian partial likelihood and sibship analysis) were compared using empirical data (microsatellite genotypes) from multiple natterjack toad (Bufo calamita) populations in Britain (n = 16) and elsewhere in Europe (n = 10). Census size data were available for the British populations. Because toads have overlapping generations, all of these methods estimated the number of effective breeders N_b rather than N_e. The heterozygote excess method only provided results, without confidence limits, for nine of the British populations. Linkage disequilibrium gave estimates for 10 British populations, but only six had finite confidence limits. The Bayesian and sibship methods both produced estimates with finite confidence limits for all the populations. Although the Bayesian method was the most precise, on most criteria (insensitivity to locus number, correlation with other effective and census size estimates and correlation with genetic diversity) the sibship method performed best. The results also provided evidence of genetic compensation in natterjack toads, and highlighted how the relationship between effective size and genetic diversity can vary as a function of geographical scale.     

The annual number of breeding adults and the effective population size of syntopic newts (Triturus cristatus, T. marmoratus)

Pond-breeding amphibians are deme-structured organisms with a population genetic structure particularly susceptible to demographic threats. We estimated the effective number of breeding adults (Nb) and the effective population size (Ne) of the European urodele amphibians Triturus cristatus (the crested newt) and T. marmoratus (the marbled newt), using temporal shifts in microsatellite allele frequencies. Eight microsatellite loci isolated from a T. cristatus library were used, five of which proved polymorphic in T. marmoratus, albeit with high frequencies of null alleles at two loci. Three ponds in western France were sampled, situated 4-10 kilometers apart and inhabited by both species. Parent-offspring cohort comparisons were used to measure Nb; samples collected at time intervals of nine or 12 years, respectively, were used to measure Ne. The adult population census size (N) was determined by mark-recapture techniques. With one exception, genetic distances (FST) between temporal samples were lower than among populations. Nb ranged between 10.6 and 101.8 individuals, Ne ranged between 9.6 and 13.4 individuals. For the pond where both parameters were available, Nb/N (overall range: 0.10-0.19) was marginally larger than Ne/N (overall range: 0.09-0.16), which is reflected in the temporal stability of N. In line with the observed differences in reproductive life-histories between the species, Nb/N ratios for newts were about one order of magnitude higher than for the anuran amphibian Bufo bufo. Despite of the colonization of the study area by T. cristatus only some decades ago, no significant genetic bottleneck could be detected. Our findings give rise to concerns about the long-term demographic viability of amphibian populations in situations typical for European landscapes.     

Low genetic diversity and small population size of Takahe Porphyrio hochstetteri on European arrival in New Zealand

The rediscovery of the Takahe Porphyrio hochstetteri in 1948 in the remote mountains of Fiordland, New Zealand, has been described as one of the greatest moments in ornithological history. The subsequent management of the population has become a model for avian recovery programmes, yet questions still remain regarding the population size at the time of, and prior to, its rediscovery. We used 20 microsatellite markers to genotype samples of the three surviving museum specimens (1849–1898) collected prior to the initial declaration of extinction to estimate levels of genetic diversity and effective population size. These estimates were compared with equivalent estimates from DNA samples of three specimens preserved at the time of rediscovery (1949) and with 20 contemporary samples. Using rarefaction simulations to account for the limited sample sizes, the results suggest that only slightly more genetic diversity (allelic diversity and numbers of polymorphic loci) existed in the earliest Takahe sampled and that levels of genetic diversity at the time of rediscovery were very similar to those today. Effective population size estimates showed a similar pattern. Contemporary samples from a widespread congener to Takahe, the Pukeko Porphyrio porphyrio, showed consistently higher levels of genetic diversity and greater effective population size, even after equivalent rarefaction to the same small sample sizes available for Takahe. It is likely that the population size of Takahe in Fiordland at the time of European arrivals in the 1800s was similar to its current size. These results provide molecular support for the hypothesis that Takahe were common throughout most coastal and eastern parts of the South Island of New Zealand before being hunted to extinction in these regions by early Maori, and persisted as a relatively small and isolated population in Fiordland where they may never have been very common. This is in marked contrast to other New Zealand endemic birds found in Fiordland, such as the Kakapo Strigops habroptilus and several forest passerines, which remained relatively numerous until the time of European arrival before undergoing rapid declines thereafter.     

The effects of cyclic dynamics and mating system on the effective size of an island mouflon population

The Haute Island mouflon (Ovis aries) population is isolated on one small (6.5 km2) island of the remote Kerguelen archipelago. Given a promiscuous mating system, a cyclic demography and a strong female-biased sex ratio after population crashes, we expected a low effective population size (Ne). We estimated Ne using demographic and temporal genetic approaches based on genetic information at 25 microsatellite loci from 62 and 58 mouflons sampled in 1988 and 2003, respectively. Genetic Ne estimates were higher than expected, varying between 104 and 250 depending on the methods used. Both demographic and genetic approaches show the Haute Island Ne is buffered against population crashes. The unexpectedly high Ne likely results from the cyclic winter crashes that allow young males to reproduce, limiting the variance of male reproductive success. Based on individual-based simulations, we suggest that despite a strongly female-biased sex ratio, the effects of the mating system on the effective population size more closely resemble random mating or weak polygyny.     

Monitoring the effective population size of a brown bear (Ursus arctos) population using new single-sample approaches

The effective population size (N(e) ) could be the ideal parameter for monitoring populations of conservation concern as it conveniently summarizes both the evolutionary potential of the population and its sensitivity to genetic stochasticity. However, tracing its change through time is difficult in natural populations. We applied four new methods for estimating N(e) from a single sample of genotypes to trace temporal change in N(e) for bears in the Northern Dinaric Mountains. We genotyped 510 bears using 20 microsatellite loci and determined their age. The samples were organized into cohorts with regard to the year when the animals were born and yearly samples with age categories for every year when they were alive. We used the Estimator by Parentage Assignment (EPA) to directly estimate both N(e) and generation interval for each yearly sample. For cohorts, we estimated the effective number of breeders (N(b) ) using linkage disequilibrium, sibship assignment and approximate Bayesian computation methods and extrapolated these estimates to N(e) using the generation interval. The N(e) estimate by EPA is 276 (183-350 95% CI), meeting the inbreeding-avoidance criterion of N(e) > 50 but short of the long-term minimum viable population goal of N(e) > 500. The results obtained by the other methods are highly consistent with this result, and all indicate a rapid increase in N(e) probably in the late 1990s and early 2000s. The new single-sample approaches to the estimation of N(e) provide efficient means for including N(e) in monitoring frameworks and will be of great importance for future management and conservation.     

Contemporary effective population size and predicted maintenance of genetic diversity in the endangered kea (Nestor notabilis)

Population size and the potential for maintenance of genetic diversity are critical information for the monitoring of species of conservation concern. However, direct estimates of population size are not always feasible, making indirect genetic approaches a valuable alternative. We estimated contemporary effective population size (N_e) in the endangered kea (Nestor notabilis) using three different methods. We then inferred the census size (N_C) using published N_e/N_C ratios and modelled the future maintenance of genetic diversity assuming a number of demographic parameters. Short-term N_e was small with a range-wide N_e?N_C was within the range of the current estimate (c. 1000–5000). Forward simulations showed low probability of retaining 90% of rare alleles without immigration. However, the probability of maintaining genetic diversity was high with immigration, juvenile survival of?≥?30%, and an initial sex ratio of c. 0.5–0.6. Despite the low N_e in kea, predator control and/or artificial immigration might be sufficient to maintain the present genetic diversity.     

Reduced genetic diversity and low effective size in peripheral northern European catfish Silurus glanis populations

Using 10 polymorphic microsatellites and 1251 individual samples (some dating back to the early 1980s), genetic structure and effective population size in all native and introduced Swedish populations of the European wels catfish or Silurus glanis were studied. Levels of genetic variability and phylogeographic relationships were compared with data from a previous study of populations in other parts of Europe. The genetically distinct Swedish populations displayed comparably low levels of genetic variability and according to one-sample estimates based on linkage disequilibrium and sib ship-reconstruction, current local effective population sizes were lower than minimum levels recommended for short-term genetic conservation. In line with a previous suggestion of postglacial colonisation from a single refugium, all Swedish populations were assembled on a common branch in a star-shaped dendrogram together with other European populations. Two distinct subpopulations were detected in upper and lower habitats of River Emån, indicating that even minor dispersal barriers may restrict gene flow for wels in running waters. Genetic assignment of specimens encountered in the brackish Baltic Sea and in lakes where the species does not occur naturally indicated presence of long-distance sea dispersal and confirmed unauthorised translocations, respectively.     

Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout

Estimates of effective population size (Ne) are required to predict the impacts of genetic drift and inbreeding on the evolutionary dynamics of populations. How the ratio of Ne to the number of sexually mature adults (N) varies in natural vertebrate populations has not been addressed. We examined the sensitivity of Ne/N to fluctuations of N and determined the major variables responsible for changing the ratio over a period of 17 years in a population of steelhead trout (Oncorhynchus mykiss) from Washington State. Demographic and genetic methods were used to estimate Ne. Genetic estimates of Ne were gained via temporal and linkage disequilibrium methods using data from eight microsatellite loci. DNA for genetic analysis was amplified from archived smolt scales. The Ne/N from 1977 to 1994, estimated using the temporal method, was 0.73 and the comprehensive demographic estimate of Ne/N over the same time period was 0.53. Demographic estimates of Ne indicated that variance in reproductive success had the most substantial impact on reducing Ne in this population, followed by fluctuations in population size. We found increased Ne/N ratios at low N, which we identified as genetic compensation. Combining the information from the demographic and genetic methods of estimating Ne allowed us to determine that a reduction in variance in reproductive success must be responsible for this compensation effect. Understanding genetic compensation in natural populations will be valuable for predicting the effects of changes in N (i.e. periods of high population density and bottlenecks) on the fitness and genetic variation of natural populations.