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.     

Reproductive success and effective population size in woodrats (Neotoma macrotis)

Discrepancies between the census size and the genetically effective size of populations (N(e)) can be caused by a number of behavioural and demographic factors operating within populations. Specifically, strong skew in male reproductive success, as would be expected in a polygynous mating system, could cause a substantial decrease in N(e) relative to census size. Because the mating system of Neotoma macrotis had previously been described as one nearing harem polygyny, I examined the distribution of reproductive success and genetic variation within a population of this species. Combining genetic data and three years of field observations, I show that variance in reproductive success does not deviate from poisson expectations within either sex and variance in success is similar between the sexes. Furthermore, both males and females had multiple partners across litters in addition to some evidence of multiple paternity within litters. Despite a lack of strong skew in reproductive success, an estimate of N(e) based on a number of demographic parameters suggests that the ratio of N(e)/N in this population is 0.48. Although the ratio of N(e)/N suggests that the population is experiencing higher rates of genetic drift than would be expected based on census size alone, the population maintains high levels of genetic diversity. Estimates of neighbourhood size and patterns of recruitment to the study site suggest that immigration plays an important role in this population and may contribute to the maintenance of high levels of genetic diversity.     

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.     

Determinants of effective population size for loci with different modes of inheritance

Here we report an assessment of the determinants of effective population size (N(e)) in species with overlapping generations. Specifically, we used a stochastic demographic model to investigate the influence of different life-history variables on N(e)/N (where N = population census number) and the influence of sex differences in life-history variables on N(e) for loci with different modes of inheritance. We applied an individual-based modeling approach to two datasets: one from a natural population of savannah baboons (Papio cynocephalus) in the Amboseli basin of southern Kenya and one from a human tribal population (the Gainj of Papua New Guinea). Simulation-based estimates of N(e)/N averaged 0.329 for the Amboseli baboon population (SD = 0.116, 95% CI = 0.172 - 0.537) and 0.786 for the Gainj (SD = 0.184, 95% CI = 0.498 - 1.115). Although variance in male fitness had a substantial impact on N(e)/N in each of the two primate populations, ratios of N(e) values for autosomal and sex-linked loci exhibited no significant departures from Poisson-expected values. In each case, similarities in sex-specific N(e) values were attributable to the unexpectedly high variance in female fitness. Variance in male fitness resulted primarily from age-dependent variance in reproductive success, whereas variance in female fitness resulted primarily from stochastic variance in survival during the reproductive phase.     

A modified stepping-stone model of population structure in red drum, Sciaenops ocellatus (Sciaenidae), from the northern Gulf of Mexico

Genetic studies of population or stock structure in exploited marine fishes typically are designed to determine whether geographic boundaries useful for conservation and management planning are identifiable. Implicit in many such studies is the notion that subpopulations or stocks, if they exist, have fixed territories with little or no gene exchange between them. Herein, we review our long-term genetic studies of red drum (Sciaenops ocellatus), an estuarine-dependent sciaenid fish in the Gulf of Mexico and western Atlantic Ocean. Significant differences in frequencies of mitochondrial DNA haplotypes and of alleles at nuclear-encoded microsatellites occur among red drum sampled across the northern Gulf of Mexico. The spatial distribution of the genetic variation, however, follows a pattern of isolation-by-distance consistent with the hypothesis that gene flow occurs among subpopulations and is an inverse (and continuous) function of geographic distance. However, successful reproduction and recruitment of red drum depend on estuarine habitats that have geographically discrete boundaries. We hypothesize that population structure in red drum follows a modified one-dimensional, linear stepping-stone model where gene exchange occurs primarily (but not exclusively) between adjacent bays and estuaries distributed linearly along the coastline. Gene flow does occur among estuaries that are not adjacent but probabilities of gene exchange decrease as a function of geographic distance. Implications of our hypothesis are discussed in terms of inferences drawn from patterns of isolation-by-distance and relative to conservation and management of estuarine-dependent species like red drum. Based on estimates of the ratio of genetic effective population size and census size in red drum, observed patterns of gene flow in red drum may play a significant role in recruitment.     

Concurrent habitat and life history influences on effective/census population size ratios in stream-dwelling trout

Lower effective sizes (N(e)) than census sizes (N) are routinely documented in natural populations, but knowledge of how multiple factors interact to lower N(e)/N ratios is often limited. We show how combined habitat and life-history influences drive a 2.4- to 6.1-fold difference in N(e)/N ratios between two pristine brook trout (Salvelinus fontinalis) populations occupying streams separated by only 750 m. Local habitat features, particularly drainage area and stream depth, govern trout biomass produced in each stream. They also generate higher trout densities in the shallower stream by favoring smaller body size and earlier age-at-maturity. The combination of higher densities and reduced breeding site availability in the shallower stream likely leads to more competition among breeding trout, which results in greater variance in individual reproductive success and a greater reduction in N(e) relative to N. A similar disparity between juvenile or adult densities and breeding habitat availability is reported for other species and hence may also result in divergent N(e)/N ratios elsewhere. These divergent N(e)/N ratios between adjacent populations are also an instructive reminder for species conservation programs that genetic and demographic parameters may differ dramatically within species.     

Local extinction and recolonization, species effective population size, and modern human origins

A primary objection from a population genetics perspective to a multiregional model of modern human origins is that the model posits a large census size, whereas genetic data suggest a small effective population size. The relationship between census size and effective size is complex, but arguments based on an island model of migration show that if the effective population size reflects the number of breeding individuals and the effects of population subdivision, then an effective population size of 10,000 is inconsistent with the census size of 500,000 to 1,000,000 that has been suggested by archeological evidence. However, these models have ignored the effects of population extinction and recolonization, which increase the expected variance among demes and reduce the inbreeding effective population size. Using models developed for population extinction and recolonization, we show that a large census size consistent with the multiregional model can be reconciled with an effective population size of 10,000, but genetic variation among demes must be high, reflecting low interdeme migration rates and a colonization process that involves a small number of colonists or kin-structured colonization. Ethnographic and archeological evidence is insufficient to determine whether such demographic conditions existed among Pleistocene human populations, and further work needs to be done. More realistic models that incorporate isolation by distance and heterogeneity in extinction rates and effective deme sizes also need to be developed. However, if true, a process of population extinction and recolonization has interesting implications for human demographic history.     

Allozyme differentiation within and between red drum (Sciaenops ocellatus) from the Gulf of Mexico and Atlantic Ocean

Nine polymorphic nuclear-gene (allozyme) loci were surveyed among 491 red drum ( Sciaenops ocellatus ) sampled in 1988 and 1989 from nearshore localities in the northern Gulf of Mexico (Gulf) and the Atlantic coast of the southeastern United States (Atlantic). Data were combined with those from a previous study to generate a data set of 762 individuals representing 11 sample localities in the Gulf and 175 individuals representing five sample localities in the Atlantic. The combined data set included individuals from the 1986 and 1987 year classes and permitted rigorous testing of both temporal and spatial genetic heterogeneity. Average heterozygosity-per-locus values (estimated using 33 assumed monomorphic loci) were 0·048 (Gulf red drum) and 0·046 (Atlantic red drum). Tests of heterogeneity in allele frequencies between year classes at individual localities and across regions (Gulf and Atlantic) were non-significant. Tests of spatial (geographic) heterogeneity indicated that red drum are weakly subdivided: genetically-differentiated subpopulations occur in the northern Gulf and along the south-eastern Atlantic coast. Genetic data were consistent with the hypothesis that red drum within the Gulf and along the Atlantic coast comprise singie subpopulalions. Genetic differences between Gulf and Atlantic red drum seem likeiy to stem from historical or recent interactions between dispersal and impediments to gene flow.     

Estimation of effective population size for the long-lived darkblotched rockfish Sebastes crameri

We report the variance effective population size (Ne) in darkblotched rockfish (Sebastes crameri) utilizing the temporal method for overlapping generations, which requires a combination of age-specific demography and genetic information from cohorts. Following calculations of age-specific survival and reproductive success from fishery data, we genotyped a sample (n = 1087) comprised by 6 cohorts (from 1995 to 2000) across 7 microsatellite loci. Our Ne estimate (Ne) plus 95% confidence interval was (Ne) = 9157 [6495-12 215], showing that the breeding population number could be 3-4 orders of magnitude smaller than the census population size (N) = 24 376 210). Our estimates resemble closely those found for fishes with similar life history, suggesting that the small (Ne)/(N) ratio for S. crameri is most likely explained by a combination of high variance in reproductive success among individuals, genetic structure, and demographic perturbations such as historical fishing. Because small (Ne)/(N) ratios have been commonly associated with potential loss of genetic variation, our estimates need careful consideration in rockfish management and conservation.     

The influence of persistent individual differences and age at maturity on effective population size

Ratios of effective populations size, N(e), to census population size, N, are used as a measure of genetic drift in populations. Several life-history parameters have been shown to affect these ratios, including mating system and age at sexual maturation. Using a stochastic matrix model, we examine how different levels of persistent individual differences in mating success among males may affect N(e)/N, and how this relates to generation time. Individual differences of this type are shown to cause a lower N(e)/N ratio than would be expected when mating is independent among seasons. Examining the way in which age at maturity affects N(e)/N, we find that both the direction and magnitude of the effect depends on the survival rate of juveniles in the population. In particular, when maturation is delayed, lowered juvenile survival causes higher levels of genetic drift. In addition, predicted shifts in N(e)/N with changing age at maturity are shown to be dependent on which of the commonly used definitions of census population size, N, is employed. Our results demonstrate that patterns of mating success, as well as juvenile survival probabilities, have substantial effects on rates of genetic drift.     

Effective population size of steelhead trout: influence of variance in reproductive success, hatchery programs, and genetic compensation between life-history forms

The effective population size is influenced by many biological factors in natural populations. To evaluate their relative importance, we estimated the effective number of breeders per year (Nb) and effective population size per generation (Ne) in anadromous steelhead trout (Oncorhynchus mykiss) in the Hood River, Oregon (USA). Using demographic data and genetic parentage analysis on an almost complete sample of all adults that returned to the river over 15 years (>15,000 individuals), we estimated Nb for 13 run years and Ne for three entire generations. The results are as follows: (i) the ratio of Ne to the estimated census population size (N) was 0.17-0.40, with large variance in reproductive success among individuals being the primary cause of the reduction in Ne/N; (ii) fish from a traditional hatchery program (Htrad: nonlocal, multiple generations in a hatchery) had negative effects on Nb, not only by reducing mean reproductive success but also by increasing variance in reproductive success among breeding parents, whereas no sign of such effects was found in fish from supplementation hatchery programs (Hsupp: local, single generation in a hatchery); and (iii) Nb was relatively stable among run years, despite the widely fluctuating annual run sizes of anadromous adults. We found high levels of reproductive contribution of nonanadromous parents to anadromous offspring when anadromous run size is small, suggesting a genetic compensation between life-history forms (anadromous and nonanadromous). This is the first study showing that reproductive interaction between different life-history forms can buffer the genetic impact of fluctuating census size on Ne.     

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.     

Glossina swynnertoni (Diptera: Glossinidae): effective population size and breeding structure estimated by mitochondrial diversity

Nucleotide diversity was examined at mitochondrial COI and r16S2 loci in eight Glossina swynnertoni Austen collections from northern Tanzania and from a culture maintained by the International Atomic Energy Agency. Eighteen composite haplotypes were observed among 149 flies, two of which were common to all samples and 10 were private. Mean haplotype diversity was 0.59 and nucleotide diversity was 0.0013. There were excess singular haplotypes and mutation-drift disequilibrium suggesting that populations had experienced an earlier bottleneck and subsequent expansion. Factorial correspondence analysis showed that haplotype frequencies varied much more temporally (G ST=0.18) than spatially (G ST=0.04). The estimate of effective population size N e in Tarangire was a harmonic mean approximately 50 reproductive flies averaged over approximately 47 generations. The mean rate of gene flow was estimated to be approximately 5+/-1 reproducing females per generation but inflated because of mutation-drift disequilibrium arising from likely earlier bottlenecks.     

Fixation probability and time in subdivided populations

New alleles arising in a population by mutation ultimately are either fixed or lost. Either is possible, for both beneficial and deleterious alleles, because of stochastic changes in allele frequency due to genetic drift. Spatially structured populations differ from unstructured populations in the probability of fixation and the time that this fixation takes. Previous results have generally made many assumptions: that all demes contribute to the next generation in exact proportion to their current sizes, that new mutations are beneficial, and that new alleles have additive effects. In this article these assumptions are relaxed, allowing for an arbitrary distribution among demes of reproductive success, both beneficial and deleterious effects, and arbitrary dominance. The effects of population structure can be expressed with two summary statistics: the effective population size and a variant of Wright's F(ST). In general, the probability of fixation is strongly affected by population structure, as is the expected time to fixation or loss. Population structure changes the effective size of the species, often strongly downward; smaller effective size increases the probability of fixing deleterious alleles and decreases the probability of fixing beneficial alleles. On the other hand, population structure causes an increase in the homozygosity of alleles, which increases the probability of fixing beneficial alleles but somewhat decreases the probability of fixing deleterious alleles. The probability of fixing new beneficial alleles can be simply described by 2hs(1 - F(ST))N(e)/N(tot), where hs is the change in fitness of heterozygotes relative to the ancestral homozygote, F(ST) is a weighted version of Wright's measure of population subdivision, and N(e) and N(tot) are the effective and census sizes, respectively. These results are verified by simulation for a broad range of population structures, including the island model, the stepping-stone model, and a model with extinction and recolonization.     

Evolution of population structure in an estuarine‐dependent marine fish

Restriction site‐associated DNA (RAD) sequencing was used to characterize neutral and adaptive genetic variation among geographic samples of red drum, Sciaenops ocellatus, an estuarine‐dependent fish found in coastal waters along the southeastern coast of the United States (Atlantic) and the northern Gulf of Mexico (Gulf). Analyses of neutral and outlier loci revealed three genetically distinct regional clusters: one in the Atlantic and two in the northern Gulf. Divergence in neutral loci indicated gradual genetic change and followed a linear pattern of isolation by distance. Divergence in outlier loci was at least an order of magnitude greater than divergence in neutral loci, and divergence between the regions in the Gulf was twice that of divergence between other regions. Discordance in patterns of genetic divergence between outlier and neutral loci is consistent with the hypothesis that the former reflects adaptive responses to environmental factors that vary on regional scales, while the latter largely reflects drift processes. Differences in basic habitat, initiated by glacial retreat and perpetuated by contemporary oceanic and atmospheric forces interacting with the geomorphology of the northern Gulf, followed by selection, appear to have led to reduced gene flow among red drum across the northern Gulf, reinforcing differences accrued during isolation and resulting in continued divergence across the genome. This same dynamic also may pertain to other coastal or nearshore fishes (18 species in 14 families) where genetically or morphologically defined sister taxa occur in the three regions.     

Sibship reconstruction demonstrates the extremely low effective population size of striped bass Morone saxatilis in the Santee–Cooper system, South Carolina, USA

For organisms with great fecundity and high mortality in early life stages, such as shellfish or fishes, the need to match reproductive activity with environmental conditions conducive to spawning, fertilization, larval development and recruitment may result in extreme variance in reproductive success among individuals. The main objective of this study was to investigate evidence of large variance in the reproductive success of the striped bass Morone saxatilis in the Santee–Cooper system, South Carolina, USA. Seven microsatellite loci were analysed in 603 recruits representing three yearly cohorts from 1992 to 1994, and a group analysis was performed to identify full-sib families. Large variance in reproductive success was detected, with a few large, full-sib families contributing disproportionately to each of the cohorts. The severity of sweepstakes reproductive success varied among cohorts depending on environmentally imposed mortality. Estimations of the effective number of breeders in these long-lived fish ranged from 24 in 1992 to 44 in 1994. Furthermore, the estimated genetic effective population size ( N _e = 93) is approximately four orders of magnitude lower than estimates of adult census size ( N  =   362 000). Furthermore, the presence of large full-sib families indicates that striped bass engage in pair mating in the wild. Heterogeneity in genetic composition was also observed among cohorts, suggesting that genetically different adults contribute to different cohorts and that chance rather than fitness variation determines reproductive success.     

Effective size of subpopulations in early-run sockeye salmon Oncorhynchus nerka from Azabach'e Lake (Kamchatka): the effect of relative reproductive success of different-year cohorts

The effect of variation in reproductive success of cohorts of different year of birth (within generation) on the effective subpopulation (breeding group) size in early-run sockeye salmon Oncorhynchus nerka from Azabach'e Lake (Kamchatka). The annual variation in census size and overlapping of year classes reduced the ratio of the effective subpopulation size to the census size by 7 to 88% in different subpopulations. The total effect of the variance of reproductive success in individual years and the variance of reproductive success of different cohorts reduced the effective size/census size ratio by 68-96%.     

The effective size of mixed sexually and asexually reproducing populations

Using the transition matrix of inbreeding and coancestry coefficients, the inbreeding (N(eI)), variance (N(eV)), and asymptotic (N(e lambda)) effective sizes of mixed sexual and asexual populations are formulated in terms of asexuality rate (delta), variance of asexual (C) and sexual (K) reproductive contributions of individuals, correlation between asexual and sexual contributions (rho(ck)), selfing rate (beta), and census population size (N). The trajectory of N(eI) toward N(e lambda) changes crucially depending on delta, N, and beta, whereas that of N(eV) is rather consistent. With increasing asexuality, N(e lambda) either increases or decreases depending on C, K, and rho(ck). The parameter space in which a partially asexual population has a larger N(e lambda) than a fully sexual population is delineated. This structure is destroyed when N(1 - delta) < 1 or delta > 1 - 1/N. With such a high asexuality, tremendously many generations are required for the asymptotic size N(e lambda) to be established, and N(e lambda) is extremely large with any value of C, K, and rho(ck) because the population is dominated eventually by individuals of the same genotype and the allelic diversity within the individuals decays quite slowly. In reality, the asymptotic state would occur only occasionally, and instantaneous rather than asymptotic effective sizes should be practical when predicting evolutionary dynamics of highly asexual populations.     

Effective size of fluctuating populations with two sexes and overlapping generations

We derive formulas that can be applied to estimate the effective population size N(e) for organisms with two sexes reproducing once a year and having constant adult mean vital rates independent of age. Temporal fluctuations in population size are generated by demographic and environmental stochasticity. For populations with even sex ratio at birth, no deterministic population growth and identical mean vital rates for both sexes, the key parameter determining N(e) is simply the mean value of the demographic variance for males and females considered separately. In this case Crow and Kimura's generalization of Wright's formula for N(e) with two sexes, in terms of the effective population sizes for each sex, is applicable even for fluctuating populations with different stochasticity in vital rates for males and females. If the mean vital rates are different for the sexes then a simple linear combination of the demographic variances determines N(e), further extending Wright's formula. For long-lived species an expression is derived for N(e) involving the generation times for both sexes. In the general case with nonzero population growth and uneven sex ratio of newborns, we use the model to investigate numerically the effects of different population parameters on N(e). We also estimate the ratio of effective to actual population size in six populations of house sparrows on islands off the coast of northern Norway. This ratio showed large interisland variation because of demographic differences among the populations. Finally, we calculate how N(e) in a growing house sparrow population will change over time.     

The consequences of the variance-mean rescaling effect on effective population size

The effective population size (N_e), and the ratio between N_e and census population size (N) are often used as measures of population viability. We show that using the harmonic mean of population sizes over time – a common proxy for N_e– has some important evolutionary consequences and implications for conservation management. This stems from the fact that there is no unambiguous relationship between the arithmetic and harmonic means for populations fluctuating in size. As long as the variance of population size increases moderately with increasing arithmetic mean population size, the harmonic mean also increases. However, if the variance of population size increases more rapidly, which existing data often suggest, then the harmonic mean may actually decrease with increasing arithmetic mean. Thus maximizing N may not maximize N_e, but could instead lower the adaptive potential and hence limit the evolutionary response to environmental change. Large census size has the clear advantage of lowering demographic stochasticity, and hence extinction risk, and under certain conditions large census size also minimizes the loss of genetic variation. Consequently, maximising census size has served as a useful dogma in ecology, genetics and conservation. Nonetheless, due to the intricate relationships among N_e, population viability and the properties of population fluctuations, we suggest that this dogma should be taken only as a rule of thumb.