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%.     

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.     

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.     

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.     

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.     

Large variance in reproductive success and the Ne/N ratio

The ratio of the effective population size to adult (or census) population size (Ne/N) is an indicator of the extent of genetic variation expected in a population. It has been suggested that this ratio may be quite low for highly fecund species in which there is a sweepstakes-like chance of reproductive success, known as the Hedgecock effect. Here I show theoretically how the ratio may be quite small when there are only a few successful breeders (Nb) and that in this case, the Ne/N ratio is approximately Nb/N. In other words, high variance in reproductive success within a generation can result in a very low effective population size in an organism with large numbers of adults and consequently a very low Ne/N ratio. This finding appears robust when there is a large proportion of families with exactly two progeny or when there is random variation in progeny numbers among these families.     

The recruitment sweepstakes has many winners: genetic evidence from the sea urchin Strongylocentrotus purpuratus

As a consequence of free spawning in the unpredictable nearshore environment, marine species with large fecundities and high pre-reproductive mortality may be subject to extreme variance in reproductive success. If the unpredictability of the ocean results in only a small subset of the adult population contributing to each larval cohort, then reproduction may be viewed as a sweepstakes, with chance events determining which adults are successful each spawning season. Such a reproductive sweepstakes scenario may partially account for large reductions in effective population sizes relative to census population sizes in marine species. We evaluated two predictions of the sweepstakes reproductive success hypothesis by testing: (1) whether sea urchin recruits contain reduced genetic variation relative to the adult population; and (2) whether cohorts of sea urchin recruits are genetically differentiated. Mitochondrial DNA sequences were collected from 283 recently settled Strongylocentrotus purpuratus recruits from four annual cohorts spanning seven years in locations throughout California. Observed haplotype numbers and haplotype diversities showed little evidence of reduced genetic variation in the recruits relative to the diversity estimated from a previously reported sample of 145 S. purpuratus adults. Different cohorts of recruits were in some cases mildly differentiated from each other. A computer simulation of sweepstakes recruitment indicates that our sampling strategy had sufficient statistical power to detect large variances in reproductive success.     

Genetic effective size is three orders of magnitude smaller than adult census size in an abundant,Estuarine-dependent marine fish (Sciaenops ocellatus)

Using eight microsatellite loci and a variety of analytical methods, we estimated genetic effective size (N(e)) of an abundant and long-lived marine fish species, the red drum (Sciaenops ocellatus), in the northern Gulf of Mexico (Gulf). The ratio N(e)/N, where short-term variance N(e) was estimated via the temporal method from shifts in allele-frequency data over four cohorts and where N reflected a current estimate of adult census size in the northern Gulf, was approximately 0.001. In an idealized population, this ratio should approximate unity. The extraordinarily low value of N(e)/N appears to arise from high variance in individual reproductive success and perhaps more importantly from variance in productivity of critical spawning and nursery habitats located in spatially discrete bays and estuaries throughout the northern Gulf. An estimate of N(e) based on a coalescent approach, which measures long-term, inbreeding effective size, was four orders of magnitude lower than the estimate of current census size, suggesting that factors presently driving N(e)/N to low values among red drum in the northern Gulf may have operated similarly in the past. Models that predict N(e)/N exclusively from demographic and life-history features will seriously overestimate N(e) if variance in reproductive success and variance in productivity among spatially discrete demes is underestimated. Our results indicate that these variances, especially variance in productivity among demes, must be large for red drum. Moreover, our study indicates that vertebrate populations with enormous adult census numbers may still be at risk relative to decline and extinction from genetic factors.     

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.     

Effective size of harvested ungulate populations

The harvest of ungulate populations is often directed against certain sex or age classes to maximize the yield in terms of biomass, number of shot animals or number of trophies. Here we examine how such directional harvest affects the effective size of the population. We parameterize an age-specific model assumed to describe the dynamics of Fennoscandian moose. Based on expressions for the demographic variance     for a small subpopulation of heterozygotes Aa bearing a rare neutral allele a , we use this model to calculate how different harvest strategies influence the effective size of the population, given that the population remains stable after harvest. We show that the annual genetic drift, determined by     , increases with decreasing harvest rate of calves and increasing sex bias in the harvest towards bulls 1 year or older. The effective population size per generation decreased with reduced harvest of calves and increased harvest of bulls 1 year or older. The magnitude of these effects depends on the age-specific pattern of variation in reproductive success, which influences the demographic variance. This shows that the choice of harvest strategy strongly affects the genetic dynamics of harvested ungulate populations.     

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.     

Sexual selection has minimal impact on effective population sizes in species with high rates of random offspring mortality: An empirical demonstration using fitness distributions

The effective population size (N_e) is a fundamental parameter in population genetics that influences the rate of loss of genetic diversity. Sexual selection has the potential to reduce N_e by causing the sex‐specific distributions of individuals that successfully reproduce to diverge. To empirically estimate the effect of sexual selection on N_e, we obtained fitness distributions for males and females from an outbred, laboratory‐adapted population of Drosophila melanogaster. We observed strong sexual selection in this population (the variance in male reproductive success was ～14 times higher than that for females), but found that sexual selection had only a modest effect on N_e, which was 75% of the census size. This occurs because the substantial random offspring mortality in this population diminishes the effects of sexual selection on N_e, a result that necessarily applies to other high fecundity species. The inclusion of this random offspring mortality creates a scaling effect that reduces the variance/mean ratios for male and female reproductive success and causes them to converge. Our results demonstrate that measuring reproductive success without considering offspring mortality can underestimate N_e and overestimate the genetic consequences of sexual selection. Similarly, comparing genetic diversity among different genomic components may fail to detect strong sexual selection.     

Seasonal changes in components of male and female reproductive success in Raphanus sativus L. (Brassicaceae)

Summary To document seasonal changes in the reproductive behavior of the perfect-flowered, self-incompatible mustard, Raphanus sativus L., we monitored individual survival, flower and fruit production among 58 individuals in a California population over six census dates (cohorts). Population size declined dramatically and mean individual levels of fruit set changed significantly between cohorts. The frequency distribution of flower and fruit production became increasingly skewed over the first four cohorts. The phenotypic maleness of individuals, a standardized measure of phenotypic gender, oscillated during the reproductive season, peaking in the third and fourth cohorts. We calculated a simple estimate of expected male reproductive success of each plant (the number of fruits sired on conspecifics); this estimate was a function of an individual's flower production and the fruit production of its potential mates in our sampled population. Mean expected male success did not differ significantly among cohorts; expected male success per flower did, however, change significantly among cohorts. Among individuals within each cohort, maternal fruit production and expected male success were both positively correlated with flower production throughout the season. Spearman rank correlation coefficients indicate that the strength of these associations, however, changed during the season. Linear regressions of transformed variables indicated that the shape of several fitness functions also changed over time. In addition, the amount of variation in maternal or expected paternal success explained by flower production declined over the first four cohorts. If typical of wild populations, these temporal changes in these functions suggest that measurements of the intensity of phenotypic selection on flower production will depend on when and how fitness is measured in natural populations.     

Variation in reproductive success and effective number of breeders in a hatchery population of steelhead trout (Oncorhynchus mykiss): examination by microsatellite-based parentage analysis

Conservation programs that release captive-bred individuals into the wild to mix with naturally produced individuals are an increasingly common method of supporting or enhancing weak or reduced populations that otherwise may not be self-sustaining. Captive and supportive breeding can be important conservation tools for species with small or declining populations; however, in the case of hatcheries producing salmonid fishes, detailed evaluation of spawning programs is rare. We examined variation in reproductive success, measured by adult offspring production, from three parental generations of hatchery-bred steelhead trout (Oncorhynchus mykiss) using an exclusion-based method of genetic parentage assignment. Reproductive success varied greatly among individuals (especially males) and was correlated with fecundity and maternal spawning date. Estimates of egg to smolt survival for the population as a whole among years ranged from 64% to 95%, marine survival ranged from 0.32% to 2.30%, and the number of adults produced per female ranged from 0 to 18 and the number of adults produced per male ranged from 0 to 32. The effective number of breeders ranged from 11% to 31% of the census population size for that brood year. These ratios fell within estimates from estimates of Ne/N in chinook (O. tshawytscha) and rainbow trout (O. mykiss) hatchery populations.     

Genetic evidence for the mating system and reproductive success of black sea bream (Acanthopagrus schlegelii)

Understanding the mating system and reproductive success of a species provides evidence for sexual selection. We examined the mating system and the reproductive success of captive adult black sea bream (Acanthopagrus schlegelii), using parentage assignment based on two microsatellites multiplex PCR systems, with 91.5% accuracy in a mixed family (29 sires, 25 dams, and 200 offspring). Based on the parentage result, we found that 93.1% of males and 100% of females participated in reproduction. A total of 79% of males and 92% of females mated with multiple partners (only 1 sire and 1 dam were monogamous), indicating that polygynandry best described the genetic mating system of black sea bream. For males, maximizing the reproductive success by multiple mating was accorded with the sexual selection theory while the material benefits hypothesis may contribute to explain the multiple mating for females. For both sexes, there was a significant correlation between mating success and reproductive success and the variance in reproductive success of males was higher than females. Variation in mating success is the greatest determinant to variation in reproductive success when the relationship is strongly positive. The opportunity for sexual selection of males was twice that of females, as well as the higher slope of the Bateman curve in males suggested that the intensity of intrasexual selection of males was higher than females. Thus, male–male competition would lead to the greater variation of mating success for males, which caused greater variation in reproductive success in males. The effective population number of breeders (N_b) was 33, and the N_b/N ratio was 0.61, slightly higher than the general ratio in polygynandrous fish populations which possibly because most individuals mated and had offspring with a low variance. The relatively high N_b contributes to the maintenance of genetic diversity in farmed black sea bream populations.     

Interannual variation in effective number of breeders and estimation of effective population size in long‐lived iteroparous lake sturgeon (Acipenser fulvescens)

Quantifying interannual variation in effective adult breeding number (N_b) and relationships between N_b, effective population size (N_e), adult census size (N) and population demographic characteristics are important to predict genetic changes in populations of conservation concern. Such relationships are rarely available for long‐lived iteroparous species like lake sturgeon (Acipenser fulvescens). We estimated annual N_b and generational N_e using genotypes from 12 microsatellite loci for lake sturgeon adults (n = 796) captured during ten spawning seasons and offspring (n = 3925) collected during larval dispersal in a closed population over 8 years. Inbreeding and variance N_b estimated using mean and variance in individual reproductive success derived from genetically identified parentage and using linkage disequilibrium (LD) were similar within and among years (interannual range of N_b across estimators: 41–205). Variance in reproductive success and unequal sex ratios reduced N_b relative to N on average 36.8% and 16.3%, respectively. Interannual variation in N_b/N ratios (0.27–0.86) resulted from stable N and low standardized variance in reproductive success due to high proportions of adults breeding and the species' polygamous mating system, despite a 40‐fold difference in annual larval production across years (437–16 417). Results indicated environmental conditions and features of the species' reproductive ecology interact to affect demographic parameters and N_b/N. Estimates of N_e based on three single‐sample estimators, including LD, approximate Bayesian computation and sibship assignment, were similar to annual estimates of N_b. Findings have important implications concerning applications of genetic monitoring in conservation planning for lake sturgeon and other species with similar life histories and mating systems.     

Conspecific reproductive success affects age of recruitment in a great cormorant, Phalacrocorax carbo sinensis, colony.

Few studies have addressed the proximate factors affecting the age at which individuals of long-lived bird species are recruited into the breeding population. We use capture-recapture analysis of resightings of 16 birth cohorts of colour-ringed great cormorants, Phalacrocorax carbo sinensis, in a Danish colony to assess the evidence for two hypotheses: conspecific attraction (earlier recruitment when the colony is large) and conspecific reproductive success (earlier recruitment following years of high breeding success). For both males and females, conspecific reproductive success was the most important covariate explaining the interannual variation in age of recruitment; colony size was also important for females. These covariates explained nearly 60% of the year-to-year variation for both sexes. The age of recruitment increased for cohorts born after 1990, and this increase was correlated with a decline in breeding success in the colony; we interpret this as an indirect and delayed density-dependent effect. Females were recruited earlier than males (mean age of recruitment for cohorts born before 1990: 2.98 years versus 3.53 years); the most plausible reason for this is a skewed sex ratio in favour of males in the adult population. Recruitment of males may thus, to some extent, be constrained by the availability of females. This study provides the first evidence that conspecific reproductive success can affect the age at which individual birds start to breed.     

Experience versus effort: what explains dynamic heterogeneity with respect to age?

Age‐related patterns of survival and reproduction have been explained by accumulated experience (‘experience hypothesis’), increased effort (‘effort hypothesis’), and intrinsic differences in phenotypes (‘selection hypothesis’). We examined the experience and effort hypotheses using a 40‐year data set in a population of Leach's storm‐petrels Oceanodroma leucorhoa, long‐lived seabirds for which the effect of phenotypic variation has been previously demonstrated. Age was quantified by time since recruitment (‘breeding age’). The best model of adult survival included a positive effect of breeding age (1, 2, 3+ years), sex (male > female), and year. Among‐individuals variation (fixed heterogeneity) accounted for 31.6% of the variance in annual reproductive success. We further examined within‐individual patterns in reproductive success (dynamic heterogeneity) in the subset of individuals with at least five breeding attempts. Three distinct phases characterized reproductive success – early increase, long asymptotic peak, late decline. No effect of early reproductive output on longevity was found, however, early success was positively correlated with lifetime reproductive success. Reproductive success was lower earlier than later in life. Among the few natally philopatric individuals in the population, age of first breeding had no effect on longevity, lifetime reproductive success, or early reproductive success. No support for the effort hypothesis was found in this population. Instead, age‐specific patterns of survival and reproduction in these birds are best explained by the experience hypothesis over and above the effect of intrinsic differences among individuals.     

On the Potential for Estimating the Effective Number of Breeders from Heterozygote-Excess in Progeny

The important parameter of effective population size is rarely estimable directly from demographic data. Indirect estimates of effective population size may be made from genetic data such as temporal variation of allelic frequencies or linkage disequilibrium in cohorts. We suggest here that an indirect estimate of the effective number of breeders might be based on the excess of heterozygosity expected in a cohort of progeny produced by a limited number of males and females. In computer simulations, heterozygote excesses for 30 unlinked loci having various numbers of alleles and allele-frequency profiles were obtained for cohorts produced by samples of breeders drawn from an age-structured population and having known variance in reproductive success and effective number. The 95% confidence limits around the estimate contained the true effective population size in 70 of 72 trials and the Spearman rank correlation of estimated and actual values was 0.991. An estimate based on heterozygote excess might have certain advantages over the previous estimates, requiring only single-locus and single-cohort data, but the sampling error among individuals and the effect of departures from random union of gametes still need to be explored.     

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.