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 (Nb ) 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 Nb 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 Nb (3-567) and identified major environmental variables affecting the two parameters. N or habitat size alone explained 47-57% of the variance in Nb , and Nb was strongly correlated with effective population size. The ratio Nb /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 Nb . We found no evidence for a consistent, directional difference between variability in Nb and/or Nb /N among small and large populations; however, small populations had more varying temporal variability in Nb /N ratios than large populations. Finally, Nb and Nb /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 Nb 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 Nb vs. N dynamics.

Retention of Ancestral Genetic Variation Across Life-Stages of an Endangered, Long-Lived Iteroparous Fish.

As with many endangered, long-lived iteroparous fishes, survival of razorback sucker depends on a management strategy that circumvents recruitment failure that results from predation by non-native fishes. In Lake Mohave, AZ-NV, management of razorback sucker centers on capture of larvae spawned in the lake, rearing them in off-channel habitats, and subsequent release ("repatriation") to the lake when adults are sufficiently large to resist predation. The effects of this strategy on genetic diversity, however, remained uncertain. After correction for differences in sample size among groups, metrics of mitochondrial DNA (mtDNA; number of haplotypes, N H , and haplotype diversity, H D ) and microsatellite (number of alleles, N A , and expected heterozygosity, H E ) diversity did not differ significantly between annual samples of repatriated adults and larval year-classes or among pooled samples of repatriated adults, larvae, and wild fish. These findings indicate that the current management program thus far maintained historical genetic variation of razorback sucker in the lake. Because effective population size, N e , is closely tied to the small census population size (N c = ~1500-3000) of razorback sucker in Lake Mohave, this population will remain at risk from genetic, as well as demographic risk of extinction unless N c is increased substantially.

Effective number of breeders provides a link between interannual variation in stream flow and individual reproductive contribution in a stream salmonid.

The effective number of breeders that give rise to a cohort (N(b)) is a promising metric for genetic monitoring of species with overlapping generations; however, more work is needed to understand factors that contribute to variation in this measure in natural populations. We tested hypotheses related to interannual variation in N(b) in two long-term studies of brook trout populations. We found no supporting evidence for our initial hypothesis that N^(b) reflects N^(c) (defined as the number of adults in a population at the time of reproduction). N^(b) was stable relative to N^(C) and did not follow trends in abundance (one stream negative, the other positive). We used stream flow estimates to test the alternative hypothesis that environmental factors constrain N(b). We observed an intermediate optimum autumn stream flow for both N^(b) (R(2) = 0.73, P = 0.02) and full-sibling family evenness (R(2) = 0.77, P = 0.01) in one population and a negative correlation between autumn stream flow and full-sib family evenness in the other population (r = -0.95, P = 0.02). Evidence for greater reproductive skew at the lowest and highest autumn flow was consistent with suboptimal conditions at flow extremes. A series of additional tests provided no supporting evidence for a related hypothesis that density-dependent reproductive success was responsible for the lack of relationship between N(b) and N(C) (so-called genetic compensation). This work provides evidence that N(b) is a useful metric of population-specific individual reproductive contribution for genetic monitoring across populations and the link we provide between stream flow and N(b) could be used to help predict population resilience to environmental change.

Multiple estimates of effective population size for monitoring a long-lived vertebrate: an application to Yellowstone grizzly bears.

Effective population size (N(e)) is a key parameter for monitoring the genetic health of threatened populations because it reflects a population's evolutionary potential and risk of extinction due to genetic stochasticity. However, its application to wildlife monitoring has been limited because it is difficult to measure in natural populations. The isolated and well-studied population of grizzly bears (Ursus arctos) in the Greater Yellowstone Ecosystem provides a rare opportunity to examine the usefulness of different N(e) estimators for monitoring. We genotyped 729 Yellowstone grizzly bears using 20 microsatellites and applied three single-sample estimators to examine contemporary trends in generation interval (GI), effective number of breeders (N(b)) and N(e) during 1982-2007. We also used multisample methods to estimate variance (N(eV)) and inbreeding N(e) (N(eI)). Single-sample estimates revealed positive trajectories, with over a fourfold increase in N(e) (≈100 to 450) and near doubling of the GI (≈8 to 14) from the 1980s to 2000s. N(eV) (240-319) and N(eI) (256) were comparable with the harmonic mean single-sample N(e) (213) over the time period. Reanalysing historical data, we found N(eV) increased from ≈80 in the 1910s-1960s to ≈280 in the contemporary population. The estimated ratio of effective to total census size (N(e) /N(c)) was stable and high (0.42-0.66) compared to previous brown bear studies. These results support independent demographic evidence for Yellowstone grizzly bear population growth since the 1980s. They further demonstrate how genetic monitoring of N(e) can complement demographic-based monitoring of N(c) and vital rates, providing a valuable tool for wildlife managers.

Use of sibling relationship reconstruction to complement traditional monitoring in fisheries management and conservation of brown trout.

Declining trends in the abundance of many fish urgently call for more efficient and informative monitoring methods that would provide necessary demographic data for the evaluation of existing conservation, restoration, and management actions. We investigated how genetic sibship reconstruction from young-of-the-year brown trout (Salmo trutta L.) juveniles provides valuable, complementary demographic information that allowed us to disentangle the effects of habitat quality and number of breeders on juvenile density. We studied restored (n = 15) and control (n = 15) spawning and nursery habitats in 16 brown trout rivers and streams over 2 consecutive years to evaluate the effectiveness of habitat restoration activities. Similar juvenile densities both in restored and control spawning and nursery grounds were observed. Similarly, no differences in the effective number of breeders, Nb(SA) , were detected between habitats, indicating that brown trout readily used recently restored spawning grounds. Only a weak relationship between the Nb(SA) and juvenile density was observed, suggesting that multiple factors affect juvenile abundance. In some areas, very low estimates of Nb(SA) were found at sites with high juvenile density, indicating that a small number of breeders can produce a high number of progeny in favorable conditions. In other sites, high Nb(SA) estimates were associated with low juvenile density, suggesting low habitat quality or lack of suitable spawning substrate in relation to available breeders. Based on these results, we recommend the incorporation of genetic sibship reconstruction to ongoing and future fish evaluation and monitoring programs to gain novel insights into local demographic and evolutionary processes relevant for fisheries management, habitat restoration, and conservation.

El Uso de la Reconstrucción de Relaciones Fraternales para Complementar el Monitoreo Tradicional en el Manejo de Pesquerías y en la Conservación de la Trucha Café Resumen Las tendencias de declinación en la abundancia de muchos peces son un llamado urgente para métodos de monitoreo más eficientes e informativos que proporcionarían los datos demográficos necesarios para la evaluación de la conservación actual, la restauración y las acciones de manejo. Investigamos cómo la reconstrucción genética del número de crías producidas por una pareja de padres de juveniles de ese mismo año de trucha café (Salmo trutta L.) proporciona información demográfica valiosa y complementaria, la cual nos permitió revelar los efectos de la calidad de hábitat y el número de reproductores sobre la densidad juvenil. Estudiamos hábitats de reproducción y crianza restaurados (n = 15) y controlados (n = 15) en 16 ríos y arroyos de trucha café a lo largo de dos años consecutivos para evaluar la efectividad de las actividades de restauración de hábitat. Se observaron densidades juveniles similares en ambos tipos de hábitat. De manera similar, no se detectaron diferencias entre los hábitats en el número efectivo de reproductores (Nb(SA) ), lo que indica que la trucha café usó de manera inmediata y reciente los hábitats de reproducción restaurados. Sólo se observó una relación débil entre el Nb(SA) y la densidad juvenil, lo que sugiere que múltiples factores afectan a la abundancia juvenil. En algunas áreas, se encontraron estimados muy bajos de Nb(SA) en sitios con una alta densidad juvenil, lo que indica que un pequeño número de reproductores puede producir un alto número de descendencia en condiciones favorables. En otros sitios, los estimados altos de Nb(SA) estuvieron asociados con una baja densidad juvenil, lo que sugiere que una baja calidad de hábitat o la falta de un sustrato adecuado para la reproducción en relación con los reproductores disponibles. Con base en estos resultados, recomendamos la incorporación de esta reconstrucción genética a la evaluación actual y futura de peces y a los programas de monitoreo para obtener percepciones novedosas de los procesos demográficos y evolutivos relevantes para el manejo de pesqueras, restauración de hábitat y conservación.

Alternative life-history strategy contributions to effective population size in a naturally spawning salmon population.

Alternative life-history tactics are predicted to affect within-population genetic processes but have received little attention. For example, the impact of precocious males on effective population size (N e) has not been quantified directly in Pacific salmon Oncorhynchus spp., even though they can make up a large percentage of the total male spawners. We investigated the contribution of precocial males ("jacks") to N e in a naturally spawning population of Coho Salmon O. kisutch from the Auke Creek watershed in Juneau, Alaska. Mature adults that returned from 2009 to 2019 (~8000 individuals) were genotyped at 259 single-nucleotide polymorphism (SNP) loci for parentage analysis. We used demographic and genetic methods to estimate the effective number of breeders per year (N b). Jack contribution to N b was assessed by comparing values of N b calculated with and without jacks and their offspring. Over a range of N b values (108-406), the average jack contribution to N b from 2009 to 2015 was 12.9% (SE = 3.8%). Jacks consistently made up over 20% of the total male spawners. The presence of jacks did not seem to influence N b/N. The linkage disequilibrium N e estimate was lower than the demographic estimate, possibly due to immigration effects on population genetic processes: based on external marks and parentage data, we estimated that immigrant spawners produced 4.5% of all returning offspring. Our results demonstrate that jacks can influence N b and N e and can make a substantial contribution to population dynamics and conservation of threatened stocks.

Effective number of white shark (Carcharodon carcharias, Linnaeus) breeders is stable over four successive years in the population adjacent to eastern Australia and New Zealand.

Population size is a central parameter for conservation; however, monitoring abundance is often problematic for threatened marine species. Despite substantial investment in research, many marine species remain data-poor presenting barriers to the evaluation of conservation management outcomes and the modeling of future solutions. Such is the case for the white shark (Carcharodon carcharias), a highly mobile apex predator for whom recent and substantial population declines have been recorded in many globally distributed populations. Here, we estimate the effective number of breeders that successfully contribute offspring in one reproductive cycle (Nb) to provide a snapshot of recent reproductive effort in an east Australian-New Zealand population of white shark. Nb was estimated over four consecutive age cohorts (2010, 2011, 2012, and 2013) using two genetic estimators (linkage disequilibrium; LD and sibship assignment; SA) based on genetic data derived from two types of genetic markers (single nucleotide polymorphisms; SNPs and microsatellite loci). While estimates of Nb using different marker types produced comparable estimates, microsatellite loci were the least precise. The LD and SA estimates of Nb within cohorts using SNPs were comparable; for example, the 2013 age cohort Nb(SA) was 289 (95% CI 200-461) and Nb(LD) was 208.5 (95% CI 116.4-712.7). We show that over the time period studied, Nb was stable and ranged between 206.1 (SD ± 45.9) and 252.0 (SD ± 46.7) per year using a combined estimate of Nb(LD+SA) from SNP loci. In addition, a simulation approach showed that in this population the effective population size (Ne) per generation can be expected to be larger than Nb per reproductive cycle. This study demonstrates how breeding population size can be monitored over time to provide insight into the effectiveness of recovery and conservation measures for the white shark, where the methods described here may be applicable to other data-poor species of conservation concern.

Keeping things local: Subpopulation Nb and Ne in a stream network with partial barriers to fish migration.

For organisms with overlapping generations that occur in metapopulations, uncertainty remains regarding the spatiotemporal scale of inference of estimates of the effective number of breeders (N^b) and whether these estimates can be used to predict generational Ne. We conducted a series of tests of the spatiotemporal scale of inference of estimates of Nb in nine consecutive cohorts within a long-term study of brook trout (Salvelinus fontinalis). We also tested a recently developed approach to estimate generational Ne from N^b and compared this to an alternative approach for estimating N^e that also accounts for age structure. Multiple lines of evidence were consistent with N^b corresponding to the local (subpopulation) spatial scale and the cohort-specific temporal scale. We found that at least four consecutive cohort-specific estimates of N^b were necessary to obtain reliable estimates of harmonic mean N^b for a subpopulation. Generational N^e derived from cohort-specific N^b was within 7%-50% of an alternative approach to obtain N^e, suggesting some population specificity for concordance between approaches. Our results regarding the spatiotemporal scale of inference for Nb should apply broadly to many taxa that exhibit overlapping generations and metapopulation structure and point to promising avenues for using cohort-specific N^b for local-scale genetic monitoring.

Effects of overlapping generations on linkage disequilibrium estimates of effective population size.

Use of single-sample genetic methods to estimate effective population size has skyrocketed in recent years. Although the underlying models assume discrete generations, they are widely applied to age-structured species. We simulated genetic data for 21 iteroparous animal and plant species to evaluate two untested hypotheses regarding performance of the single-sample method based on linkage disequilibrium (LD): (1) estimates based on single-cohort samples reflect the effective number of breeders in one reproductive cycle (Nb), and (2) mixed-age samples reflect the effective size per generation (Ne). We calculated true Ne and Nb, using the model species' vital rates, and verified these with individual-based simulations. We show that single-cohort samples should be equally influenced by Nb and Ne and confirm this with simulated results: [Formula: see text] was a linear (r(2) = 0.98) function of the harmonic mean of Ne and Nb. We provide a quantitative bias correction for raw [Formula: see text] based on the ratio Nb/Ne, which can be estimated from two or three simple life history traits. Bias-adjusted estimates were within 5% of true Nb for all 21 study species and proved robust when challenged with new data. Mixed-age adult samples produced downwardly biased estimates in all species, which we attribute to a two-locus Wahlund effect (mixture LD) caused by combining parents from different cohorts in a single sample. Results from this study will facilitate interpretation of rapidly accumulating genetic estimates in terms of both Ne (which influences long-term evolutionary processes) and Nb (which is more important for understanding eco-evolutionary dynamics and mating systems).

Time-series analysis reveals genetic responses to intensive management of razorback sucker (Xyrauchen texanus).

Time-series analysis is used widely in ecology to study complex phenomena and may have considerable potential to clarify relationships of genetic and demographic processes in natural and exploited populations. We explored the utility of this approach to evaluate population responses to management in razorback sucker, a long-lived and fecund, but declining freshwater fish species. A core population in Lake Mohave (Arizona-Nevada, USA) has experienced no natural recruitment for decades and is maintained by harvesting naturally produced larvae from the lake, rearing them in protective custody, and repatriating them at sizes less vulnerable to predation. Analyses of mtDNA and 15 microsatellites characterized for sequential larval cohorts collected over a 15-year time series revealed no changes in geographic structuring but indicated significant increase in mtDNA diversity for the entire population over time. Likewise, ratios of annual effective breeders to annual census size (N b /N a) increased significantly despite sevenfold reduction of N a. These results indicated that conservation actions diminished near-term extinction risk due to genetic factors and should now focus on increasing numbers of fish in Lake Mohave to ameliorate longer-term risks. More generally, time-series analysis permitted robust testing of trends in genetic diversity, despite low precision of some metrics.

Alternative reproductive tactics increase effective population size and decrease inbreeding in wild Atlantic salmon.

While nonanadromous males (stream-resident and/or mature male parr) contribute to reproduction in anadromous salmonids, little is known about their impacts on key population genetic parameters. Here, we evaluated the contribution of Atlantic salmon mature male parr to the effective number of breeders (Nb) using both demographic (variance in reproductive success) and genetic (linkage disequilibrium) methods, the number of alleles, and the relatedness among breeders. We used a recently published pedigree reconstruction of a wild anadromous Atlantic salmon population in which 2548 fry born in 2010 were assigned parentage to 144 anadromous female and 101 anadromous females that returned to the river to spawn in 2009 and to 462 mature male parr. Demographic and genetic methods revealed that mature male parr increased population Nb by 1.79 and 1.85 times, respectively. Moreover, mature male parr boosted the number of alleles found among progenies. Finally, mature male parr were in average less related to anadromous females than were anadromous males, likely because of asynchronous sexual maturation between mature male parr and anadromous fish of a given cohort. By increasing Nb and allelic richness, and by decreasing inbreeding, the reproductive contribution of mature male parr has important evolutionary and conservation implications for declining Atlantic salmon populations.

Linkage disequilibrium and effective population size when generations overlap.

Estimates of effective population size are critical for species of conservation concern. Genetic datasets can be used to provide robust estimates of this important parameter. However, the methods used to obtain these estimates assume that generations are discrete. We used simulated data to assess the influences of overlapping generations on the estimates of effective size provided by the linkage disequilibrium (LD) method. Our simulations focus on two factors: the degree of reproductive skew exhibited by the focal species and the generation time, without considering sample size or the level of polymorphism at marker loci. In situations where a majority of reproduction is achieved by a small fraction of the population, the effective number of breeders can be much smaller than the per-generation effective population size. The LD in samples of newborns can provide estimates of the former size, while our results indicate that the latter size is best estimated using random samples of reproductively mature adults. Using samples of adults, the downwards bias was less than approximately 15% across our simulated life histories. As noted in previous assessments, precision of the estimate depends on the magnitude of effective size itself, with greater precision achieved for small populations.

Estimation of effective number of breeders from molecular coancestry of single cohort sample.

The effective population size, N e, is an important parameter in population genetics and conservation biology. It is, however, difficult to directly estimate N e from demographic data in many wild species. Alternatively, the use of genetic data has received much attention in recent years. In the present study, I propose a new method for estimating the effective number of breeders N eb from a parameter of allele sharing (molecular coancestry) among sampled progeny. The bias and confidence interval of the new estimator are compared with those from a published method, i.e. the heterozygote-excess method, using computer simulation. Two population models are simulated; the noninbred population that consists of noninbred and nonrelated parents and the inbred population that is composed of inbred and related parents. Both methods give essentially unbiased estimates of N eb when applied to the noninbred population. In the inbred population, the proposed method gives a downward biased estimate, but the confidence interval is remarkably narrowed compared with that in the noninbred population. Estimate from the heterozygote-excess method is nearly unbiased in the inbred population, but suffers from a larger confidence interval. By combining the estimates from the two methods as a harmonic mean, the reliability is remarkably improved.