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Drift by drift: effective population size is limited by advection.

Wares JP, Pringle JM - BMC Evol. Biol. (2008)

Bottom Line: Genetic estimates of effective population size often generate surprising results, including dramatically low ratios of effective population size to census size.This is particularly true for many marine species, and this effect has been associated with hypotheses of "sweepstakes" reproduction and selective hitchhiking.This result leads to predictions about the maintenance of diversity in advective systems, and complements the "sweepstakes" hypothesis and other hypotheses proposed to explain cases of low allelic diversity in species with high fecundity.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Genetics, University of Georgia, Life Science Building, Athens, Georgia 30602, USA. jpwares@uga.edu

ABSTRACT

Background: Genetic estimates of effective population size often generate surprising results, including dramatically low ratios of effective population size to census size. This is particularly true for many marine species, and this effect has been associated with hypotheses of "sweepstakes" reproduction and selective hitchhiking.

Results: Here we show that in advective environments such as oceans and rivers, the mean asymmetric transport of passively dispersed reproductive propagules will act to limit the effective population size in species with a drifting developmental stage. As advection increases, effective population size becomes decoupled from census size as the persistence of novel genetic lineages is restricted to those that arise in a small upstream portion of the species domain.

Conclusion: This result leads to predictions about the maintenance of diversity in advective systems, and complements the "sweepstakes" hypothesis and other hypotheses proposed to explain cases of low allelic diversity in species with high fecundity. We describe the spatial extent of the species domain in which novel allelic diversity will be retained, thus determining how large an appropriately placed marine reserve must be to allow the persistence of endemic allelic diversity.

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(Thick Black Line) Estimate of Ne from equation (2). (Dashed Thin Lines) Census population in domain. The squares (□) are for a domain 1024 km in size, the circles (○) are for a domain 4096 km in size, and the diamonds (◇) for a domain 16384 km in size. (Solid Lines) Estimates of Ne from a numerical model with varying Ladv and a constant Ldiff of 200 km. For the purposes of simulation, the carrying capacity of the domain is about 0.5 individuals per kilometer.
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Figure 3: (Thick Black Line) Estimate of Ne from equation (2). (Dashed Thin Lines) Census population in domain. The squares (□) are for a domain 1024 km in size, the circles (○) are for a domain 4096 km in size, and the diamonds (◇) for a domain 16384 km in size. (Solid Lines) Estimates of Ne from a numerical model with varying Ladv and a constant Ldiff of 200 km. For the purposes of simulation, the carrying capacity of the domain is about 0.5 individuals per kilometer.

Mentions: To determine Ne as a function of Ladv and Ldiff, we calculate the inbreeding effective population size Ne [28] given the mean lifetime of a novel allele in the system. We initialize the model with two alleles, each randomly distributed and each comprising 50% of the population. The neutral time to fixation in such a model will be 2.7 Ne [21], and so we estimate Ne from the average fixation time of 100 model runs. In Figure 3, we run the model in three domains of sizes Ldomain = 103, 4 × 103, and 1.6 × 104 km. In each domain, we fix Ldiff to 200 km, and vary Ladv from 0 to 110km, and compare the estimated Ne from (2) to the estimation from fixation time in an upstream region of the model Lreten in size. Once there is fixation in this upstream region, the allele fixes rapidly in the rest of the species domain in approximately Ldomain/Ladv generations. When the size of the domain is less than Lreten in extent, Ne is limited to the population census size (figure 3). Thus when Ladv is small, Ne is nearly equal to the census population of the entire population, though somewhat smaller due to loss of larvae from the edges of the domain caused by stochastic larval transport. When the domain size is greater than Lreten, eq. (2) captures the variability of Ne with Ladv very well, capturing the several order of magnitude decline in Ne with increasing Ladv. As mentioned above, the estimate of Ne from (2) is, for most values of Ladv, very much smaller than – and not dependent upon – the census population size. When the model is re-run with Laplace's dispersal kernel, the results shown in Figure 3 remain unchanged (not shown), suggesting that these results are not very sensitive to the kurtosis of the dispersal kernel.


Drift by drift: effective population size is limited by advection.

Wares JP, Pringle JM - BMC Evol. Biol. (2008)

(Thick Black Line) Estimate of Ne from equation (2). (Dashed Thin Lines) Census population in domain. The squares (□) are for a domain 1024 km in size, the circles (○) are for a domain 4096 km in size, and the diamonds (◇) for a domain 16384 km in size. (Solid Lines) Estimates of Ne from a numerical model with varying Ladv and a constant Ldiff of 200 km. For the purposes of simulation, the carrying capacity of the domain is about 0.5 individuals per kilometer.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2536672&req=5

Figure 3: (Thick Black Line) Estimate of Ne from equation (2). (Dashed Thin Lines) Census population in domain. The squares (□) are for a domain 1024 km in size, the circles (○) are for a domain 4096 km in size, and the diamonds (◇) for a domain 16384 km in size. (Solid Lines) Estimates of Ne from a numerical model with varying Ladv and a constant Ldiff of 200 km. For the purposes of simulation, the carrying capacity of the domain is about 0.5 individuals per kilometer.
Mentions: To determine Ne as a function of Ladv and Ldiff, we calculate the inbreeding effective population size Ne [28] given the mean lifetime of a novel allele in the system. We initialize the model with two alleles, each randomly distributed and each comprising 50% of the population. The neutral time to fixation in such a model will be 2.7 Ne [21], and so we estimate Ne from the average fixation time of 100 model runs. In Figure 3, we run the model in three domains of sizes Ldomain = 103, 4 × 103, and 1.6 × 104 km. In each domain, we fix Ldiff to 200 km, and vary Ladv from 0 to 110km, and compare the estimated Ne from (2) to the estimation from fixation time in an upstream region of the model Lreten in size. Once there is fixation in this upstream region, the allele fixes rapidly in the rest of the species domain in approximately Ldomain/Ladv generations. When the size of the domain is less than Lreten in extent, Ne is limited to the population census size (figure 3). Thus when Ladv is small, Ne is nearly equal to the census population of the entire population, though somewhat smaller due to loss of larvae from the edges of the domain caused by stochastic larval transport. When the domain size is greater than Lreten, eq. (2) captures the variability of Ne with Ladv very well, capturing the several order of magnitude decline in Ne with increasing Ladv. As mentioned above, the estimate of Ne from (2) is, for most values of Ladv, very much smaller than – and not dependent upon – the census population size. When the model is re-run with Laplace's dispersal kernel, the results shown in Figure 3 remain unchanged (not shown), suggesting that these results are not very sensitive to the kurtosis of the dispersal kernel.

Bottom Line: Genetic estimates of effective population size often generate surprising results, including dramatically low ratios of effective population size to census size.This is particularly true for many marine species, and this effect has been associated with hypotheses of "sweepstakes" reproduction and selective hitchhiking.This result leads to predictions about the maintenance of diversity in advective systems, and complements the "sweepstakes" hypothesis and other hypotheses proposed to explain cases of low allelic diversity in species with high fecundity.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Genetics, University of Georgia, Life Science Building, Athens, Georgia 30602, USA. jpwares@uga.edu

ABSTRACT

Background: Genetic estimates of effective population size often generate surprising results, including dramatically low ratios of effective population size to census size. This is particularly true for many marine species, and this effect has been associated with hypotheses of "sweepstakes" reproduction and selective hitchhiking.

Results: Here we show that in advective environments such as oceans and rivers, the mean asymmetric transport of passively dispersed reproductive propagules will act to limit the effective population size in species with a drifting developmental stage. As advection increases, effective population size becomes decoupled from census size as the persistence of novel genetic lineages is restricted to those that arise in a small upstream portion of the species domain.

Conclusion: This result leads to predictions about the maintenance of diversity in advective systems, and complements the "sweepstakes" hypothesis and other hypotheses proposed to explain cases of low allelic diversity in species with high fecundity. We describe the spatial extent of the species domain in which novel allelic diversity will be retained, thus determining how large an appropriately placed marine reserve must be to allow the persistence of endemic allelic diversity.

Show MeSH