Gene flow and the restoration of genetic diversity in a fluctuating collared pika (Ochotona collaris) population.

J. M. Zgurski*a, D. S. Hika

Journal: Conservation Genetics

aDepartment of Biological Sciences, University of Alberta, Edmonton, AB, Canada

*Corresponding author:

Potential for a Genetic Bottleneck

The program Bottleneck (Piry et al. 1999) was used to determine if the population displayed a genetic signature of having gone through a bottleneck (decrease in Ne) during the study period. Populations that have undergone a recent decrease in Ne generally display an excess of expected heterozygosity (He) compared to the heterozygosity expected under drift-mutation equilibrium (Heq, Neiet al. 1975; Maruyama andFuerst 1985). Here, a sign test and a Wilcoxon signed-rank test were used to determine if the collared pika population displayed an excess of He compared to Heq. To generate the distribution of Heq for the population in each separate year, 1000 iterations were used with a two-phase model of microsatellite mutation. This model combines the infinite alleles model and the single-step mutation model (Di Renzo et al. 1994). As recommended by Piryet al. (1999), 95% of the mutations were set as single-step and 5% were set as multi-step, with a variance of 12 for the multi-step mutations.

The mode shift test, as described in Luikartet al.(1998), was used to determine if the distribution of allele frequencies in the population was characteristic of a population that has gone through a bottleneck. A population in mutation-drift equilibrium will have a large proportion of alleles present at a low frequency (<0.1) (Luikartet al.1998), and alleles at a low frequency are expected to be more common than alleles present at an intermediate frequency, regardless of the mutation mode (Nei et al. 1976). After a bottleneck, there is often a shift in allele frequency distribution towards more alleles being present at an intermediate frequency than at a low frequency (Luikartet al. 1998).

Genetic Bottleneck – Results

As indicated by a Wilcoxon signed rank test, there was no evidence for an excess of He in any year throughout the study (Table S1). The sign test also failed to indicate that there were more loci with a heterozygosity excess than a heterozygosity deficit. In three years (1998, 2006 and 2007), there were significantly more loci with a heterozygosity deficit than excess (ten loci with a deficit and five with excess, Table S1). The mode shift test indicated that the distribution of allele frequencies fitted the normal “L-shaped” distribution expected from a population in mutation-drift equilibrium (Table S1).

Genetic Bottleneck – Discussion

The pika population declined sharply in 2000, and increased during 2001 and 2002, only to decline again in 2003. After 2003, the population increased and stayed relatively high for the remainder of the study period (Table 1). The observed heterozygosities did not decline in response to the population decline, but the mean number of alleles per locus in the population declined in 2000 (Table 1). However, this loss was temporary, and by 2008, but the mean number of alleles per locus was higher than it was at the beginning of the study (Table 1). None of the tests used to detect a genetic signature of a bottleneck indicated that a reduction had occurred (see supplementary material), although there was a drop in the average number of alleles per locus from 1999 to 2000 (Table 1).

Common bottleneck-detection techniques, such as those used in this paper, often fail to detect bottlenecks because these methods lack statistical power for the population sizes typically used to detect bottlenecks (Peery et al. 2012). However, the majority of pikas present in the study population were caught and genotyped, and our study extended over a decade. We documented increases in allele number after population declines, so the failure of bottleneck detection methods to detect a bottleneck is more likely due to the arrival of immigrants. The population is not completely isolated from adjacent valleys, so dispersal plays a large role in maintaining the genetic diversity of this population.

Genetic signatures of bottlenecks can be difficult to detect in populations of lagomorphs or rodents because they are rarely sufficiently isolated to completely prevent gene flow among populations. For example, a population of banner-tailed kangaroo rats also showed none of the genetic signatures of a bottleneck, despite having been recently through one (Busch et al. 2007). Mark-recapture studies of the same kangaroo rat population showed that individuals have low dispersal ranges and that >80% of individuals remained within 100 m of their birthplace (Waseret al. 2006). Even so, migration was the most likely explanation for the failure of several methods to detect the allele frequency distortions typically associated with a bottleneck (Busch et al. 2007). Although mark-recapture analyses indicated that migration among populations of kangaroo rats was unlikely, genetic parentage analyses documented cases of precapture dispersal in juveniles (Waseret al. 2006).

References

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Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238-247

Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675-689

Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution29:1-10

Nei M, Chakraborty R, Fuerst PA (1976) Infinite allele model with varying mutation rate. P NatlAcadSci USA73:4164-4168

Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vásquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403-3418

Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data.J Hered 90:502-503

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Table S1 Results from three bottleneck detection methods: Wilcoxon signed-rank test, sign test, and mode shift test, as implemented by BOTTLENECK (Piryet al. 1999). Hdef = Heterozygote deficiency. Hexc = Heterozygote excess. Hdef:Hexc: ratio of loci that display a heterozygote deficiency to loci that display a heterozygote excess.

Year / P (one tail), Wilcoxon signed-rank test / Sign Test / Expected No. of Loci with Hexc / Hdef:Hexc / Evidence for
Mode Shift
1998 / 0.98 / 0.047 / 8.70 / 10:5 / No
1999 / 0.64 / 0.43 / 8.82 / 7:8 / No
2000 / 0.28 / 0.45 / 8.73 / 7:8 / No
2001 / 0.72 / 0.12 / 8.78 / 9:6 / No
2002 / 0.72 / 0.24 / 8.80 / 8:7 / No
2003 / 0.74 / 0.25 / 8.77 / 8:7 / No
2004 / 0.81 / 0.13 / 8.68 / 9:6 / No
2005 / 0.90 / 0.13 / 8.68 / 9:6 / No
2006 / 0.98 / 0.048 / 8.69 / 10:5 / No
2007 / 0.91 / 0.045 / 8.75 / 10:5 / No
2008 / 0.64 / 0.26 / 8.72 / 8:7 / No
2009 / 0.90 / 0.11 / 8.87 / 9:6 / No