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Rapid fixation of non-native alleles revealed by genome-wide SNP analysis of hybrid tiger salamanders.

Fitzpatrick BM, Johnson JR, Kump DK, Shaffer HB, Smith JJ, Voss SR - BMC Evol. Biol. (2009)

Bottom Line: Another marker (GNAT1) showed consistent heterozygote deficits in the wild, and this marker was associated with embryonic mortality in laboratory F2's.Other deviations from equilibrium expectations were idiosyncratic among breeding ponds, consistent with highly stochastic demographic effects.Introgression of a few, strongly selected introduced alleles should not necessarily affect the conservation status of California Tiger Salamanders, but suggests that genetically pure populations of this endangered species will be difficult to maintain.

View Article: PubMed Central - HTML - PubMed

Affiliation: Ecology & Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA. benfitz@utk.edu

ABSTRACT

Background: Hybrid zones represent valuable opportunities to observe evolution in systems that are unusually dynamic and where the potential for the origin of novelty and rapid adaptation co-occur with the potential for dysfunction. Recently initiated hybrid zones are particularly exciting evolutionary experiments because ongoing natural selection on novel genetic combinations can be studied in ecological time. Moreover, when hybrid zones involve native and introduced species, complex genetic patterns present important challenges for conservation policy. To assess variation of admixture dynamics, we scored a large panel of markers in five wild hybrid populations formed when Barred Tiger Salamanders were introduced into the range of California Tiger Salamanders.

Results: At three of 64 markers, introduced alleles have largely displaced native alleles within the hybrid populations. Another marker (GNAT1) showed consistent heterozygote deficits in the wild, and this marker was associated with embryonic mortality in laboratory F2's. Other deviations from equilibrium expectations were idiosyncratic among breeding ponds, consistent with highly stochastic demographic effects.

Conclusion: While most markers retain native and introduced alleles in expected proportions, strong selection appears to be eliminating native alleles at a smaller set of loci. Such rapid fixation of alleles is detectable only in recently formed hybrid zones, though it might be representative of dynamics that frequently occur in nature. These results underscore the variable and mosaic nature of hybrid genomes and illustrate the potency of recombination and selection in promoting variable, and often unpredictable genetic outcomes. Introgression of a few, strongly selected introduced alleles should not necessarily affect the conservation status of California Tiger Salamanders, but suggests that genetically pure populations of this endangered species will be difficult to maintain.

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Allele frequencies. Frequencies of introduced alleles by position in the Ambystoma linkage map [36] and by study pond: (A) Bluestone, (B) Melindy, (C) Pond H, (D) Sycamore, (E) Toro. Red points are markers (from left to right) E23C06, E06E11, and E12C11. Vertical dashed lines separate linkage groups, which are plotted end to end from largest to smallest [36]. The last marker is the mtDNA marker, placed arbitrarily at the end of the linkage map.
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Figure 2: Allele frequencies. Frequencies of introduced alleles by position in the Ambystoma linkage map [36] and by study pond: (A) Bluestone, (B) Melindy, (C) Pond H, (D) Sycamore, (E) Toro. Red points are markers (from left to right) E23C06, E06E11, and E12C11. Vertical dashed lines separate linkage groups, which are plotted end to end from largest to smallest [36]. The last marker is the mtDNA marker, placed arbitrarily at the end of the linkage map.

Mentions: The five ponds vary in their level of genetic invasion, from Melindy (average introduced allele frequency = 0.095) to Pond H (0.621), and most of the 64 markers frequencies fell within their predicted population variance (Figure 2, Table 2). In contrast, markers E06E11, E12C11, and E23C06 had consistently high frequencies of introduced alleles, with E23C06 fixed for introduced alleles in all samples (Figure 2, Table S1 [see Additional file 1]). Unconditionally beneficial alleles are expected to move rapidly toward fixation in hybrid populations. As a result, the distribution of allele frequencies would be distorted relative to its expectation if genetic drift alone were responsible for allele frequency changes subsequent to admixture [30]. Long's [30] test for heterogeneity of admixture rejects the hypothesis of neutral admixture when the tails of the empirical distribution of admixture estimates are thicker than expected from the variance. Applying Long's heterogeneity test to our data, we reject neutral admixture in all five study ponds (Table 2). Furthermore, the same markers are consistently responsible for the deviations in all five study ponds (Table S1 [see Additional file 1]). Dropping the three markers with the most extreme allele frequencies and recalculating Long's test yields a non-significant result for all ponds except Toro, which required additionally dropping the mtDNA marker to achieve adequate goodness-of-fit (P > 0.05) to the neutral admixture model (Table 2).


Rapid fixation of non-native alleles revealed by genome-wide SNP analysis of hybrid tiger salamanders.

Fitzpatrick BM, Johnson JR, Kump DK, Shaffer HB, Smith JJ, Voss SR - BMC Evol. Biol. (2009)

Allele frequencies. Frequencies of introduced alleles by position in the Ambystoma linkage map [36] and by study pond: (A) Bluestone, (B) Melindy, (C) Pond H, (D) Sycamore, (E) Toro. Red points are markers (from left to right) E23C06, E06E11, and E12C11. Vertical dashed lines separate linkage groups, which are plotted end to end from largest to smallest [36]. The last marker is the mtDNA marker, placed arbitrarily at the end of the linkage map.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2724412&req=5

Figure 2: Allele frequencies. Frequencies of introduced alleles by position in the Ambystoma linkage map [36] and by study pond: (A) Bluestone, (B) Melindy, (C) Pond H, (D) Sycamore, (E) Toro. Red points are markers (from left to right) E23C06, E06E11, and E12C11. Vertical dashed lines separate linkage groups, which are plotted end to end from largest to smallest [36]. The last marker is the mtDNA marker, placed arbitrarily at the end of the linkage map.
Mentions: The five ponds vary in their level of genetic invasion, from Melindy (average introduced allele frequency = 0.095) to Pond H (0.621), and most of the 64 markers frequencies fell within their predicted population variance (Figure 2, Table 2). In contrast, markers E06E11, E12C11, and E23C06 had consistently high frequencies of introduced alleles, with E23C06 fixed for introduced alleles in all samples (Figure 2, Table S1 [see Additional file 1]). Unconditionally beneficial alleles are expected to move rapidly toward fixation in hybrid populations. As a result, the distribution of allele frequencies would be distorted relative to its expectation if genetic drift alone were responsible for allele frequency changes subsequent to admixture [30]. Long's [30] test for heterogeneity of admixture rejects the hypothesis of neutral admixture when the tails of the empirical distribution of admixture estimates are thicker than expected from the variance. Applying Long's heterogeneity test to our data, we reject neutral admixture in all five study ponds (Table 2). Furthermore, the same markers are consistently responsible for the deviations in all five study ponds (Table S1 [see Additional file 1]). Dropping the three markers with the most extreme allele frequencies and recalculating Long's test yields a non-significant result for all ponds except Toro, which required additionally dropping the mtDNA marker to achieve adequate goodness-of-fit (P > 0.05) to the neutral admixture model (Table 2).

Bottom Line: Another marker (GNAT1) showed consistent heterozygote deficits in the wild, and this marker was associated with embryonic mortality in laboratory F2's.Other deviations from equilibrium expectations were idiosyncratic among breeding ponds, consistent with highly stochastic demographic effects.Introgression of a few, strongly selected introduced alleles should not necessarily affect the conservation status of California Tiger Salamanders, but suggests that genetically pure populations of this endangered species will be difficult to maintain.

View Article: PubMed Central - HTML - PubMed

Affiliation: Ecology & Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA. benfitz@utk.edu

ABSTRACT

Background: Hybrid zones represent valuable opportunities to observe evolution in systems that are unusually dynamic and where the potential for the origin of novelty and rapid adaptation co-occur with the potential for dysfunction. Recently initiated hybrid zones are particularly exciting evolutionary experiments because ongoing natural selection on novel genetic combinations can be studied in ecological time. Moreover, when hybrid zones involve native and introduced species, complex genetic patterns present important challenges for conservation policy. To assess variation of admixture dynamics, we scored a large panel of markers in five wild hybrid populations formed when Barred Tiger Salamanders were introduced into the range of California Tiger Salamanders.

Results: At three of 64 markers, introduced alleles have largely displaced native alleles within the hybrid populations. Another marker (GNAT1) showed consistent heterozygote deficits in the wild, and this marker was associated with embryonic mortality in laboratory F2's. Other deviations from equilibrium expectations were idiosyncratic among breeding ponds, consistent with highly stochastic demographic effects.

Conclusion: While most markers retain native and introduced alleles in expected proportions, strong selection appears to be eliminating native alleles at a smaller set of loci. Such rapid fixation of alleles is detectable only in recently formed hybrid zones, though it might be representative of dynamics that frequently occur in nature. These results underscore the variable and mosaic nature of hybrid genomes and illustrate the potency of recombination and selection in promoting variable, and often unpredictable genetic outcomes. Introgression of a few, strongly selected introduced alleles should not necessarily affect the conservation status of California Tiger Salamanders, but suggests that genetically pure populations of this endangered species will be difficult to maintain.

Show MeSH