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Signatures of selection in natural populations adapted to chronic pollution.

Williams LM, Oleksiak MF - BMC Evol. Biol. (2008)

Bottom Line: Two outlier loci were shared between New Bedford Harbor and Elizabeth River populations, and two different loci were shared between Newark Bay and Elizabeth River populations.In total, 1% to 6% of loci are implicated as being under selection or linked to areas of the genome under selection in three F. heteroclitus populations that reside in polluted estuaries.Shared loci among polluted sites indicate that selection may be acting on multiple loci involved in adaptation, and loci shared between polluted sites potentially are involved in a generalized adaptive response.

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Affiliation: Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA. lmwillia@ncsu.edu

ABSTRACT

Background: Populations of the teleost fish Fundulus heteroclitus appear to flourish in heavily polluted and geographically separated Superfund sites. Populations from three Superfund sites (New Bedford Harbor, MA, Newark Bay, NJ, and Elizabeth River, VA) have independently evolved adaptive resistance to chemical pollutants. In these polluted populations, natural selection likely has altered allele frequencies of loci that affect fitness or that are linked to these loci. The aim of this study was to identify loci that exhibit non-neutral behavior in the F. heteroclitus genome in polluted populations versus clean reference populations.

Results: To detect signatures of natural selection and thus identify genetic bases for adaptation to anthropogenic stressors, we examined allele frequencies for many hundreds of amplified fragment length polymorphism markers among populations of F. heteroclitus. Specifically, we contrasted populations from three Superfund sites (New Bedford Harbor, MA, Newark Bay, NJ, and Elizabeth River, VA) to clean reference populations flanking the polluted sites. When empirical FST values were compared to a simulated distribution of FST values, 24 distinct outlier loci were identified among pairwise comparisons of pollutant impacted F. heteroclitus populations and both surrounding reference populations. Upon removal of all outlier loci, there was a strong correlation (R2=0.79, p<0.0001) between genetic and geographical distance. This apparently neutral evolutionary pattern was not evident when outlier loci were included (R2=0.092, p=0.0721). Two outlier loci were shared between New Bedford Harbor and Elizabeth River populations, and two different loci were shared between Newark Bay and Elizabeth River populations.

Conclusion: In total, 1% to 6% of loci are implicated as being under selection or linked to areas of the genome under selection in three F. heteroclitus populations that reside in polluted estuaries. Shared loci among polluted sites indicate that selection may be acting on multiple loci involved in adaptation, and loci shared between polluted sites potentially are involved in a generalized adaptive response.

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FST versus allele frequency values. FST values estimated from approximately 300 variable AFLP loci plotted against mean allele frequency. The solid line represents the 0.99 quantile estimated from a simulation model for each comparison. Loci shared among the same Superfund site are labeled with their primer set (letter) and number. Loci shared between Superfund sites are starred. §Shared loci included in these points are: A2, A19, A34, A56, D87, E118, E127, E137, E150, E156, C186, C194, C205, and C252. E118 also is shared between New Bedford Harbor and Elizabeth River populations.
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Figure 2: FST versus allele frequency values. FST values estimated from approximately 300 variable AFLP loci plotted against mean allele frequency. The solid line represents the 0.99 quantile estimated from a simulation model for each comparison. Loci shared among the same Superfund site are labeled with their primer set (letter) and number. Loci shared between Superfund sites are starred. §Shared loci included in these points are: A2, A19, A34, A56, D87, E118, E127, E137, E150, E156, C186, C194, C205, and C252. E118 also is shared between New Bedford Harbor and Elizabeth River populations.

Mentions: The frequency of band presence allele was calculated using the formula P = 1 - ((N - C)/N)0.5 where N equals the sample size and C is the number of individuals with the band [65]. This formula assumes Hardy-Weinberg equilibrium. However, because AFLPs are dominant markers and heterozygotes are not observed, Hardy-Weinberg equilibrium cannot be directly tested. Due to strong selection or increased mutational rates, some of the loci may not be in Hardy-Weinberg equilibrium. Though not directly comparable, microsatellites are in Hardy-Weinberg equilibrium in these F. heteroclitus populations [66]. This calculation also assumes that shared band presence or absence between two individuals is due to common evolutionary origin and not homoplasy. Pairwise FST values between populations were calculated for each locus by the method of Nei [67] with the correction of Nei and Chesser [68] for finite sample sizes, and a distribution of FST values versus allele frequency was simulated using the Winkles program ([69], Fig. 2).


Signatures of selection in natural populations adapted to chronic pollution.

Williams LM, Oleksiak MF - BMC Evol. Biol. (2008)

FST versus allele frequency values. FST values estimated from approximately 300 variable AFLP loci plotted against mean allele frequency. The solid line represents the 0.99 quantile estimated from a simulation model for each comparison. Loci shared among the same Superfund site are labeled with their primer set (letter) and number. Loci shared between Superfund sites are starred. §Shared loci included in these points are: A2, A19, A34, A56, D87, E118, E127, E137, E150, E156, C186, C194, C205, and C252. E118 also is shared between New Bedford Harbor and Elizabeth River populations.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2570689&req=5

Figure 2: FST versus allele frequency values. FST values estimated from approximately 300 variable AFLP loci plotted against mean allele frequency. The solid line represents the 0.99 quantile estimated from a simulation model for each comparison. Loci shared among the same Superfund site are labeled with their primer set (letter) and number. Loci shared between Superfund sites are starred. §Shared loci included in these points are: A2, A19, A34, A56, D87, E118, E127, E137, E150, E156, C186, C194, C205, and C252. E118 also is shared between New Bedford Harbor and Elizabeth River populations.
Mentions: The frequency of band presence allele was calculated using the formula P = 1 - ((N - C)/N)0.5 where N equals the sample size and C is the number of individuals with the band [65]. This formula assumes Hardy-Weinberg equilibrium. However, because AFLPs are dominant markers and heterozygotes are not observed, Hardy-Weinberg equilibrium cannot be directly tested. Due to strong selection or increased mutational rates, some of the loci may not be in Hardy-Weinberg equilibrium. Though not directly comparable, microsatellites are in Hardy-Weinberg equilibrium in these F. heteroclitus populations [66]. This calculation also assumes that shared band presence or absence between two individuals is due to common evolutionary origin and not homoplasy. Pairwise FST values between populations were calculated for each locus by the method of Nei [67] with the correction of Nei and Chesser [68] for finite sample sizes, and a distribution of FST values versus allele frequency was simulated using the Winkles program ([69], Fig. 2).

Bottom Line: Two outlier loci were shared between New Bedford Harbor and Elizabeth River populations, and two different loci were shared between Newark Bay and Elizabeth River populations.In total, 1% to 6% of loci are implicated as being under selection or linked to areas of the genome under selection in three F. heteroclitus populations that reside in polluted estuaries.Shared loci among polluted sites indicate that selection may be acting on multiple loci involved in adaptation, and loci shared between polluted sites potentially are involved in a generalized adaptive response.

View Article: PubMed Central - HTML - PubMed

Affiliation: Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA. lmwillia@ncsu.edu

ABSTRACT

Background: Populations of the teleost fish Fundulus heteroclitus appear to flourish in heavily polluted and geographically separated Superfund sites. Populations from three Superfund sites (New Bedford Harbor, MA, Newark Bay, NJ, and Elizabeth River, VA) have independently evolved adaptive resistance to chemical pollutants. In these polluted populations, natural selection likely has altered allele frequencies of loci that affect fitness or that are linked to these loci. The aim of this study was to identify loci that exhibit non-neutral behavior in the F. heteroclitus genome in polluted populations versus clean reference populations.

Results: To detect signatures of natural selection and thus identify genetic bases for adaptation to anthropogenic stressors, we examined allele frequencies for many hundreds of amplified fragment length polymorphism markers among populations of F. heteroclitus. Specifically, we contrasted populations from three Superfund sites (New Bedford Harbor, MA, Newark Bay, NJ, and Elizabeth River, VA) to clean reference populations flanking the polluted sites. When empirical FST values were compared to a simulated distribution of FST values, 24 distinct outlier loci were identified among pairwise comparisons of pollutant impacted F. heteroclitus populations and both surrounding reference populations. Upon removal of all outlier loci, there was a strong correlation (R2=0.79, p<0.0001) between genetic and geographical distance. This apparently neutral evolutionary pattern was not evident when outlier loci were included (R2=0.092, p=0.0721). Two outlier loci were shared between New Bedford Harbor and Elizabeth River populations, and two different loci were shared between Newark Bay and Elizabeth River populations.

Conclusion: In total, 1% to 6% of loci are implicated as being under selection or linked to areas of the genome under selection in three F. heteroclitus populations that reside in polluted estuaries. Shared loci among polluted sites indicate that selection may be acting on multiple loci involved in adaptation, and loci shared between polluted sites potentially are involved in a generalized adaptive response.

Show MeSH
Related in: MedlinePlus