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Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era.

Gagnaire PA, Broquet T, Aurelle D, Viard F, Souissi A, Bonhomme F, Arnaud-Haond S, Bierne N - Evol Appl (2015)

Bottom Line: We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples.We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally.We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

View Article: PubMed Central - PubMed

Affiliation: Université de Montpellier Montpellier, France ; CNRS - Institut des Sciences de l'Evolution, UMR 5554 UM-CNRS-IRD-EPHE, Station Méditerranéenne de l'Environnement Littoral Sète, France.

ABSTRACT
Estimating the rate of exchange of individuals among populations is a central concern to evolutionary ecology and its applications to conservation and management. For instance, the efficiency of protected areas in sustaining locally endangered populations and ecosystems depends on reserve network connectivity. The population genetics theory offers a powerful framework for estimating dispersal distances and migration rates from molecular data. In the marine realm, however, decades of molecular studies have met limited success in inferring genetic connectivity, due to the frequent lack of spatial genetic structure in species exhibiting high fecundity and dispersal capabilities. This is especially true within biogeographic regions bounded by well-known hotspots of genetic differentiation. Here, we provide an overview of the current methods for estimating genetic connectivity using molecular markers and propose several directions for improving existing approaches using large population genomic datasets. We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples. We then focus on alternative methods based on markers influenced by selection. Although some of these methodologies are still underexplored, our aim was to stimulate new research to test how broadly they are applicable to nonmodel marine species. We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally. We finally present how neutral markers hitchhiking with selected loci can also provide information about connectivity patterns within apparently well-mixed biogeographic regions. We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

No MeSH data available.


Related in: MedlinePlus

The chromosomal signature of local selection acting on a de novo mutation in panmixia. We consider a two habitats Levene's model (Levene 1953) represented in the left box, with random mating (in the dotted circle) and random dispersal (arrows) across two habitats of equal size (rectangles). A new selected mutation (allele a, red star) appears in habitat 1 on a haplotype bearing rare neutral variants (in green) at variable recombination distances (the initial frequency is 1/2Ne). The selected mutation has symmetrical antagonistic effects on the fitness of genotypes with respect to habitat (Habitat 1: ωAA/ωAa = 0.5, ωaa/ωAa = 2; Habitat 2: ωAA/ωAa = 2, ωaa/ωAa = 0.5). At equilibrium, varying selection among genotypes and habitats results in differentiation between habitats at the selected locus (in this example Δp ≈ 0.3). During the progress toward equilibrium, neutral variants hitchhike with the selected allele, transiently producing a narrow chromosomal region where genetic differentiation is increased around the selected locus (green line). As the selected allele progressively recombines away from its haplotypic background, differentiation at neutral alleles rapidly vanishes (green arrows). After a few thousands of generations, differentiation is almost limited to the selected locus (dashed green line).
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fig02: The chromosomal signature of local selection acting on a de novo mutation in panmixia. We consider a two habitats Levene's model (Levene 1953) represented in the left box, with random mating (in the dotted circle) and random dispersal (arrows) across two habitats of equal size (rectangles). A new selected mutation (allele a, red star) appears in habitat 1 on a haplotype bearing rare neutral variants (in green) at variable recombination distances (the initial frequency is 1/2Ne). The selected mutation has symmetrical antagonistic effects on the fitness of genotypes with respect to habitat (Habitat 1: ωAA/ωAa = 0.5, ωaa/ωAa = 2; Habitat 2: ωAA/ωAa = 2, ωaa/ωAa = 0.5). At equilibrium, varying selection among genotypes and habitats results in differentiation between habitats at the selected locus (in this example Δp ≈ 0.3). During the progress toward equilibrium, neutral variants hitchhike with the selected allele, transiently producing a narrow chromosomal region where genetic differentiation is increased around the selected locus (green line). As the selected allele progressively recombines away from its haplotypic background, differentiation at neutral alleles rapidly vanishes (green arrows). After a few thousands of generations, differentiation is almost limited to the selected locus (dashed green line).

Mentions: We refer to local adaptation clines as monogenic clinal variation patterns maintained by a balance between the divergent effects of selection and the homogenizing effects of migration. Such clines occur along environmental gradients or at the frontier between habitats when alternative alleles have antagonistic fitness effects in different environmental conditions (Powers and Place 1978; Koehn et al. 1980). Allele frequencies vary as a sigmoid function of geographic distance (Box 3A) without necessarily reaching fixation if selection cannot purge the inflow of maladapted genotypes (Slatkin 1973). Local adaptation clines can be used to estimate dispersal distance (σ) if the selection coefficient (s) can be measured, which actually represents a serious challenge to most case studies. However, a measure of selection can sometimes be obtained using experimental populations or genotype frequency comparisons between larvae and adults sampled from the same cohort. By contrast, inferring dispersal from a neutral hitchhiker locus only requires the recombination rate with the selected locus (Box 3A). This can be more readily obtained by studying the signature left by selection in the chromosomal neighborhood of individual outlier loci. For instance, resequencing the region around outliers may help to determine which polymorphism is actually under selection (i.e. the one showing the highest FST value, surrounded by decreasing differentiation on both sides; Box 3A) and provides data to estimate local recombination rates around the selected locus without needing a recombination map (Stumpf and McVean 2003). The chromosomal signature left by local selection in high gene flow species is usually limited to very narrow regions, even when selection acts on de novo mutations (Fig. 2). Therefore, high-density genome scans are usually required for efficiently detecting local adaptation loci.


Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era.

Gagnaire PA, Broquet T, Aurelle D, Viard F, Souissi A, Bonhomme F, Arnaud-Haond S, Bierne N - Evol Appl (2015)

The chromosomal signature of local selection acting on a de novo mutation in panmixia. We consider a two habitats Levene's model (Levene 1953) represented in the left box, with random mating (in the dotted circle) and random dispersal (arrows) across two habitats of equal size (rectangles). A new selected mutation (allele a, red star) appears in habitat 1 on a haplotype bearing rare neutral variants (in green) at variable recombination distances (the initial frequency is 1/2Ne). The selected mutation has symmetrical antagonistic effects on the fitness of genotypes with respect to habitat (Habitat 1: ωAA/ωAa = 0.5, ωaa/ωAa = 2; Habitat 2: ωAA/ωAa = 2, ωaa/ωAa = 0.5). At equilibrium, varying selection among genotypes and habitats results in differentiation between habitats at the selected locus (in this example Δp ≈ 0.3). During the progress toward equilibrium, neutral variants hitchhike with the selected allele, transiently producing a narrow chromosomal region where genetic differentiation is increased around the selected locus (green line). As the selected allele progressively recombines away from its haplotypic background, differentiation at neutral alleles rapidly vanishes (green arrows). After a few thousands of generations, differentiation is almost limited to the selected locus (dashed green line).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4561567&req=5

fig02: The chromosomal signature of local selection acting on a de novo mutation in panmixia. We consider a two habitats Levene's model (Levene 1953) represented in the left box, with random mating (in the dotted circle) and random dispersal (arrows) across two habitats of equal size (rectangles). A new selected mutation (allele a, red star) appears in habitat 1 on a haplotype bearing rare neutral variants (in green) at variable recombination distances (the initial frequency is 1/2Ne). The selected mutation has symmetrical antagonistic effects on the fitness of genotypes with respect to habitat (Habitat 1: ωAA/ωAa = 0.5, ωaa/ωAa = 2; Habitat 2: ωAA/ωAa = 2, ωaa/ωAa = 0.5). At equilibrium, varying selection among genotypes and habitats results in differentiation between habitats at the selected locus (in this example Δp ≈ 0.3). During the progress toward equilibrium, neutral variants hitchhike with the selected allele, transiently producing a narrow chromosomal region where genetic differentiation is increased around the selected locus (green line). As the selected allele progressively recombines away from its haplotypic background, differentiation at neutral alleles rapidly vanishes (green arrows). After a few thousands of generations, differentiation is almost limited to the selected locus (dashed green line).
Mentions: We refer to local adaptation clines as monogenic clinal variation patterns maintained by a balance between the divergent effects of selection and the homogenizing effects of migration. Such clines occur along environmental gradients or at the frontier between habitats when alternative alleles have antagonistic fitness effects in different environmental conditions (Powers and Place 1978; Koehn et al. 1980). Allele frequencies vary as a sigmoid function of geographic distance (Box 3A) without necessarily reaching fixation if selection cannot purge the inflow of maladapted genotypes (Slatkin 1973). Local adaptation clines can be used to estimate dispersal distance (σ) if the selection coefficient (s) can be measured, which actually represents a serious challenge to most case studies. However, a measure of selection can sometimes be obtained using experimental populations or genotype frequency comparisons between larvae and adults sampled from the same cohort. By contrast, inferring dispersal from a neutral hitchhiker locus only requires the recombination rate with the selected locus (Box 3A). This can be more readily obtained by studying the signature left by selection in the chromosomal neighborhood of individual outlier loci. For instance, resequencing the region around outliers may help to determine which polymorphism is actually under selection (i.e. the one showing the highest FST value, surrounded by decreasing differentiation on both sides; Box 3A) and provides data to estimate local recombination rates around the selected locus without needing a recombination map (Stumpf and McVean 2003). The chromosomal signature left by local selection in high gene flow species is usually limited to very narrow regions, even when selection acts on de novo mutations (Fig. 2). Therefore, high-density genome scans are usually required for efficiently detecting local adaptation loci.

Bottom Line: We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples.We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally.We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

View Article: PubMed Central - PubMed

Affiliation: Université de Montpellier Montpellier, France ; CNRS - Institut des Sciences de l'Evolution, UMR 5554 UM-CNRS-IRD-EPHE, Station Méditerranéenne de l'Environnement Littoral Sète, France.

ABSTRACT
Estimating the rate of exchange of individuals among populations is a central concern to evolutionary ecology and its applications to conservation and management. For instance, the efficiency of protected areas in sustaining locally endangered populations and ecosystems depends on reserve network connectivity. The population genetics theory offers a powerful framework for estimating dispersal distances and migration rates from molecular data. In the marine realm, however, decades of molecular studies have met limited success in inferring genetic connectivity, due to the frequent lack of spatial genetic structure in species exhibiting high fecundity and dispersal capabilities. This is especially true within biogeographic regions bounded by well-known hotspots of genetic differentiation. Here, we provide an overview of the current methods for estimating genetic connectivity using molecular markers and propose several directions for improving existing approaches using large population genomic datasets. We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples. We then focus on alternative methods based on markers influenced by selection. Although some of these methodologies are still underexplored, our aim was to stimulate new research to test how broadly they are applicable to nonmodel marine species. We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally. We finally present how neutral markers hitchhiking with selected loci can also provide information about connectivity patterns within apparently well-mixed biogeographic regions. We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

No MeSH data available.


Related in: MedlinePlus